Bioinspired Polymer Systems with Stimuli ... - ACS Publications

Mar 24, 2017 - force−extension data for the control polymer (top, one single peak is observed) and the modular polymer (bottom, a sawtooth-like patt...
3 downloads 10 Views 46MB Size
Review Cite This: Chem. Rev. 2017, 117, 12851-12892

pubs.acs.org/CR

Bioinspired Polymer Systems with Stimuli-Responsive Mechanical Properties Lucas Montero de Espinosa, Worarin Meesorn, Dafni Moatsou,* and Christoph Weder* Adolphe Merkle Institute, University of Fribourg, Chemin des Verdiers 4, 1700 Fribourg, Switzerland ABSTRACT: Materials with switchable mechanical properties are widespread in living organisms and endow many species with traits that are essential for their survival. Many of the mechanically morphing materials systems found in nature are based on hierarchical structures, which are the basis for mechanical robustness and often also the key to responsive behavior. Many “operating principles” involve cascades of events that translate cues from the environment into changes of the overall structure and/or the connectivity of the constituting building blocks at various levels. These concepts permit dramatic property variations without significant compositional changes. Inspired by the function and the growing understanding of the operating principles at play in biological materials with the capability to change their mechanical properties, significant efforts have been made toward mimicking such architectures and functions in artificial materials. Research in this domain has rapidly grown in the last two decades and afforded many examples of bioinspired materials that are able to reversibly alter their stiffness, shape, porosity, density, or hardness upon remote stimulation. This review summarizes the state of research in this field.

CONTENTS 1. Introduction 2. Sea Cucumber-Inspired Stiffness-Changing Polymer Composites 2.1. Sea Cucumber Dermis As Model for Mechanically Morphing Composites 2.2. Water-Responsive Sea Cucumber Mimics 2.2.1. Stiffness-Changing Polymer Nanocomposites 2.2.2. Shape-Changing Polymer Nanocomposites 3. Complex Mechanical Properties Enabled by Reversible Sacrificial Bonds and Domains 3.1. Materials Inspired by the Modular Architecture of Titin 3.2. Materials Inspired by Silk 3.3. Materials Inspired by the Mussel Byssus 3.4. Materials Inspired by Resilin 3.5. Sacrificial Bonds and Domains in Other Nonbioinspired Mechanically Adaptive Materials 4. Plant-Inspired Actuating Polymers and Polymer Systems 4.1. Model Actuators in Plants 4.2. Actuation in Bilayer Structures 4.3. Actuation in Anisotropic Nanocomposites 4.4. Actuating Hydrogels Based on Compositional Drift 5. Conclusions and Outlook Author Information Corresponding Authors ORCID © 2017 American Chemical Society

Notes Biographies Acknowledgments References

12851 12852 12852 12852

12885 12885 12885 12885

1. INTRODUCTION Bioinspired design is a general approach in which biological principles are applied to develop new solutions in domains that traditionally have few connections with biology. The concept is seemingly universally applicable,1 as documented by examples that range from robotics to architecture to computing.2−4 In the physical and engineering sciences, researchers are in many cases drawn to biological models on account of unusual, attractive, and/or useful properties and functions, such as the ability of the Venus flytrap to rapidly capture their prey or the fascinating camouflaging effects that cephalopods achieve through changes in their body patterns.5,6 Developing an understanding of how molecules, materials, and/or complex systems contribute to such functions has become the goal of scientists working in different fields, as the interpretation of the underlying mechanisms is not only of biological interest but also paves the way for the development of materials that either replicate natural functions and/or exploit similar design approaches to impart such properties to synthetic materials.7,8 A particularly intriguing and useful aspect of many natural materials is their ability to change their physicochemical properties, either in response to an external stimulus or based upon cues created within the

12852 12856 12857 12858 12864 12866 12867

12868 12868 12869 12871 12875 12880 12884 12885 12885 12885

Special Issue: Bioinspired and Biomimetic Materials Received: March 24, 2017 Published: July 28, 2017 12851

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

However, for the benefit of the reader, general references were included where possible. While research of great significance has been carried out on the design of systems where mechanical changes are achieved through macroscopic or microscopic engineering approaches, this review focuses on examples in which the mechanical response is owed to an intrinsic materials’ propensity that is usually imparted by interactions on the molecular or the nanoscale. Likewise, we present selected examples of materials in which biological functions, such as actuation, are achieved with de novo designs. Notably, the concepts of intricate hydrogel and bilayer actuators, as well as liquid-crystal-based actuators are discussed at hand of instructive examples. The review has been organized according to the biological model and type of mechanical effect achieved. The natural materials whose structure, mechanically adaptive properties, and/or motility served as blueprint are usually first presented, followed by summaries of the corresponding synthetic approaches toward materials with similar structure and/or functions and a discussion of their properties.

organism, such as the passive opening of pine cones upon drying or the stiffening of sea cucumbers when threatened. The general idea to create stimuli-responsive or adaptive materials, whose properties can be influenced, ideally in a highly specific and predictable manner upon exposure to a predefined stimulus, is also increasingly exploited in artificial materials which, on account of some analogies to living matter, are sometimes referred to as “smart” or “intelligent”.9−11 Materials that are able to alter their mechanical properties on command represent a subset of this vast family. Indeed, mechanically morphing or adaptive materials and systems are attracting great interest both in the biological domain, where the research emphasis lies on developing a better understanding of the way natural mechanisms allow survival of organisms that take advantage of mechanical morphing for key functions, as well as materials chemistry, where the main driver is their potential usefulness in applications that range from active dampening systems to soft robotics.12,13 Many examples of artificial materials that were designed to mimic the mechanical morphing effects seen in biological materials have been reported in the literature. To achieve such effects, researchers have exploited mechanisms that range from simple plasticization of polymers to sophisticated shape-memory mechanisms, supramolecular switches, and actuators. Plasticization [i.e., the effect of reducing a material’s stiffness by introducing a softening component (or plasticizer)] is at play in many natural materials. The effect is prominent in hemicelluloses, where the effective reduction of the Young’s modulus can be as significant as 3 orders of magnitude when such tissues are transferred from dry to humid conditions.14 Another widely used factor to control stiffness is the cross-linking of macromolecules, which transforms them into networks that can display mechanical properties that differ vastly from those of the linear parents. This phenomenon can be found in plant cells, which alter their mechanical properties as a secondary result of changes in the plant’s tissue porosity, which in turn is achieved by reversible cross-linking though borate chemistry.15,16 The mechanical properties of tissues in organisms have also been shown to depend on the manner in which the components are organized. A prime example for the power of hierarchical organization, although not in the context of adaptive materials, is the abalone shell nacre, where six structural levels of different scales (from ca. 30 nm up to 0.5 μm) contribute to the extremely high stiffness of this layered material.17,18 It is instructive that most of the mechanically adaptive materials found in nature rely on simple (but clever) mechanisms and are based on a rather small set of nonhazardous building blocks made from abundant elements.19,20 The striking similarity of the components in natural systems that however achieve different and complex functions are indicative of the fact that hierarchical structuring and modulation of interactions between these components are the key elements to replicating mechanical morphing.21 This article seeks to complement many excellent recent reviews on the general subject of bioinspired materials design and the specific topic of mechanically adaptive materials,22−24 respectively, by providing a comprehensive summary of the current knowledge in the narrowly defined domain of bioinspired mechanically morphing polymer-based materials. Given that inspiration, like beauty, lies usually in the eyes of the beholder, this review has been limited to papers in which the authors have clearly indicated that their materials design was inspired by nature. While in many cases similar materials have emerged from bioinspired or de novo design, a detailed discussion of materials based on the latter approach is outside the scope of this review.

2. SEA CUCUMBER-INSPIRED STIFFNESS-CHANGING POLYMER COMPOSITES 2.1. Sea Cucumber Dermis As Model for Mechanically Morphing Composites

Many marine animals, especially in the phylum Echinodermata, have the ability to rapidly and reversibly alter the stiffness of their dermis-forming tissue. A prominent example of a species that utilizes this mechanical morphing as a defense mechanism against predators is the sea cucumber, an echinoderm from the class holothuroidea. The structure of the dermis of these creatures can be described as a hierarchical composite structure that consists of rigid, high-aspect ratio collagen fibrils that are embedded in a much softer, viscoelastic hydrogel matrix.25 The animal controls the stiffness of its skin primarily by regulating the interactions among adjacent collagen fibrils (Figure 1)26 and therewith the stress transfer ability among them. The collagen fibrils are mechanically disconnected from each other in the idle (low-modulus) state, but they can be bridged on command to form a load-bearing network, which is concomitant with a significant stiffness increase.27−30 The glycoprotein stiparin, located in the extracellular matrix, has been identified as the stiffening agent that causes the rapid aggregation of collagen fibrils.27−32 Ex vivo experiments demonstrated that the local secretion of stiparin triggers the formation of a percolating network with the concomitant increase of the elastic modulus of the tissue up to an order of magnitude (i.e. from ca. 5 to ca. 50 MPa).29 It was also discovered on the basis of in vivo experiments that another protein, tensilin, assists stiparin in inducing the aggregation of collagen fibrils.33,34 The mechanical properties of the stiffened tissue can be converted back to the original soft state with the help of a stiparin inhibitor (i.e., another glycoprotein that can bind to stiparin and reverse the aggregation of collagen fibrils). While some aspects of the specific biochemistry at play in the sea cucumber have yet to be fully understood, the general mechanism is well-understood and has been successfully adapted in chemo-responsive mechanically adaptive nanocomposites.35 2.2. Water-Responsive Sea Cucumber Mimics

2.2.1. Stiffness-Changing Polymer Nanocomposites. Rowan, Weder, and co-workers developed the first mechanically adaptive materials inspired by the skin of the sea cucumber.35 In order to reproduce the structure of this composite-like material, the authors introduced tunicate-sourced cellulose nanocrystals 12852

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 2. Pictures (top) and schematic (bottom) illustrating the waterinduced switching of the mechanical properties of a PVAc/CNC nanocomposite film. The dry object can penetrate a brain-mimicking gel easily (top left) but buckles when wet (top right). This behavior is the result of hydrogen bonding of water molecules with the hydroxyl groups present on the surface of the CNCs, which disrupts CNC−CNC interactions and therewith the reinforcing CNC network. Top: Reproduced from ref 48. Copyright 2010 American Chemical Society. Bottom: Reproduced with permission from ref 24. Copyright 2017 The Royal Society of Chemistry.

Figure 1. Pictures of a sea cucumber in its relaxed, soft state (top left) and its stiff state when threatened (top right). Schematic representation of the underlying mechanism whereby the collagen fibers are disconnected in the soft dermis (bottom left) and are connected when the glycoproteins stiparin and tensilin are released (bottom right). Top: Reproduced with permission from ref 35. Copyright 2008 American Association for the Advancement of Science.

(t-CNCs) into a rubbery poly(ethylene oxide-co-epichlorohydrin) (EO-EPI) matrix. On account of their high aspect ratio, strength, and stiffness, and their emerging commercial accessibility, CNCs have become a widely used building block for the design of nanocomposites.36,37 The abundance of surface hydroxyl groups render CNCs an interesting component of adaptive nanocomposites, based on the idea that hydrogen bonds between these elements could be switched on or off with the help of a chemical regulator. The EO-EPI copolymer was originally selected because of its low modulus and moderate water uptake, and the expectation that no pronounced specific interactions with the CNCs would occur. EO-EPI/t-CNC nanocomposites with a t-CNC content above the percolation concentration exhibit a dramatic stiffness increase in comparison to the unfilled EO-EPI matrix. For instance, the introduction of 19% v/v tCNCs caused a 200-fold increase of the tensile storage modulus (E′) from ca. 4 to 800 MPa. The results mirror earlier studies by Chanzy and co-workers on the mechanical properties of nanocomposites of t-CNCs and polymer latexes,38 as well as many subsequently studied systems39−41 with various CNC types and polymers. Indeed, the significant mechanical reinforcement can be explained with the formation of a percolating network of CNCs in the polymer matrix, which is formed at CNC concentrations above the percolation threshold. The mechanical characteristics of these nanocomposites are well described by mechanical models based on percolation theory. On the basis of the assumption that above the percolation threshold the stress transfer in these nanocomposites relies on CNC− CNC hydrogen bonding involving the surface hydroxyl groups, the stimuli-responsiveness of these materials was investigated by exposing them to water, which was thought to form competitive hydrogen bonds with the CNCs and serve to reduce the nanocomposite’s stiffness (Figure 2). This mechanism is reminiscent of that of the sea cucumber (Figure 1). Indeed,

moderate water uptake (30% w/w) caused a significant decrease of E′ to ca. 20 MPa. Reference experiments with isopropanol, which swelled EO-EPI to a similar extent as water but did not change the stiffness of the nanocomposites, suggest that the softening is indeed associated with the disconnection of the CNC-network. As expected, this effect was found to be reversible upon drying. Thus, EO-EPI/t-CNC nanocomposites successfully mimic, albeit in a very simplified manner, the mechanically adaptive behavior of the skin of sea cucumbers. Poly(vinyl acetate) (PVAc)/t-CNC nanocomposites displayed similar adaptive behavior upon exposure to water, but a higher stiffness and an even larger mechanical contrast could be achieved. In the dry state, the CNCs form a reinforcing percolating network and cause a slight increase of the glass transition temperature (Tg) of the PVAc matrix to ca. 46 °C so that at ambient or physiological temperature the matrix polymer is in a glassy state. As a result, the nanocomposites display a very high stiffness. For instance, a composition with 16.5% v/v t-CNCs displays an E′ of 5.1 GPa at 25 °C, which remains virtually constant up to 37 °C. Heating the dry material to 56 °C (i.e., above Tg) caused E′ to drop to 814 MPa, whereas swelling this material with water produced a much more pronounced decrease of E′ to 10.8 MPa (Figure 3). These data show how different stimuli switch the different elements that contribute to the materials’ overall stiffness. Heating to above Tg transforms the PVAc matrix from a glassy to a rubbery state but leaves the CNC network largely intact, whereas upon aqueous swelling, the polymer is plasticized (Tg is reduced to ca. 21 °C) and the CNC−CNC interactions are decoupled. With biomedical applications in mind where mechanical adaptation is either desirable or a must, in particular intracortical implants, which benefit from materials that are sufficiently rigid to allow insertion but rapidly soften upon exposure to (emulated) 12853

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

PVAc alone. Upon immersion in ACSF at 37 °C, the E′ of a PBMA/t-CNC nanocomposite containing 15% v/v t-CNCs dropped from ca. 4 GPa to ca. 1 GPa, which represents a much smaller stiffness change than observed for a PVAc/CNC nanocomposite discussed above.46 This pronounced difference is directly related to the fact that in the case of the PBMA-based nanocomposite, the more hydrophobic nature of the matrix limited the ACSF take-up to 15%. This caused only a minor Tg reduction from 70 to 50 °C, so that at ambient or physiological temperatures, the matrix is still in a glassy state. When the PBMA/t-CNC nanocomposite was exposed to ACSF at 65 °C (i.e., close to the Tg), a higher uptake of ACSF (80%) and a more pronounced decrease of the wet modulus (163 MPa vs 1 GPa) were observed. The influences of the matrix polarity and the Tg on the adaptive behavior of such nanocomposites were further explored by investigating a series of t-CNCs-based nanocomposites with blends of PBMA and PVAc. The data revealed that the wet modulus can be readily tuned across a relatively wide range via merely changing the PBMA/PVAc ratio. Styrene−butadiene rubber (SBR) and polybutadiene (PBD) were also employed to investigate the effect of polymer matrix polarity on the water permeability of these mechanically adaptive materials.49 To be able to form percolating CNC networks within these highly hydrophobic polymer matrices, t-CNC-based nanocomposites were fabricated using a template approach,50 whereby a t-CNC/acetone organogel was placed in a tetrahydrofuran (THF) solution of SBR or PBD and thus imbibed with a polymer solution via solvent-exchange before drying. Dynamic mechanical analyses of the resulting nanocomposites showed that E′ increased by more than 3 orders of magnitude from about one to a few hundred MPa upon introduction of 17−20% v/v t-CNCs. Significant softening was observed after exposure to water (e.g., from ca. 236 MPa to ca. 39 MPa for SBR containing 17% v/v t-CNCs), although the process was slower than in the case of nanocomposites with more polar matrices and required several days.35,46 The data show strikingly that within hydrophobic matrices, the polar CNC networks can serve as hydrophilic channels through which water can diffuse and that the extent of water uptake depends on the CNC content. The effect of the processing method on the level of reinforcement and mechanical properties of such nanocomposites was further investigated by incorporating 20% v/v c-CNC into SBR.51 The largest mechanical contrast was found for the solvent-cast samples, where E′ decreased from ca. 740 MPa to ca. 6 MPa when immersed in water. The SBR matrix has a low Tg and a comparable E′ as EO-EPI and the level of reinforcement induced by CNC introduction and water-induced softening are comparable, even though matrix chemistry and processing method were entirely different. However, the SBR-based composites display a much slower response, on account of their hydrophobic character. This underlines how important ultimately the polymer matrix chemistry is for the properties of these materials. The Weder group further explored mechanically adaptive nanocomposites based on poly(vinyl alcohol) (PVA) as the matrix and t-CNCs or c-CNCs as the filler, based on the assumption that a polar glassy polymer that would form hydrogen bonds with the CNCs would afford in stiffer nanocomposites.52 Indeed, dynamic mechanical analysis (DMA) data reveal a significant increase of E′ upon introduction of CNCs, which depended on the CNC type and content. Exposing these nanocomposites to emulated physiological conditions caused a very pronounced softening, from 9.0 GPa

Figure 3. Tensile storage moduli of PVAc/t-CNC nanocomposites as a function of t-CNC content in the dry state (■) and swollen with ACSF (□). Lines represent values predicted by the Halpin Kardos (dashed) and the percolation (solid) model. Reproduced with permission from ref 46. Copyright 2010 Elsevier Ltd.

physiological conditions and thus reduce the inflammatory response of the surrounding tissue (Figure 2-top),42−45 the authors explored the materials’ responses upon immersion into artificial cerebrospinal fluid (ACSF) at physiological temperature, which caused the reduction of E′ from ca. 4.4 GPa (dry, 37 °C) to 60 MPa within minutes and reduced further over time.46 Swelling of these materials upon exposure to water or ACSF was, however, significant (up to 70% w/w). With cortical interface applications in mind, the same team sought to decrease the swelling and the “soft state” modulus to better match the mechanical characteristics of the brain tissue and explored cotton as an alternative, more accessible CNCs source (c-CNCs).47 A PVAc/c-CNC nanocomposite with 16.5% v/v c-CNCs showed a room-temperature tensile storage modulus of ca. 4 GPa below Tg, which is quite close to the value of the corresponding nanocomposite made with t-CNCs (ca. 5 GPa). On the other hand, the reinforcement above Tg (ca. 45 MPa at 82 °C) was much less pronounced than for the tCNC-based nanocomposites (ca. 600 MPa at the same temperature). This reinforcing effect can be explained by the higher aspect ratio of t-CNCs compared to c-CNCs, which allows them maintaining an interconnected network within lowstiffness polymeric matrices (i.e., above Tg). When immersed in ACSF, the PVAc/c-CNC nanocomposite showed a degree of swelling of only 28%, which is much lower than for the previously studied PVAc/t-CNC system. This difference was explained on the basis of the higher density of surface sulfate groups displayed by t-CNCs, which are introduced during their sulfuric acidmediated isolation process and increase the water affinity of CNCs. Indeed, the concentration of surface sulfate groups depends on the CNC-type and isolation process and can lead to the observed water uptake differences. However, while c-CNCs promote a much lower water uptake, the wet-state moduli of the PVAc/c-CNC (5 MPa) and PVAc/t-CNC (12 MPa) nanocomposites are very similar. To develop a better understanding of the role of the polymer matrix and its influence on the adaptive properties of nanocomposites with CNCs, Rowan, Weder, and co-workers further investigated t-CNC-based nanocomposites with poly(butyl methacrylate) (PBMA) and blends of this polymer with PVAc.48 PBMA was used as a hydrophobic matrix to reduce the extent of aqueous swelling vis-à-vis nanocomposites made with 12854

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

to 1 MPa in the case of the composite containing c-CNCs and from 13.7 GPa to 160 MPa for the material made with t-CNCs (16% v/v). The authors showed further that the extent of swelling and thereby the magnitude of the mechanical switching could be influenced via the amount and type of CNCs and the introduction of cross-links between the PVA molecules. The PVA/CNC composites investigated exhibit the largest mechanical contrast of all sea-cucumber inspired nanocomposites reported to date. It is also clear that in these specific materials, in addition to CNC−CNC interactions, pronounced polymer− CNC interactions, which are promoted by the strong propensity of PVA to form hydrogen bonds, must be at play or even dominant. Thus, in these particular nanocomposites the waterinduced switching likely involves the mitigation of polymer− CNC interactions. One can extend this thought and speculate that this mechanism may also contribute to the switching of other materials discussed in this section, at a level that should depend on the matrix polymers’ ability to interact with the CNCs. The sea-cucumber approach has been used to develop other mechanically adaptive CNC-based nanocomposites. For instance, chitin-derived nanocrystals have been used to render a low modulus carboxylated SBR water-responsive,53 and in another example, the introduction of CNCs functionalized with either amino or carboxylic acid groups into PVAc was found to yield pH-responsive mechanically adaptive nanocomposites.54 In this latter study, Way et al. showed that the surface chemistry of the CNCs can be modified through the introduction of carboxylic acid or amine groups, which are both pH-responsive moieties. Thus, aminated CNCs readily dispersed in water at low pH values, due to the electrostatic repulsions between charged amine groups, but formed gels at high pH (Figure 4). The carboxylic acid-functionalized CNCs on the other hand were observed to disperse in water at high pH values and form gels at low pH values. Once introduced in a polymer matrix, the interactions between CNCs could be thus switched on and off by swelling the nanocomposites with water at specific pH values, which was used to reversibly alter their mechanical properties. Differing from previous studies in which water was used as a trigger, this work represents a first step toward achieving higher specificity for the mechanical switching of CNC-based polymer nanocomposites. In another study, Korley and co-workers took the concept of water transportation through hydrophilic channels a step further by incorporating electrospun PVA mats as filler into PVAc or EO-EPI matrices. The authors observed a reduction of the modulus of these materials upon exposure to water;55,56 however, unlike in the case of the sea cucumber or the CNC/polymer nanocomposite mimics discussed above, where mechanical switching is achieved by changing the interactions among reinforcing nano- or micro fillers, the mechanical switching of these materials is caused by changing the properties of the filler itself. In the case of the PVA-based nanofibers, the uptake of water was reported to induce plasticization and crystallinity changes. Inspired by the structure of plant cell walls, which contain rigid cellulose nanofibers connected by soft polymeric hemicellulose chains, Kontturi, Ikkala, and co-workers designed and prepared thermoresponsive nanocomposite hydrogels based on CNCs.57 In these materials, the CNCs were bound together with methylcellulose (MC). Keeping the MC content constant at a level of 1.0% w/w, the authors showed that E′ can be tuned by increasing the CNC content, which was varied from 0 to 3.5% w/ w. The mechanical properties of these MC/CNC hydrogels were found to strongly depend on the temperature; for instance, when

Figure 4. Schematic representation of the proposed mechanism for pHresponsive nanocomposites containing functionalized CNCs with carboxylic acid or amine (top) and the interactions between functionalized CNCs at different pH conditions (bottom). Reproduced from ref 54. Copyright 2012 American Chemical Society.

the MC/CNC hydrogel with 3.5% w/w CNCs was heated from 20 to 60 °C, the E′ raised from 75 to 900 Pa, further increased to 2200 Pa upon heating to 75 °C, and recovered its original mechanical properties when cooled back to 20 °C. This temperature-responsive behavior had already been observed in aqueous MC solutions, although the mechanism of this sol−gel transition is still a subject of research.58 It has been proposed that MC loses its affinity toward water upon heating, which in turn causes its aggregation into fibrils that eventually lead to gelation.59 The introduction of CNCs into MC gels thus expands the property matrix of this class of temperature responsive gels by adding tunability at the mechanical property level. Much like sea-cucumber inspired materials, another example of a stimuli-responsive material that changes its mechanical properties was reported to mimic nacre. Among all composite materials found in nature, nacre is one of the strongest and most resilient.60,61 The outstanding mechanical properties of nacre originate in its particular layered structure, which features aragonite microplatelets that are separated by protein-covered βchitin layers. The presence of the chitin phase confers nacre with a fracture resistance that is about 3000-fold higher than that of the neat aragonite.62 The impressive influence of the soft phase on the properties of nacre and nacre-inspired materials can in principle be exploited to access materials with a wide range of properties. An illustrative example is found in a recent publication by Barner-Kowollik, Walther, and co-workers, who synthesized a nacre mimic containing a “switchable” soft binder phase in which ureidopyrimidinone (UPy) dimers served as supramolecular cross-links and thermally reduced graphene 12855

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

models to develop reversible molecular switches. Among them, moisture-responsive materials are key elements of many biological processes, such as the release of seeds and spores (c.f. section 4.1). Water is a readily available and safe switching agent and can be a particularly useful trigger in biomedical applications. Building on the adaptive mechanical properties of seacucumber-inspired polymer nanocomposites (c.f. section 2.2), Foster, Weder, and co-workers investigated the shape memory property of a series of nanocomposites based on a thermoplastic polyurethane elastomer [based on poly(tetramethylene glycol), butanediol, and 4,4′-methylenebis(phenyl isocyanate)] and cellulose nanocrystals (CNCs), with CNC contents of between 2 and 20% v/v (Figure 6a).67 The introduction of CNCs caused a

oxide (RGO) was embedded as a light-to-heat converter (Figure 5).63 The mechanical properties of this nacre mimic could be

Figure 5. Schematic illustrating the nacre-mimetic nanocomposite with hierarchical coassembly of synthetic clay, reduced graphene oxide, and copolymer-containing UPy motifs. Adapted from ref 63. Copyright 2016 American Chemical Society.

reversibly modulated via the application of near-infrared (NIR) light; the introduction of 1% w/w RGO was sufficient to increase the temperature up to the dissociation temperature of the UPy dimers, which caused a considerable softening of the binder and an increase of the strain at break (from 1.3% to 4.0%). It was also found that the material adapted its mechanical performance to the light flux in a dynamic way. This work provides an apparently versatile approach to add mechanical adaptiveness to the property matrix of highly stiff materials. 2.2.2. Shape-Changing Polymer Nanocomposites. The switching principle at play in the sea-cucumber skin has also been exploited to create shape-memory nanocomposites. These materials form part of an ever-growing family polymer systems that are capable of adopting one or more temporary shapes while remembering their permanent shape, to which they can recover when exposed to a specific external stimulus.64,65 Shape-memory characteristics can be imparted to polymers by combining rubber elasticity with a switching element that can be stimulated to enable (during shape programming and recovery) or prevent (to fix the temporary shape) elastic deformation. Rubber elasticity is typically achieved through a network structure involving covalent or physical cross-links, whereas reversible covalent or noncovalent bonds or a phase transition in the polymer can be used as the switching element. The stimulus used for fixing and releasing the temporary shape will thus depend on the choice of the latter. Most shape memory polymers studied so far respond to a change in temperature, but many alternative switching schemes have been developed where the shape memory effect is driven by exposure to light, chemicals, or other stimuli.66 Although the development of the first shape-memory polymers was not motivated by biological systems, material scientists have found inspiration in many mechanically adaptive biological

Figure 6. (a) Schematic representation of the shape memory concept in polymer/CNC nanocomposites, which relies on the disconnection and reformation of CNC−CNC interactions by addition and removal of water. (b) Series of pictures that demonstrate the shape memory property of a polymer/CNC nanocomposite: a self-propelled artificial fishing lure that is activated under water. Reproduced from ref 67. Copyright 2011 American Chemical Society.

stiffness increase, which matched the predictions of the HalpinKardos model below, and a percolation model above the CNC percolation threshold concentration. At the maximum CNC concentration of 20% v/v CNCs, a storage modulus of ca. 1 GPa was observed, which is almost 2 orders of magnitude higher than that of the neat polyurethane. Exposing the nanocomposites with a CNC content above the percolation threshold to deionized water resulted in a significant stiffness decrease (c.f. section 2.2). On the other hand, the effect of water on the stiffness of the nanocomposites with CNC contents below the percolation threshold was marginal, which is in agreement with the proposed role of water as competitive hydrogen bonding binder that disrupts the reinforcing hydrogen-bonded CNC network. Drying the composites restored their original stiffness, and the process was shown to be reproducible in cyclic wetting/dewetting tests. The ability to reversibly interrupt hydrogen bond based CNC− 12856

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

CNC interactions in these nanocomposites provides the basis for a water-triggered shape memory effect, which was investigated by swelling samples with water, deforming them into a temporary shape, and drying the samples in the deformed state to restore CNC−CNC interactions and fixate the temporary shape. The performance of shape memory materials is measured by two characteristic parameters, the shape fixity ratio Rf, which measures the ability of the system to retain the temporary shape, and the shape recovery ratio Rr, which expresses the ability of the system to recover the permanent shape. Unlike a sample of the neat polyurethane, which showed poor shape fixation under the same conditions (fixity rate of 13%), the nanocomposites with 10% and 20% v/v CNCs displayed significantly higher fixity rates of 61% and 74%, respectively. Rewetting the samples disrupted the CNC network and allowed the systems to relax to the original shape, driven by the elasticity of the polyurethane matrix (Figure 6b). Despite the typical hysteresis characteristic of polyurethane-based shape-memory polymers, the nanocomposites with 10% and 20% v/v CNCs showed reasonable recovery rates of 44% and 55%, respectively. On the other hand, the neat polyurethane did not appreciably change its shape (recovery rate of 1.6%). A very similar study of polyurethane/CNC nanocomposites was reported by Hu and co-workers,68 who showed that the time required for swelling and drying could be considerably reduced by conducting the swelling and drying steps at 75 °C instead of 37 °C. The water-induced shape memory effect of polymer/CNC nanocomposites was also investigated by Chen and co-workers, who employed poly(glycerol sebacate urethane) (PGSU) as a hydrophobic polymer matrix.69 Unlike in the previous study, the CNCs and the polymer matrix were covalently cross-linked using hexamethyl diisocyanate (Figure 7a). The introduction of CNCs produced the expected increase of stiffness and water responsiveness on account of the percolating CNCs network. The shape-memory properties of nanocomposites containing between 9.3% and 29% w/w CNCs were investigated using distilled water and phosphate buffer saline (PBS) as triggers. Both the fixity and recovery rates were observed to increase during the first three shape memory cycles and then leveled off at values of up to 98% and 99%, respectively (Figure 7b). A similar shape memory behavior was observed with water and PBS, and the best results were obtained with the highest CNC content (Figure 7, panels b and c). On the other hand, no shape memory effect was observed when the neat polymer matrix was studied under the same conditions. These results are in agreement with the previous works discussed above and support the role of the CNCs network in water transportation through the polymer matrix. In addition to the shape memory property, the CNC nanocomposites were shown to be enzymatically degradable, which according to the authors opens the way to their application in minimally invasive medical devices. The underlying mechanism of the sea cucumber’s mechanical adaptation has served as inspiration for many synthetic nanocomposites which, through simplified approaches, achieve comparable mechanical switching. So far, such artificial systems rely exclusively on external stimuli, which renders them strongly dependent on the transport kinetics of the switching agents in/ out of the system and results in a slow response compared to the biological model. To overcome this limitation, future efforts should be focused on designing systems in which the switching agent is released internally in response to an external stimulus. Additionally, recent studies show that the picture described by these studies, in which stress-transfer is assumed to take place

Figure 7. (a) Chemical structure of PGSU and the PGSU-CNC crosslinking points. (b) Shape-memory properties (fixity Rf and recovery Rr ratios as a function on the shape memory cycle) of PGSU−CNC nanocomposites with PBS (pH = 7.4, 37 °C) as the stimulus. (c) Sequence of images showing the shape memory property of the PGSU− CNC nanocomposite with 29% w/w CNCs: (a) sample in its original shape immersed in water for 1 h, (b) sample in its fixed temporary shape after drying for 4 h at ambient, and two moments of the shape recovery process as the sample was (c, d) immersed in water and (e) the recovered sample. Reproduced from ref 69. Copyright 2014 American Chemical Society.

primarily on the basis of filler−filler interactions, is likely an oversimplified version of the actual mechanism. Filler−matrix interactions may indeed play an important role, especially in cases where polymer matrices capable of interacting with CNCs through, for example, hydrogen bonding, are used.

3. COMPLEX MECHANICAL PROPERTIES ENABLED BY REVERSIBLE SACRIFICIAL BONDS AND DOMAINS While high strength and high toughness proved difficult to combine in synthetic polymers,70 nature has created a plethora of 12857

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 8. (a) Original (folded) structure of the protein titin. (b) Snapshots of the structure of titin at different points of the stress induced unfolding process. (c) Sawtooth-like force−extension profile (purple) of titin showing the sequential unfolding of its macrodomains. Reproduced with permission from ref 74. Copyright 2010 National Academy of Sciences.

3.1. Materials Inspired by the Modular Architecture of Titin

materials with mechanical properties that have yet to be matched with synthetic mimics, including, for example, silk,71 nacre,72 connective proteins,73,74 or bone.75 These materials share as a common feature a hierarchical nanostructure in which interconnected soft and hard phases provide at the same time strength and toughness. Detailed structural and single-molecule mechanical analyses have shown that the exceptionally high capacity of these materials to dissipate mechanical energy originates not only in their particular microstructure but also in the presence of weak and reversible interactions, which act as energy-absorbing sacrificial bonds.75−80 Different hierarchical types of such weak points have been identified in biological materials, ranging from the hydrogen bonds across peptide sequences to β-sheet structures that unfold under mechanical stress.70 These structural features provide biopolymers with mechanisms that allow for the dissipation of energy when subjected to a mechanical force. Importantly, the underlying processes are reversible, and the materials’ structure and properties are changed in a dynamic manner as a function of the induced stress. In this section, different bioinspired approaches used to introduce reversible sacrificial bonds into synthetic polymers as a means to enhance their mechanical properties and render them adaptive, as well as to provide them with shape memory, are discussed. The emphasis has been placed on studies with a direct connection to a biological model, but several nonbioinspired systems in which reversible interactions serve the same purpose are also included. Studies whose focus was simply the mechanical strengthening of a polymer but in which no dynamic recovery was demonstrated and approaches in which nonreversible sacrificial bonds were used are intentionally excluded, as unlike biological systems, these materials show a stress-response that is a priori irreversible. Readers with an interest in such systems should refer to excellent reports and reviews focused on this topic.81−84

One of the most studied connective proteins is titin, which is found in the human skeletal muscle and is responsible for its passive elasticity. The structure of titin consists of a sequence of protein domains that are connected through unstructured peptide segments and reversibly unfold to absorb energy when the muscle is stretched (Figure 8).74,76 Guan and co-workers reported a combined theoretical and experimental (singlemolecule force) study on the mechanisms underlying the mechanical properties of such domain-based proteins74 and investigated the role of their hydrophobic core in the shielding of the load-bearing regions against water. It was found that the exclusion of water in such regions has a direct impact on the protein toughness, as it extends the lifetime of hydrogen bonds significantly. On the basis of the understanding of the mechanisms at play in the natural model, the Guan group pioneered the development of titin-inspired polymers, originally with the aim of pushing the mechanical properties of synthetic polymers toward those of sophisticated biopolymer systems. In a seminal paper, the group synthesized a polyurethane containing ureidopyrimidinone (UPy) units within the backbone through the polymerization of a UPy derivative containing two hydroxyl groups in the presence of an oligomeric diisocyanate (number-average molecular weight, Mn = 1400 g/mol) (Figure 9, panels a and b).85 The resulting “modular” polyurethane (Mn = 70 000 g/ mol) could, on account of UPy dimerization, form intra- or interchain loops that would respond to mechanical stress in a similar fashion as the folded domains of titin. A “control” polymer was also prepared using a protected UPy derivative (unable of dimerizing) in the synthesis of the polyurethane. Initial studies were directed to probe the mechanical properties of single polymer chains using atomic force microscopy (AFM). The single-chain force−extension curve of the control polymer shows a single peak, which is characteristic of the extension of a 12858

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 9. Synthesis of (a) the UPy-based monomer and (b) the UPy-containing modular polymer and the control polymer. (c) AFM single-chain force−extension data for the control polymer (top, one single peak is observed) and the modular polymer (bottom, a sawtooth-like pattern is observed) where the points are experimental data and the lines are the result of a WLC (wormlike chain model) fitting. (d) Stress−strain curves of the modular and control polymers and a nonfunctionalized polyurethane; the inset shows a cyclic stress−strain curve of the modular polymer evidencing hysteresis. Reproduced from ref 85. Copyright 2004 American Chemical Society.

with hydrocarbon chains. Unlike in the previous system, random dimerization is minimized thanks to the presence of two closing hydrocarbon loops, which maximize in-chain hydrogen bonding. Indeed, the single-chain force−extension curve obtained by AFM shows a more uniform pattern than the one observed for the UPy system, and the force required to unfold each module was considerably lower (ca. 50 pN vs. ca. 150 pN), reflecting a binding strength difference between the two supramolecular motifs utilized (ca. 107 vs ca. 104 M−1). As in the previous system, the increase of the contour length was not constant, which was ascribed to the formation of tertiary structures through π−π stacking of the phenyl rings of the hydrogen bonding duplex. The titin-inspired toughening strategy was subsequently adapted by Guan and co-workers to enhance the mechanical properties of a cross-linked polymer system.87 To this end, the researchers synthesized a dimethacrylate monomer consisting of a UPy dimer locked with two hydrocarbon loops (Figure 11a). This monomer was then copolymerized with n-butyl acrylate in the presence of a radical initiator to obtain a series of transparent rubbery networks with UPy contents of 2−6 mol % (Figure 11a). In addition, control polymer networks were prepared using 2−6 mol % of poly(ethylene glycol) dimethacrylate (Mn = 750 g/ mol) as cross-linker, and the mechanical properties of all compositions were evaluated by DMA and tensile tests (Figure 11b). As expected, the control networks showed an increase of tensile strength (from 0.52 to 0.63 MPa) and modulus (from 1.2 to 3.8 MPa) together with a decrease of extensibility (from 0.59 to 0.19 mm/mm) as the cross-linker content was increased. On the other hand, increasing the cross-linker content in the UPybased networks produced an increase of the tensile strength (from 0.95 to 4.5 MPa) and modulus (from 1.6 to 5.6 MPa)

random coil chain (Figure 9c, top). By contrast, the trace of the UPy-functionalized polyurethane shows a distinct sawtooth pattern similar to that observed for titin (Figure 9c, bottom).76,77 Tensile tests were then performed with films produced from both materials (polyurethanes with free and protected UPy units, respectively) as well as with a “reference” polyurethane containing neither free nor protected UPy groups (Figure 9d). The polyurethane containing protected UPy units showed increased toughness and stiffness compared to the neat polyurethane, arguably due to π−π stacking and residual hydrogen bonding between the protected UPy groups. The introduction of free UPy units produced a remarkable increase of toughness to the point that the sample did not yield at the limit of the equipment used (60 MPa). Furthermore, large hysteresis was observed when the UPy-functionalized polyurethane was subjected to two consecutive stress−strain cycles (Figure 9d, inset), indicating great energy dissipation through the dissociation of UPy dimers. Overall, these results confirmed the role of sacrificial bonds on the exceptional mechanical properties observed for the UPy-functionalized polyurethane. A subsequent study from the same group addressed the main limitations found in the original system, namely, the nonuniform structure of the polymer and the uncontrolled UPy dimerization, which could take place both intra- and interchain.86 A titin-like polymer system with well-defined loops (synthesized by the ringclosing olefin metathesis of a preassembled hydrogen-bonded motif, Figure 10a) was thus synthesized via the polymerization of a peptidomimetic β-sheet motif bearing two hydroxyl groups and 4,4′-methylenebis(phenyl isocyanate) (MDI) (Figure 10b). The resulting polyurethane (Mn = 89 000 g/mol) displays in-chain loops formed by β-sheet-like duplexes connected at both ends 12859

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 10. (a) Synthesis of a peptidomimetic β-sheet motif by ringclosing metathesis of a preassembled olefinic precursor. (b) Chemical structure of the polyurethane obtained by reaction of the ring-closed peptidomimetic β-sheet motif with 4,4′-methylenebis(phenyl isocyanate). Reproduced from ref 86. Copyright 2004 American Chemical Society.

Figure 11. (a) Schematic representation of a titin-inspired polymer network displaying UPy-based modular cross-linking sites. (b) Stress− strain curves of a control polymer network made with poly(ethylene glycol) dimethacrylate as cross-linker (black line) and the modular polymer network made with UPy dimer motifs as cross-linker (blue line). Reproduced from ref 87. Copyright 2007 American Chemical Society.

without compromising the extensibility. These observations are in accordance with the results discussed above and can be explained on the basis of the energy dissipation provided by the dissociation of UPy dimers; it was estimated that the free-energy change involved in stretching the control network to 100% strain is ca. 0.6 kcal/mol, while for the UPy-based network it was calculated to be ca. 11 kcal/mol. Further work of the groups of Guan and Li explored the introduction of folded amide-based segments (foldamers) as cross-linking points of polymer networks.88 Similarly to UPy dimers, these hydrogen-bonded foldamers were expected to act as energy dissipation sites under mechanical stress via the cleavage of intramolecular hydrogen bonds. A series of aromatic oligoamides of various lengths with and without (for control purposes) intramolecular hydrogen bonding ability were synthesized and used to cross-link poly(n-butyl methacrylate). Increasing the length of the cross-linking foldamer was observed to retard the creep and relaxation processes as a result of the increased energy storing capability. On the other hand, the foldamers in which intramolecular hydrogen bonding had been disabled did not provide an advantage in terms of mechanical properties. In work by Weng and co-workers,89,90 the dissipation of stressinduced energy through the unfolding of modular domains was also part of the strategy to create tough bioinspired polymeric materials. A first example involved the synthesis of a copolymer containing the tridentate ligand 2,6-bis(1,2,3-triazol-4-yl)pyridine (BTP) as pendant groups as well as poly(tetrahydrofuran) (poly(THF)) soft segments (Figure 12a).89

Mixing this copolymer with Zn2+ or Eu3+ salts yielded a series of metallo-supramolecular networks (Figure 12a) with excellent mechanical properties, including a tensile strength of up to 18 MPa and a strain at break of more than 1000% (Figure 12b). Small-angle X-ray scattering (SAXS) analysis showed that these materials are phase-segregated into poly(THF) and crystalline metal−ligand-rich phases with domain spacings of around 12 nm. Further SAXS analyses on samples stretched to different strains provided insights into the toughening mechanism. At low strain (elastic region), the domains are spaced apart from each other, but they retain their shape integrity upon deformation. In an intermediate strain regime, the hard domains deform significantly and eventually shatter, which translates into a moderate increase of stress over a large strain range. At high strains, the strain-induced alignment of polymer chains, the continuous disruption of hard domains, and possibly also the dissociation of metal−ligand complexes result in significant strain hardening. The toughening effect is more pronounced in the materials containing a higher fraction of Eu3+, which is unexpected when taking into account the higher binding constant of Zn2+ with the BTP ligand.91 However, it was found through SAXS analyses that the Eu3+-BTP complexes crystallize into a better packed hard phase within the polymer matrix, which in turn leads to an improved mechanical stability. In another example,90 the Weng group synthesized a similar copolymer displaying poly(THF) segments as well as UPy and spiropyran units. In this system, the UPy units dimerized intra12860

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 12. (a) Chemical structure of the synthesized polyurethane containing main-chain BTP ligands and a cartoon illustrating the cross-linking upon addition of Zn2+ cations and the formation of metal complex-rich segregated domains. (b) Stress−strain curves of polymer films containing different Zn2+:Eu3+ ratios. Reproduced with permission from ref 89. Copyright 2013 The Royal Society of Chemistry.

and intermolecularly92 and subsequently crystallized into hard domains that phase segregated from the soft poly(THF) phase, whereas the spiropyran units were introduced to serve as mechanochromic sensors (Figure 13a).93 In order to investigate

mechanical and mechano-responsive properties of this material at the nanoscale. The data obtained point to a similar strain response mechanism as the one found for the previously studied system,89 whereby the UPy-rich hard domains are separated from each other at low strains (92% and >99%, respectively. These results show that β-sheets are excellent hard domains for shape recovery when combined with a crystalline switching phase such as PCL. The silk spun by caddisworms, the larvae of caddisflies, has also served as a source of inspiration for material scientists. These aquatic creatures produce an adhesive silk that acts as a pressure12865

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

18c); samples stretched to 50% showed 90% recovery and negligible hysteresis respectively after 90 min of recovery time. While the modulus and toughness of these materials were below those of caddisworm silk, the Ca2+ and Mg2+ hydrogels displayed a much higher toughness (work of extension) than articular cartilage. 3.3. Materials Inspired by the Mussel Byssus

The outstanding mechanical and adhesive properties of the mussel byssus, which allows these mollusks to adhere to rocks underwater and against high shear forces caused by tides, has inspired several works that focus on the improvement of the mechanical properties of a material through similar supramolecular interactions.108−116 Indeed, the mussel byssus is a high-modulus material mainly composed of proteins that contain the amino acid 3,4-dihydroxyphenyl-L-alanine (DOPA) in high concentration. The latter is thought to be involved both in adhesion and cross-linking processes through the formation of metal−ligand complexes.117,118 This section collects a series of works that were inspired by this working principle and in which materials displaying strain hardening or shape memory were developed. As in the biological model, metal salt-ligand interactions have been widely exploited to mimic the sacrificial bond-based mechanical reinforcement found in biological systems.119,120 Aiming at improving the mechanical properties of epoxidized natural rubber (ENR) Guo, Zhang, and co-workers introduced Fe3+, a metal ion capable of coordinating to six oxygen atoms.121 They performed the curing of ENR with zinc acrylate in the presence of FeCl3 to create a network structure that features covalent as well as metallosupramolecular cross-links (Figure 19a). The authors prepared samples containing between 0 and 3% w/w Fe3+ and observed that the Tg of the ENR could be tuned between 7 and 65 °C, depending on the equivalents of zinc acrylate and FeCl3 used. Stress−strain curves were performed on the samples with lower Tgs (7−37 °C) at room temperature, which showed a remarkable reinforcement upon introduction of Fe3+-O links. The dissociation of Fe3+-O links under stress was observed by means of cyclic tensile tests, which showed the expected hysteresis and confirmed the role of these sacrificial links in the increased toughness. The presence of two coexisting networks (covalent and supramolecular) bestows this material with two possible shape-fixation mechanisms (i.e., the Tg of the covalent network and the reversible metal−ligand coordination). Thus, the triple shape-memory effect of a sample containing 4% w/w of Fe3+ was investigated by heating the material to 110 °C (T > Tg and dissociation temperature of Fe3+-O links) and deforming it to the first temporary shape, cooling it down to 42 °C, while maintaining the deformation force (Fe3+-O links reform and fix the temporary shape), deforming it to the second temporary shape, and fixing it at low temperature (Tg fixes the second temporary shape, Figure 19, panels b and c). Both the fixity (91 and 98% for the first and second temporary shapes) and recovery (100 and 88% for the first temporary shape and original shape) rates were excellent. In further related studies from the same group, hydrogen bonds (triazole groups) and metal complexes (Zn2+-triazole, Zn2+-carboxylic acid) were combined in a chemically cross-linked cis-1,4-poly(isoprene) network,122 and hydrogen bonds (urazole groups) were introduced in a cross-linked solution-polymerized SBR.123 In all cases, the mechanical properties of the host networks were significantly improved in a similar way to the above-discussed examples.

Figure 19. (a) Cartoon showing the shape-fixation mechanism of an ENR-containing covalent cross-links and Fe3+-O complexes as reversible cross-links. (b) Shape memory cycle and (c) series of images showing the triple shape memory property of a sample of ENR containing 4% w/ w of Fe3+; the sample was heated to 100 °C and given the first temporary shape, cooled down to 43 °C to fix it, given the second temporary shape and cooled down to 0 °C to fix it. Reproduced from ref 121. Copyright 2016 American Chemical Society.

Aiming to improve the typically limited mechanical properties of rubbers through the introduction of such sacrificial links, Guo, Zhang, and co-workers also introduced Zn2+ cations to the vulcanization reaction of a butadiene-styrene-vinylpyridine rubber (commonly known as vinylpyridine rubber or VPR) to generate transient pyridine-Zn2+-pyridine cross-links.124 This approach does not replicate a particular biological model but mirrors the ability of the various reversible bonds found in nature to dissipate stress. A series of VPRs were thus synthesized with Zn2+/VP ratios between 0.25 and 0.67 (Figure 20a). As expected, significant hysteresis was observed on account of slow reassociation of the noncovalent bonds when a rubber prepared with a Zn2+/VP ratio of 0.5 was subjected to cyclic tensile tests. However, the original network structure could be quickly (30 s) recovered by heating at 80 °C. Similarly, all Zn-VPRs showed higher stress relaxation than the control sample when stretched to and held at 200% strain. The stress−strain curves of the ZnVPRs confirmed the benefit of the pyridine-Zn2+-pyridine crosslinks compared to the control sample (Figure 20b); the tensile modulus and tensile strength were increased, while the extensibility was not compromised. The shape memory property of a VPR with a Zn2+/VP ratio of 0.5 was subsequently 12866

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Zhang, and co-workers improved sensibly the mechanical properties of a commercial rubber and showed advanced functionality, following a relatively simple synthetic approach which appears to be scalable. 3.4. Materials Inspired by Resilin

The natural protein with the highest-known elasticity is resilin. It is found in cuticle regions of insects, where it withstands millions of extensions and retractions during their lifetime.125 This highly resilient material was first isolated by Weis-Fogh from locust wing-hinges in the 1960’s.126 More recent studies have shown that this rubberlike material has 95% resilience under high frequency conditions and that it can be stretched to >300% strain before breaking.127 Resilin features hard and soft phases and is cross-linked at the tyrosine residues. It has been proposed that when subjected to mechanical stress, the soft phase is the first to react due to its quasi-perfect elasticity, transferring the absorbed energy to the hard phase, which uses it to undergo a rearrangement to a beta-turn structure. Once the stress is removed, the hard phase releases the stored energy to the soft phase returning to an unstructured conformation (original state), and the energy is then used by the insect to jump or fly.125 The polypeptide structure of resilin served Kiick and coworkers as inspiration to design a protein-based elastomeric material for tissue engineering applications.128 With this purpose in mind, the group synthesized a recombinant polypeptidic material displaying distinct domains with specific biological activities, good mechanical properties, cell-adhesion, material degradation, and growth factor delivery. Fortunately, the polypeptide conformational properties of the amino acid sequence of resilin were not affected by the introduction of such domains. Tensile tests on a hydrogel of this material showed a Young’s modulus of 30−60 kPa with an elongation at break of ca. 130%, which represents an 8-fold decrease of the modulus with respect to the resilin tendon of a dragonfly, but a 10-fold increase relative to the value reported for a rubber-like material obtained through photochemical cross-linking of recombinant resilin.127 The resilience of this material was found to be >90% in cyclic tensile tests.129 The teams of Wang and Tang reported a resilin-inspired polymer network displaying covalently connected cellulosebased hard phases and poly(isoprene) soft phases.130 Their synthetic approach involved the grafting of poly(isoprene) chains from cellulose that had been previously functionalized with atom-transfer radical-polymerization (ATRP) initiators

Figure 20. (a) Cartoon and chemical structures showing the shapefixation mechanism of a VPR-containing covalent cross-links and metal−ligand reversible cross-links. (1) The as-prepared VPR is stretched during the tensile tests, (2) which causes the dissociation of pyridine-Zn2+ complexes. The temporary (stressed) shape can be fixed by reforming the pyridine-Zn2+ complexes at low temperature (3). When the sample is heated, the pyridine-Zn2+ complexes are again dissociated and the network recovers its nonstressed shape. (b) Stress− strain curves of VRP with different Zn2+/VP ratios. (c) Pictures documenting the shape recovery process of VPR with a 0.5 Zn2+/VP ratio (fixing temperature = −10 °C, recovery temperature = 60 °C). Reproduced from ref 124. Copyright 2016 American Chemical Society.

investigated both quantitatively and qualitatively (Figure 20c). Applying a tensile load of 3 N, the sample was elongated to 80% strain at 60 °C and cooled in the stretched state to 10 °C, which resulted in shape fixing with a fixity ratio of 80%. Heating the sample to 60 °C resulted in the recovery of ca. 100% of the original shape. In this system, the original shape is dictated by the covalent network, while the transient network serves as the switch to fix/release the temporary shape. With this work, Guo,

Figure 21. (a) Schematic showing the preparation of resilin-inspired elastomers via the synthesis of a cellulose-based multifunctional macroinitiator and subsequent polymerization of isoprene involving cross-linking via radical−radical coupling at high monomer conversion. (b) Step-cycle stress−strain curves (the strain was increased steadily and curves are shifted horizontally for clarity) of a sample containing 0.5% w/w cellulose and 10% w/w of mineral oil as plasticizer; the inset shows the strain profile as a function of time. Reproduced from ref 130. Copyright 2016 American Chemical Society. 12867

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

(Figure 21a). During the polymerization via activatorregenerated-by-electron-transfer ATRP (ARGET-ATRP), radical−radical coupling at the later stages of the polymerization led to the desired cross-linking (Figure 21a). A series of networks with cellulose contents between 0.5 and 2.3% w/w was thus synthesized and the tensile properties of these materials were investigated. The stress−strain curves showed almost linear responses, confirming the high elasticity of the samples, which displayed tensile strengths between 2.1 and 4.3 MPa, strains at break of 104 to 233 MPa, and elastic moduli between 2.3 and 5.7 MPa. The degree of stress relaxation at a constant strain of 80% decreased with the cellulose content. Thus, the sample containing 2.3% w/w cellulose showed 23.5% relaxation within 10 h, while the sample with 0.5% w/w relaxed 11%. The authors explained this observation on the basis of the higher entropic elasticity of the samples containing a higher fraction of poly(isoprene). The resilience of these materials was found to be lower than that of resilin (63−87% vs 95%), probably due to the presence of some degree of chain entanglement between poly(isoprene) chains. This was supported by cyclic tensile tests which, after 10 cycles, showed an increase of resilience up to 98.7% for the sample containing 2.3% w/w of cellulose. The resilience was also tested after plasticizing the networks with mineral oil (Figure 21b). This was done to reproduce the natural hydrated state of resilin, whose properties are influenced by the lubrication effect of water molecules.125 In this study, however, mineral oil was used instead of water due to the hydrophobicity of the poly(isoprene) matrix. The resilience was observed to increase as a result of reduced chain friction, which in turn minimizes energy losses.

domains and the subsequent dissociation of discrete supramolecular motifs. One frequent drawback of these materials is their slow recovery once the applied stress is removed, which stems from the dynamic nature of supramolecular bonds. Chemically bypassing the components of the supramolecular motifs to facilitate reassembly appears to be an effective solution; however, it is a synthesis-intensive strategy with limited upscaling potential. In this regard, the lowest hysteresis is achieved with resilin-mimicking materials in which the toughening mechanism does not involve the dissociation of supramolecular units but the interplay between soft and hard phases under stress. The works reviewed in this section show that reversible interactions can also be used to impart shape-memory behavior to synthetic polymers. To this end, various hydrogen-bonded and metal−ligand motifs have been used and shown to provide very high shape fixity and recovery values upon exposure to an external stimulus. It is also worth noting that most of these works involve relatively straightforward syntheses, which is interesting from an applied viewpoint.

4. PLANT-INSPIRED ACTUATING POLYMERS AND POLYMER SYSTEMS One of the essential functions in living organisms is actuation (i.e., the ability to cause mechanical action or motion). In this section, the focus is placed on artificial materials that display this actuation capability as a stimulus-induced change of their physicochemical properties, as opposed to objects that carry out functions when coupled to instruments or energy supplies.173 Strictly speaking, virtually all materials can expand or contract in response to changes in the surrounding environment, for example on account of thermal expansion or swelling and can, at least in principle, be employed to provide actuation. Early examples of materials performing as actuators were reported as early as 1932, when cadmium−gold alloys were found to wrinkle in an unexpected way upon cooling,174 although the fundamental mechanisms of the thermoelastic behavior remained unknown until 20 years later.175,176 Polymeric actuating materials started to receive more widespread attention much later when research into stimuliresponsive materials afforded concepts and building blocks that proved to be useful in the context of actuation. Indeed, the everincreasing interest in polymeric actuators has generated a plethora of publications that approach the topic from a design, inspiration, or material point of view,64,154,177−185 while the resulting shape transformations,186−191 actuation mechanisms, and possible applications have been reviewed elsewhere.192−195 Bioinspired shape-shifting has been the focus of other recent reviews that summarize the state of this growing field and highlight its dynamics.13,23,196−198 This section expands on these reviews by including newer bioinspired actuating polymers and polymer systems, which are categorized based on the underlying mechanism. Initially, the mechanisms behind motion in several plant systems are presented as the models on which many bioinspired synthetic actuators are based. While actuation in animals is prominent and dictated by muscle movement, plants represent a group of more simplistic, yet elegant models, as they rely on changes in the turgor pressure of specialized cells and/or changes in the directionality of their components. Furthermore, in the examples discussed herein (c.f. section 4.1), the observed movement is a result of the properties of the material rather than a metabolic process; indeed, the driver for these movements are cues from the environment, such as changes in light, temperature, and humidity, and the ensuing motion is essential for the

3.5. Sacrificial Bonds and Domains in Other Nonbioinspired Mechanically Adaptive Materials

Many other nonbioinspired works have demonstrated the benefits of sacrificial bonds or domains on the mechanical properties of polymers. For instance, hydrogen bonding units such as UPy,131−134 benzene-1,3,5-tricarboxamide (BTA),135,136 urazole,137 amide,136,138 and mixed hydrogen-bonded systems139−145 have been used to impart strength and toughness to solid polymers, hydrogels, and nanocomposites. Ionic interactions,146−149 metal−ligand complexes,150 and physical interactions151,152 have as well been used for the same purpose, which underlines the broad interest that noncovalent interactions awake in various fields of material science. Furthermore, noncovalent interactions have been used as temporary shape fixation points in many nonbioinspired shape memory polymeric materials.153−155 For instance, hydrogen bonding motifs such as the UPy dimer,156−161 the carboxylic acid-pyridine pair,162−164 the pyridine-urethane pair,165,166 or carboxylic acid dimers,167 as well as metal-terpyridine ligand complexes168,169 and ionic interactions170−172 have proven very powerful tools for the programing of shape memory polymers. To summarize, nature’s concept to create materials which change their mechanical properties under mechanical load via the introduction of reversible sacrificial bonds/domains has been widely and successfully mimicked in a broad variety of synthetic polymers. The examples discussed above demonstrate that supramolecular motifs can be used either as discrete sacrificial bonds or as building blocks of larger sacrificial domains in materials that display a hierarchical structure (i.e., in which the supramolecular motifs crystallize as a hard phase). In contrast to the former, domain-based materials benefit from a dual stress dissipation mechanism which involves the unfolding of the 12868

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

survival of the plant species.199 Similarly, bioinspired polymerbased actuators discussed here are chosen on the premises of the material being responsible for the stimuli-responsive motion, rather than the actuation being a feat of smart engineering or design. Potential applications of polymer-based actuators include soft robotics, targeted drug delivery, and microfluidics,200−206 especially in fields where the combination of robustness and structural integrity of tough materials with the flexibility and deformability of compliant materials enables interfacing with the environment and biological tissues.207 4.1. Model Actuators in Plants

Materials found in plants are rich in water and cellulose. These components contribute to the mechanical properties of the tissue and are also responsible for stimulus-induced motion through changes in osmotic potential of cell membranes (i.e., turgor pressure) and/or nonisotropic expansion/contraction effects that originate in the nonisotropic orientation of the cellulose fibers. Both mechanisms are a result of biochemical processes, which have been reviewed elsewhere in great detail,196,208−210 and together support the motility of the corresponding tissue. The two effects are often intimately connected, as the orientation of cellulose fibrils has been shown to predictably affect the motility of the tissue.211 In a simplified cell wall model, the effect of water uptake on the directional swelling of the cell wall as a factor of the cellulose fibril orientation was shown, assuming that oriented cellulose fibrils are embedded in an elastic matrix that swells in an isotropic fashion when exposed to water. When the matrix swells, the fibrils assume part of the stress imposed to the matrix in the direction of the fibril orientation. As a consequence, as long as the fibril orientation with respect to the cell wall long axis is below 45°, the stresses are directed toward a predominant swelling along the longitude of the cell wall. In contrast to this, randomly oriented cellulose fibrils resulted in minimal swelling along the longitude of the cell, presumably at the expense of significant lateral swelling that increases the cell wall thickness. This effect is more prominent when cellulose fibrils are oriented at a large angle, thus leading to greater lateral swelling. Many plants exploit the principle of cellulose orientation directing moisture driven deployment, such as the unfurling of the desert resurrection plant.212 For instance Selaginella lepidophylla, a resurrection plant found in the Chihuahuan desert, has been shown to curl its stems upon dehydration forming a sphere, allowing the reduction of exposure to the sun (Figure 22). This actuation mechanism is the result of the compositional variation in the inner and outer layer of the plant stems. Behaving as a bilayer structure, the abaxial (lower) and adaxial (upper) zones of the stem tissue differ in cell density, with smaller and denser cells on the abaxial side. Furthermore, lignified tissues were also observed on the abaxial side, thus increasing the local stiffness of the tissue. Upon (de)hydration, the differential shrinkage or swelling causes strains, which induce the actuation causing curling of the stems.212 Tendrils offer a survival solution to plants such as the cucumber; they constitute an integral part of its ability to climb on other structures and thus increase its sunlight exposure.213 This is achieved through the reaching of a straight tendril to an anchoring point, followed by a coiling motion, which not only wraps the tendril around the anchor but also effectively shortens its length, thus hoisting the plant. Investigations of the cucumber tendril structure have shown that in their resting state, the tendrils are straight with a uniform cell distribution. Upon actuation, a fiber ribbon is formed that runs across the long axis of

Figure 22. Pictures of the desert resurrection plant under (a) dry and (b) wet conditions. The latter cause the curling of the (c and d) stems as a result of their anisotropic lignification, which is reflected by the fluorescence microscopy image shown in (e). Adapted with permission from ref 212. Copyright 2015 Macmillan Publishers Ltd.: Scientific Reports.

the inner part of the coiling tendril. This ribbon consists of two layers of cells that are lignified, albeit to a different degree, thus unevenly increasing the stiffness of the formed ribbon. The overall helical shape of the tendril is attributed to the inherent coiling of the ribbon, which was proposed to be a result of the asymmetric contraction of the two cell layers. The latter is a result of the variant hydrophobicity of the two cell layers, a direct result of their uneven degree of lignification (Figure 23).213 Another fascinating example of materials-driven actuation in nature is the seed dispersal mechanism of plants, such as the geranium species Erodium gruinum, whose awns coil upon dehydration and thus causes an accumulation of tension.214 At the threshold coiling, and as a result of mechanical failure, the awn detaches and the seeds are propelled. The investigation of the microstructure of the awns revealed a bilayer structure. Interestingly, however, only one of these layers is responsible for the coiling. It was shown that this effect originates in a structure of cellulose fibrils that are wound around elongated cells in a tilted helix formation within the cell wall. The angle of the tilt of the helix (i.e., the direction of the cellulose microfibrils with respect to the cell long axis) was shown to increase toward the base of the awn (Figure 24).215,216 Another example of a complex structure in which turgor pressure and cellulose fibril orientation cooperatively induce a macroscopic twisting motion can be found in seedpods, where two multilayered structures encase the seed. One example is the seedpods of orchid trees, such as Bauhinia (Figure 25).217 The layered structures are largely composed of cellulose fibrils that are responsible for the directional swelling of the matrix. As in the above examples, the fibril orientation determines the direction of the swelling/deformation (e.g., a parallel fibril configuration results in strains perpendicular to the fibrils). As a result of the 12869

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 23. Pictures (a, d, and i), darkfield microscopy images (b, e, and g), and UV autofluorescence images (c, f, and h) of cucumber tendrils that are straight before attachment to a (a) target with a (b and c) uniform structure but upon attachment they (d) coil as a result of the (e, f, g, and h) anisotropic lignification. The isolated lignified tissue indeed forms a (i) stable ribbon. Scale bars: (b and c) 0.5 mm, (e and f) 100 μm, (g and h) 10 μm, and (i) 1 mm. Reproduced with permission from ref 213. Copyright 2012 American Association for the Advancement of Science.

Figure 24. (a) Picture of an Erodium awn and the corresponding SAXS patterns indicating a tighter coil in the bottom part. (b) Cryo-SEM image of a single cell showing the orientation of the cellulose fibrils, indicated by the dotted lines, which dictates the coiling of the tissue. Reproduced with permission from ref 216. Copyright 2012 The Royal Society.

Figure 25. Pictures of Bauhinia variegate seedpods in the (a) hydrated and (b) dried state. The transition is a direct result of the orientation of the fibrous layers, which upon dehydration shrink perpendicularly to the long axis of the pod, inducing the helical twisting seen in (b). Reproduced with permission from ref 217. Copyright 2011 American Association for the Advancement of Science.

microdeformations and the hierarchical layered tissue structure, macroscopic deformations, such as twisting, occur.218 In the case of orchid tree seedpods, the directors of the cellulose microfibrils in the two layers are shifted at angles of π/4 with respect to the pod’s long axis and they are arranged orthogonal to each other, and this arrangement drives the twisting upon dehydration of the pod. Based merely on changes in humidity, pine cones represent a model example of how material structure can impart unique properties. When in a humid environment, pine cones adopt a closed packed structure, whereas upon dehydration, often as a result of detachment from the tree, the scales open, a process that is reversible upon rehydration (Figure 26). This effect has been found to be the result of the structure of the individual scales, which consist of two types of tissues that differ in tensile stiffness and coefficient of hygroscopic expansion. Furthermore, the orientation of the cellulose microfibril components of the two tissues was found to be drastically different with the outer tissue bearing cellulose fibers aligned perpendicularly to the long axis of the scale while those of the inner tissue are almost parallel. This variation in orientation of the fibrils results in the top (inner)

section being reinforced against swelling along the scale’s long axis while the bottom (outer) freely swells. This bilayer structure and anisotropic response to hydration therefore accounts for the passive movement of the pine cone scales and the overall open/ close form of the pine cones.219−221 Similarly to pine cones, ice plant (Aizoaceae) seeds are dispersed through a nonmetabolic process (i.e., through waterinduced actuation of a complex, but nonliving, materials system). Via cooperative flexing-and-packing that is induced through the water-swelling of a cellulose layer filling specialized plant cells, a reversible origami-like folding takes place. The cellulose swelling is translated into a movement through simple geometric constraints embedded in the hierarchical architecture of the ice plant valves (Figure 27).222 Perhaps known more for its seed dispersal mechanism, the dandelion has been shown to have a fascinating structure that allows it to alter the angle of its pappus (i.e., the fine appendage of 12870

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 28. Pictures capturing the opening and closing of dandelion pappi upon changes in the relative humidity. Adapted with permission from ref 223. Copyright 2016 John Wiley & Sons, Inc.

Figure 26. Pictures of pine cones in their wet/closed (top) and dry/ open (bottom) state as a result of the unilateral swelling of the scales. Upon dehydration, the anisotropic shrinkage of the outer layer of the scale results in its overall bending to an angle θ with respect to the hydrated scale (i−ii). Reproduced with permission from ref 220. Copyright 2009 The Royal Society.

aligned along their long axis and are essentially parallel with the long axis of the awn. On the other hand, in the outer active layer, the cellulose microfibrils are randomly orientated. As a result, when water is absorbed from the matrix, the outer layer swells, resulting in the macroscopic bending of the awn toward the oriented fibrils (Figure 29), thus pushing the awns together.224,225 Note that this bilayer configuration is only present at the bottom of the ridge. Another elegant actuating mechanism found in nature is the rapid closure of the Venus fly trap (Dionaea muscipula) leaves to capture insect. This process differs from those previously discussed in the sense that it entails a variety of biochemical processes and it is not just a result of the effect of humidity on the plant tissue.226 The rapid change of the leaf geometry from convex to concave upon biochemical stimulation has been the center of attention of various studies which assign the movement to loss of turgor, acid-induced swelling, or electrical stimulation, although the exact mechanism is unclear.5 Nonetheless, it has been proposed that the actuation mechanism relies on the difference in hydrostatic pressure of the outer and inner layers of the plant leaves. This builds elastic energy when the plant leaves are open, which is released upon stimulation and the leaves close, while water channels allow equilibration of the hydrostatic pressure of the layers.227 The trap closing of the Venus flytrap is a particularly fascinating actuation example as it is exceptionally fast (ca. 0.3 s).228

Figure 27. (a and b) Photographs and (c and d) confocal microscopy images of the ice plant seed capsules in their (a and c) dry and (b and d) hydrated state. Adapted with permission from ref 222. Copyright 2011 Macmillan Publishers Ltd.: Nature Communications.

4.2. Actuation in Bilayer Structures

the dandelion) with respect to the pulvinus (i.e., the body) as a function of the relative humidity (Figure 28).223 The configuration of the pappus affects the aerodynamic properties of the single seed unit, and thus its chances for successful germination. Under humid conditions, the pulvinus cells are swollen and the pappus is spread at an angle of 180°, while upon drying it adopts a more closed structure with the angle being as low as 72°, owing to the shrinkage of the cells. This behavior is reversed when the plant is reintroduced to humid conditions. Similar to pine cone scales, the awns of the wheat seed dispersal units bend when they dry and straighten when exposed to humid conditions. The underlying mechanism is directly related to the composition of the awns which are comprised of two layers, the inner “resistance” layer and the outer “active” layer. The resistance layer is composed of a soft hygroscopic matrix, which is reinforced with cellulose microfibrils that are

As demonstrated in the case of several natural actuators, compositional anisotropy enables an object to respond to an external stimulus by way of shape shifting. The simplest embodiment of this approach are bilayer films composed of two materials with different thermal expansion or swelling characteristics (Figure 30), although practical issues such as potential mechanical instabilities and delamination must be considered.173,229 An alternative is to create a property gradient along an axis, for example by varying the extent of cross-linking in a gradual manner. Indeed, the swelling of nonoriented cellulose fibrils was shown in an example whereby a film of nanofibrillated cellulose bended when it was placed in a humid environment,230 despite the absence of any structuring or orientation. It was postulated that the actuation stemmed from the formation of a pseudobilayer due to preferred swelling of the cellulose on the side facing the water vapor flux. 12871

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 29. Picture of (a) wheat and (b) its dispersal unit at high (left) and low (right) relative humidity. The bottom part of the awn is highlighted to indicate the resistance and active part. (c) Cryo-SEM image of the bottom part of the awn which can be distinguished to a resistant and an active part depending on the orientation of the cellulose fibrils along its axis. Reproduced with permission from ref 225. Copyright 2008 Elsevier Ltd. Wheat picture with additional permission of Dr. Zvi Peleg.

mechanism of pine cone scales, it was found that the model overestimates the generated blocking forces as it only takes into account the mechanical properties of the dry tissue, disregarding the effect of water.235 In the example of the studied pine cone scales, the model overestimated the blocking forces by a factor of 2, which was attributed to the high water content of pine cone scales that reduces the Young’s modulus by ca. 50%. This observation is significant as several of the following examples rely on water uptake to induce actuation. Besides simple geometry, key parameters that were shown to affect the actuation behavior of a stimuli-responsive polymeric bilayer include film aspect ratio, the extent of the induced response, and diffusion constraints.236 These were demonstrated by the formation of polymer bilayers whereby one layer was water-swellable, and to restrict the water diffusion, the bilayer was placed on a substrate with the responsive side down. The hydrophilic layer employed was composed of thermoresponsive poly(N-isopropylacrylamide) (PNIPAM) copolymers, while the passive layer was composed of hydrophobic polymers, either poly(methyl methacrylate-co-benzophenone acrylate) or PCL. When placed on a substrate with the PNIPAM side facing down, and, upon immersion into an aqueous solution, the hydrophilic layer of the film swelled resulting in a rolling motion of the overall bilayer. Furthermore, owing to the temperature-dependent solubility of PNIPAM in water, a similar rolling behavior was observed when the films were placed in warm water (above the lower critical solution temperature, LCST, of PNIPAM) and allowed to cool, thus resulting in the swelling of the PNIPAM layer when the temperature was below the LCST. While the size of the film did not affect the geometry of the water-swollen bilayer, the aspect ratio of the bilayer structure had a significant influence on the shape produced by the actuation process. This was confirmed by finite-element modeling which indicates that at high aspect ratios, long-side rolling of the film was found preferential (Figure 31b), although all-side rolling was observed when the width of the film was greater than the circumference of the formed tube (Figure 31c). All-side rolling is also observed when both the length and the width of the film are comparable to the circumference which also resulted in diagonal rolling (Figure 31a). The rolling motion was predominantly observed to start from the corners of the films, a fact that was attributed to favorable diffusion of water into the material. These conclusions were proposed to be relevant to all thin films composed of bilayers with unilateral swelling capacities. Inspired by the example of pine cones (vide supra), synthetic geometries relying on bilayers of materials that respond diversely to stimuli, such as humidity, have been shown to shape-morph

Figure 30. Schematic illustration showing possible bilayer or graded structures in their inactive (left) and actuated (right) states. Reproduced with permission from ref 199. Copyright 2013 Elsevier Ltd.

In terms of polymer-based bilayer-type actuators there is a plethora of possible combinations that will result in the anisotropic expansion/shrinkage of the material, which in most cases is a result of smart design and/or choice of materials rather than an inherent material property. Indeed, such top-down approaches for the preparation of bilayer-type actuators are discussed elsewhere.190,231−233 Bilayers in the form of bimetallic strips were modeled by Timoshenko in 1925, whose results have been used as a simple predictive model for polymeric actuators.234 This model describes the behavior of the bilayer in the absence of any external forces and assuming that the dimensions of the two layers are comparable with their thickness smaller than the curvature. Furthermore, it assumes that stress anisotropies are only present on the z axis and not throughout the planes of the layers. Thus, assuming that bending only takes place along one axis, the curvature of the bilayer is proportional to the elongation and inversely proportional to the thickness of the material. Using the metallic bilayer model to characterize the actuation 12872

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

reversible, and on these premises, an artificial flower was prepared using the paper-polymer bilayer film as the petals. When in contact with water, the flower was shown to “bloom” while upon drying the petals closed. Hydrogel actuators (which will be further discussed, vide infra) have also been created using strips of partially interpenetrated hydrogel networks with differing swelling properties. This concept was first demonstrated some 20 years ago using bilayers of PNIPAM and acrylamide that exhibit different swelling properties in response to humidity and temperature in aqueous environments.237 The bilayer polymer film was shown to bend toward the PNIPAM side when increasing the local temperature, as a result of the LCST of the polymer and subsequent shrinking, while introduction of a nonsolvent for the acrylamide layer resulted in the bending of the bilayer toward the acrylamide face. Similar to the bilayer structures of several natural actuating systems (see section 4.1), a film of layer-by-layer (LbL) deposited poly(allylamine hydrochloride) (PAH) and poly(acrylic acid) (PAA) was interfacially bound to a hydrophobic poly(tetrafluoro ethylene) (PTFE) sheet. The PAH/PAA LbL film is known to be hygroscopic with swelling capacities up to 40% when exposed to humidity, while the PTFE is hydrophobic and should thus remain passive under humid conditions.238,239 The resulting bilayer (whereby one layer is the swellable LbL and the other is the hydrophobic PTFE), upon exposure to humidity, was shown to bend into a coil shape whereby the coil radius was found to decrease with increasing number of layers on the hydrophilic side of the film (Figure 32). By alternating exposure to high and low humidity conditions, the curvature of the material was shown to also change. Taking advantage of this

Figure 31. Schematic illustration of the various possible shape changes for a thin bilayer film with a passive (green) and a swellable (orange) layer when placed on a substrate, depending on the aspect ratio of the film: (a) if the width (W) and the length (L) of the film is comparable to the circumference (C) of the formed tubes, diagonal rolling occurs, (b) if the length is greater than the circumference, long-side rolling takes place, and (c) if both the width and length of the film are greater than the circumference rolling from all sides occurs. Reproduced from ref 236. Copyright 2012 American Chemical Society.

efficiently. A simple example was presented by Mahadevan and co-workers, who used a bilayer of a nonresponsive polymer glued onto cellulosic paper to showcase the humidity-induced bending of the material.220 Upon exposure to humid conditions, the bilayer was shown to bend with the bending curvature increasing with increasing relative humidity. The process was shown to be

Figure 32. (a) Photographs of bilayers of PTFE and a hydrophilic LbL composition of PAH and PAA demonstrating the curvature dependence on the number of layers on the LbL side (BL indicates the number of PAH and PAA layers). (b) Graph showing the coil radius and the thickness of the polyelectrolyte multilayer (PEM) as a function of the number of PAH−PAA bilayers. (c) Photographs of the bilayers as a function of relative humidity and amount of layers. (d) Scanning electron microscope image of the polymer film containing 10 bilayers. Reproduced from ref 240. Copyright 2013 American Chemical Society. 12873

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 33. (a) Schematic representation of the synthesis of stearoyl esters of cellulose and the processing of these materials as films. (b) Images showing the bending of a film of stearoyl esters-functionalized cellulose (degree of substitution of 0.3, thickness 21 μm) as a response to the presence of moisture from warm (37 °C) water placed directly under the film. Reproduced with permission from ref 241. Copyright 2015 Macmillan Publishers Ltd.: Scientific Reports.

Figure 34. (a) Photographs of the chitosan/cellulose based bilayers at different pH values. Note that the chitosan was dyed with methyl orange to provide a red color for guidance. Schematic representation of the pH-dependent bending deformation of the bilayers indicating the swelling of the cellulose layer at high pH and (b) the swelling of the chitosan layer at low pH. (c) Scanning electron microscopy images of the cross-section of a bilayer hydrogel at pH 7 and pH 1 (d) demonstrating the respective swelling of the cellulose and the chitosan layers. Graphs showing the swelling ratio of the two layers as a function of (e) pH and (f) ionic strength and the overall curvature of the bilayer as a function of the (g) pH. Reproduced with permission from ref 243. Copyright 2017 The Royal Society of Chemistry.

12874

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

at pH values above 3.8, chitosan was on the concave side of the bent strip. At pH 3.8, the strip was straight, owing to the similar swelling of the two bilayer components. This behavior was shown to be fully reversible while programmable 3D shapes were shown to be possible by smart placement of the 2D bilayers. Among them, a simple tunable optical lens was prepared whereby two domes of chitosan were bilaterally attached to a cellulose/ carboxymethylcellulose disc forming a “flying saucer”-like shape. The focal length of the lens was found to be proportional to the pH of the solution (ca. 30 mm at pH 1, ca. 60 mm at pH 7), owing to the combined swelling/deswelling of the component hydrogels.

effect, an actuator capable of locomotion was designed whereby the lateral movement of the film was assisted by a ratchet track that immobilized the actuator when, as a result of the high relative humidity, the coil unwound.240 Zhang and co-workers reported a cellulose-based moistureresponsive bilayer film that was synthesized via the combination of cellulose decorated with stearoyl ester groups at different degrees (Figure 33a).241 Initially, a compositional screening showed that only a low degree of substitution (0.3) afforded a moisture sensitive material, while higher degree of substitution (3) resulted in a nonresponsive material. The responsive stearoyl-functionalized cellulose formed a transparent film with a transmittance of ca. 90%. When exposed to water vapor under ambient conditions (relative humidity of 35% at 22 °C), a 20 μm thick film bended away from the humidity in only 1−2 s, and returned to its original shape as soon as the water vapor source was removed. This process could be repeated many times without any change in the response time (Figure 33b). It was found that the actuation was strongly dependent on the film thickness, due to diffusion constraints. The interaction of water with the material was shown to be a result of the polarity decrease due to the presence of the stearoyl chains which, according to the authors, suggests that under ambient conditions the water content in the material is very small, and thus increases rapidly upon exposure to water vapor, which in turn causes the bending. In order to understand the actual reason for the material to bend, they performed static water vapor permeability studies. The results showed that the material does absorb water through the surface facing the vapor source, which causes both a vertical and a horizontal expansion/force that generate a bending output. During the process, no structural changes take place, which allows the film to recover its original shape. Zhang and coworkers further found that the films with a higher degree of substitution (3) were temperature-responsive and prepared bilayer composites containing both moisture- and temperaturesensitive materials. These were shown to curl into tubes when exposed to either stimulus. Inspired by the moisture-driven bending of plant leaves, the synthesis of cross-linked polymer brushes unilaterally from the surface of a thin gold sheet was shown to result in an actuating bilayer.242 The brushes were prepared by photopatterning of an atom-transfer radical polymerization (ATRP) initiator onto the surface of the gold film followed by the polymerization of glycidyl methacrylate which was subsequently cross-linked by exposure to methanolic NaOH. The cross-linking of the polymer resulted in the greater swelling of the polymer film when exposed to water or methanol, compared to the non-cross-linked film, on account of the introduction of hydroxyl groups in the cross-linking process. The bilayers were shown to bend when exposed to methanol, with the radius of the curvature increasing with increasing the thickness of the gold layer, in a fashion that agrees with the metallic bilayer model.234 Owing to this ability to predict the folding of the bilayers, more complex quasi two-dimensional (2D) structures were prepared that transformed, upon wetting, into three-dimensional (3D) objects. Utilizing biopolymers in an attempt to prepare biocompatible and biodegradable bioinspired actuators, a film of chitosan crosslinked with epichlorohydrin was cast with a cellulose/ carboxymethylcellulose mixed film, thus forming a bilayer of biopolymers whose ability to swell at different pH values is the primary actuation mechanism (Figure 34).243 Indeed, upon immersion in a low pH solution, the bilayer strip was shown to bend with the protonated chitosan layer on the convex side, while

4.3. Actuation in Anisotropic Nanocomposites

Inspired by some of the aforementioned natural actuator mechanisms (c.f. section 4.1), several studies have set out to create artificial composites and systems in which inhomogeneous swelling induces actuation. The directionality of the swelling is a direct result of anisotropic fillers within the polymer matrix and is reminiscent of the twisting of seedpods upon (de)hydration. This approach has allowed the design of nanocomposites which adopt predictable shapes upon actuation.244 Studart and co-workers investigated a series of actuating materials in which alumina platelets were used as the anisotropic filler. The platelets were 7.5 μm wide and 200 nm thick with a tensile strength in the GPa range, while to aid with their alignment they were coated with superparamagnetic iron oxide nanoparticles (12 nm in diameter).245,246 The platelets were magnetically aligned and embedded in a gelatin matrix to create a composite material with a bilayer architecture, wherein the platelets adopt different orientations in the two layers (Figure 35). The bilayer films were shown to reversibly respond to

Figure 35. Schematic illustrating the swelling/shrinkage of a bilayer structure based on alumina platelet filled gelatin. (De)hydration induces a bending motion, which is guided by the orientation of the platelets. Adapted with permission from ref 247. Copyright 2013 Macmillan Publishers Ltd.: Nature Communications.

exposure to humidity: when dry, the films bent toward the layer in which the platelets were oriented perpendicular to the bilayer long axis, while upon hydration they bent toward the layer in which the platelets were oriented parallel to the layer. The directionality of the bending motion was a direct result of the different anisotropic swelling of the two layers as a consequence of the orientation of the reinforcing platelets.247 Employing the same strategy, the structure of wheat awns was also mimicked whereby from the two layers of alumina platelet-containing gelatin only one contained oriented platelets. Once again, upon hydration the material was shown to reversibly bend toward the aligned layer as a result of the greater swelling of the disordered layer.247 In another embodiment, a bilayer structure based on alumina platelet-filled gelatin was investigated, in which the platelet orientation directions in the two films were offset by a π/2 angle with respect to each other and π/4 with respect to the long axis of the material, inspired by the structure of the orchid tree seedpod. The resulting structure exhibited hydration-induced twisting; a 12875

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 36. (a−d) Schematic representation of the actuating behavior of bilayer films consisting of a glass-fiber-reinforced hygroscopic polymer layer and a layer consisting of only the polymer. Shown are different scenarios in which the dimensions of the film, the orientation of the fibers, and the direction of the humid air flow were varied. (e) Photographs of a film where the glass fibers are perpendicular to the long axis of the strip (AG/TGF@AG) and (f) a film where the glass fibers are at a 45° angle to the long axis of the strip (AG/OGF@AG) exposed to humidity. Also shown are graphs of the bending forces vs the displacement in a three-point bending geometry induced for actuators in which the fibers are oriented (g) perpendicular or (h) at a 45° angle vis-à-vis the long axis. Reproduced with permission from ref 248. Copyright 2016 John Wiley & Sons, Inc.

process that was fully reversible, while it was noted that the orientation of the twisting was determined by the effective orientation of the platelets in the material.247 Expanding on this concept, the incorporation of alumina platelets in PNIPAM in similar bilayer structures was also demonstrated, allowing a dualtriggered response, namely upon hydration and heat. Allowing the sample to fully swell in water at temperatures below the LCST of the polymer resulted in the twisting of the material, whereas heating the water-swollen composite above the LCST led to dehydration of the hydrogel and twisting in the opposite

direction. This unique behavior was found to be reproducible for over 20 cycles. In a simple approach to prepare materials that mimic the humidity-induced actuation of pine cones, tendrils, and seed awns, instead of the microscopic cellulose fibers found in these biological systems, glass fibers with diameters of 5−10 μm were incorporated into agarose, thus forming a more rigid layer, onto which a pure agarose layer was casted that is softer and more prone to swell with water upon exposure to humidity.248 Different bilayer structures were prepared in which the orientation of the fibers with respect to the long axis of the 12876

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 37. (a) Schematic representation of the preparation method of the aligned CNT/wax/polyimide strips and the dependence of their light-induced bending on the orientation of the CNTs. Photographs documenting the motion of strips with (b) longitudinal and (c) transverse CNT orientations upon exposure to visible light (100 mW/cm2) for the times indicated. Reproduced from ref 250. Copyright 2016 American Chemical Society.

film was varied and the resulting bilayer films (thickness ca. 60 μm) were exposed to a humid air flow on one side. The orientation of the glass fibers was shown to affect the bending motion of the bilayer upon exposure to a humid air flow: similar to neat agarose films, which were shown to bend away from the humidity source when exposed to a humid air flow on just one side of the film, the bilayer film was shown to curl away from the humid air flow when the glass fibers were oriented perpendicular to the sample’s long axis (Figure 36). By contrast, when the fibers were aligned parallel to the long axis, the bilayer would bend away from the humid air flow only when the flow was aimed at the neat agarose layer. Furthermore, twisting of the bilayer was observed when the fibers were oriented at an angle (45°) with respect to the film’s long axis, albeit the helicity of the twisting depended on the face of the film exposed to the humid air flow. The angle of the bending motion was also shown to be dependent on the amount of glass fibers contained in the reinforced layer: increasing the glass fiber content resulted in greater reinforcement and thus smaller angles. This was supported by a threepoint bending mechanical test that revealed that greater forces were required for the bending of more reinforced samples. Due to the rigidity of the glass fiber reinforcement of the directing layer, the recovery of the original shape upon removal of the stimulus was rapid; coiled strips of the bilayers were shown to be able to perform work merely as a response to a humid air flow or lack thereof. A mathematical model was proposed predicting the motion ensued from the exposure of such anisotropically reinforced bilayers. Similarly, a bilayer composed of flax fibers (bundles of ca. 40 fibers with an individual diameter of ca. 15−20 μm) embedded in a polymer matrix of polypropylene and maleic anhydride was prepared, inspired by the structure of pine cones. As such, layers

of the material were combined in a fashion that resulted in the orientation of the fibers forming a 0° (top, passive layer) and 90° (bottom, active layer) angle with the Z axis of the bilayer.249 When exposed to water, the film was shown to bend toward the active layer, as a result of the greater swelling of the passive layer due to the anisotropic swelling of the flax bundles. It was proposed that the bending motion can be controlled by adjusting the relative thickness of the two layers. The observed bending motion was slow, which potentially accounts for the low generated blocking forces (up to ca. 435 mN), compared to those generated by actuating natural pine cone scales (ca. 3 N). Actuators with a bilayer architecture reminiscent of that of pine cone scales was reported by Deng et al.250 Instead of cellulose fibrils and their ensuing inhomogeneous swelling, carbon nanotubes (CNTs) were employed, resulting in thermal expansion differences of the material. The CNTs were aligned and embedded in a paraffin wax matrix, which was deposited on a polyimide film. The resulting bilayer film was cut in strips at different angles to create actuators in which the alignment direction of the CNTs in the reinforced layer adopted different orientations with respect to the long axis of the strips (Figure 37). CNTs are known in the field of actuating materials for their ability to translate infrared irradiation into locally released heat, which can be used to optically stimulate a temperatureresponsive material.251 Previous studies on CNT-containing polymer films have shown the photothermally and electrothermally induced actuation of the material, albeit these were not correlated to an example of a natural actuator.252−255 When irradiated with visible light of an intensity comparable to that of the sun (ca. 100 mW/cm2), the strips were found to bend toward or away from the light source, depending on the orientation of the CNTs.250 At small angles (parallel to the long axis of the 12877

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 38. (a) Schematic representation and pictures of PAA/PIL membranes comprising CNTs oriented at different angles. Note that the films were cross-linked and that the cross-link density gradually varied across the thickness of the film. (b−d) The dependence of the acetone-induced deformation on the CNT orientation for the composite membranes is shown schematically and in pictures. Reproduced with permission from ref 256. Copyright 2017 John Wiley & Sons, Inc.

strip), the films bent toward the light adopting a curvature of ca. 85°, while when the CNTs were oriented at 90° (perpendicular to the long axis of the strip) they bent away from the light at a curvature of ca. 60°. In both cases, the bending was reversed when the irradiation was stopped; in fact some 100000 irradiation cycles were successfully completed without compromising the actuation efficiency. The magnitude of the photoinduced bending of the CNT-containing films was shown to be related to the intensity of the irradiation. With the help of control experiments, the authors demonstrated that the actuation mechanism relied indeed on the photothermally induced anisotropic expansion of the wax/CNT layer that was directed by the aligned CNTs. A mechanical arm composed of strips of this material was also fabricated to demonstrate the potential usefulness in soft robotics, while an intelligent solar cell panel that reversibly opened when illuminated and powered a diode was also presented. Aligned CNTs were also embedded in a poly(acrylic acid) (PAA) blended with the poly(ionic liquid) (PIL) poly[3cyanomethyl-1-vinylimidazolium bis(trifluoromethane sulfonyl)imide].256 Thin films produced from these blends were soaked in aqueous ammonia, which resulted in the phase separation of the PIL with the water phase and simultaneous cross-linking on account of the electrostatic complexation of the anionic PAA and the cationic imidazolium of the PIL. Owing to the directional diffusion of the ammonia through the film (from top to bottom), the electrostatic complexation of the PIL with PAA and thus the cross-linking density formed a gradient.257 Note that the gradient structure here serves to accelerate the solvent uptake when the surface of the film is in contact with solvent vapor molecules. These membranes were then cut in rectangular sheets at different orientations with respect to the CNT alignment. Actuation was achieved upon exposure to acetone vapor, which swells the PIL (Figure 38). With dependence on the alignment of the CNTs relative to the sheet, the latter rolled into a tube, twisted into a ribbon, or formed a coil. The actuation behavior was fully reversible, and the magnitude of the bending motion was found to depend on the temperature of the vapor: the curvature of the actuated film increased with increasing acetone temperatures. The overall actuation properties of these films were found to be reminiscent

of cellulose-reinforced tissues in plants, with the CNTs here geometrically dictating the stiffness and swelling anisotropy of the composites. When poly[1-phenyl-2-[p-(trimethylsilyl)phenyl]acetylene] (PTP) was spin-coated onto a layer of aligned MWCNTs, which was subsequently deposited onto an isotropic film, the resulting material was shown to reversibly bend when exposed to organic solvents.258 The MWCNTs were shown to result in an increase of the tensile strength of the composite to ca. 290 MPa (at 30% w/w), whereas the tensile strength of the neat polymer was only ca. 16.5 MPa. The underlying actuation mechanism revolves around the interactions between the polymer and the oriented filler, which ultimately also promote some alignment of the polymer chains.259 When exposed to ethanol the PTP swells, while upon evaporation of the solvent the PTP contracts, resulting in the generation of a force with a stress of ca. 15 MPa. The overall bending of the film was found to increase with increasing PTP content of the material while the bending rate was found to be concomitant with increased temperatures that facilitated the evaporation of ethanol. A polyimide blend was recently shown to mechanically respond to moisture gradients by bending.260 When a rigid poly(aniline-co-aniline sulfonic acid) (PANI) copolymer was embedded in a flexible polyimide matrix, a microstructure was generated that allowed rapid water exchange, thus swelling the polyimide component. As a consequence, turgorlike pressure is applied to the stiff PANI which contributes to the elastic elongation of the material toward the water source. Indeed this behavior was shown to be reminiscent of the leaves of Mimosa pudica that, similarly to the Venus flytrap, contract upon contact. This similarity was more prominent when triggered merely by the moisture of a finger, the polyimide-PANI films were shown to rapidly deform. The combination of the anisotropic swelling of hydrogels containing aligned cellulose nanofibrils with 3D printing techniques was reported toward the generation of “4D” bioinspired structures.261 To achieve this, nanofibrillated cellulose from soft wood pulp was used as the key component in an photopolymerizable ink containing water, an acrylamide monomer (either N-isopropylacrylamide or N,N′-dimethylacrylamide), hectorite clay, a photoinitiator, and glucose and glucose 12878

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 39. Schematic representations of (a) the shear-assisted alignment of cellulose fibrils during the printing of the hydrogel composite ink and (b) the effect of the alignment on the swelling of the printed structures. Confocal microscopy images of the composites demonstrating the alignment of cellulose fibrils (stained blue) when the ink is (c) casted, (d) printed, and (e) patterned (scale bar: 200 μm). Pictures of (f) a lily flower used as (g) inspiration for the design of a print path of a structure (h) which, after printing and upon swelling, adopts a curvature similar to that of the flower. Adapted with permission from ref 261. Copyright 2016 Macmillan Publishers Ltd.: Nature Materials.

which macroscopically results in their shape-shifting267 and combine it with the elastic properties of polymers. In these examples, reversible actuation upon stimulation can take place, on account of the orientation of the mesogens within the liquid crystal elastomers (LCEs).268−271 Perhaps the most studied motifs in LCEs are azobenzene-based molecules which upon cis−trans isomerization alter the order of the liquid crystal phase.272 Taking advantage of this property, the helical twisting of an azobenzene-containing polymeric network was reported.273,274 A film composed of a cross-linked polymer containing azobenzene moieties was doped with a chiral molecule thus inducing a twist in the orientation of the liquid crystal director which progressively changes from the bottom to the top surface of the film (Figure 40). The film was then cut in strips at different angles which resulted in their curling at angles and pitches that were correlated with the cutting angle. A similar behavior was observed when the dopant chirality was switched, whereby mirrored curling of the films was observed. Upon UV irradiation, left-handed spirals were shown to decrease in pitch, whereas right-handed spirals were found to increase. The winding and unwinding of the spirals was accompanied by an overall contraction (up to 60% of the original length) and elongation (up to 40% of the original length), respectively, of the films. This behavior was reversible upon irradiation with visible light and was thus associated with the isomerization of the azobenzene moieties. Taking advantage of the observed properties of these films, a tendril-mimicking spring was prepared whereby films of opposite helicity were joined at a kink. The material simultaneously coiled and uncoiled upon irradiation which results in the kink moving along the axis of the spirals. This was further exploited by attaching a small magnet to

oxidase as oxygen scavengers. The clay acted as a rheological modifier and a physical cross-linker262,263 while the cellulose fibrils bundle to microfibrils, which due to their high aspect ratio and Young’s modulus, increase the composite’s stiffness. The ink was used to print three-dimensional structures that were subsequently photopolymerized, and the resulting materials could readily swell in water. The printing process promoted the shear-induced alignment of the cellulose fibrils,264 which in turn allowed creating complex structures in which the overall shape and the local orientation of the cellulose fibrils (and therefore the swelling characteristics of the material) could be controlled (Figure 39). Films processed by solution casting having the same compositions resulted in an isotropic arrangement of the cellulose fibrils (Figure 39c). The control of the swelling behavior of the printed composites was elegantly demonstrated by printing a range of biomimetic architectures, predominantly composed of bilayers where the orientation of the cellulose fibrils differed for each layer, and, upon exposure to moisture, the preprogrammed shape was adopted,265 thus mimicking the actuation behavior of natural prototypes. Although liquid crystals constitute an integral part of the development of polymeric actuators, only a few examples exist where there is a clear correlation between the underlying mechanism and a biological actuator-model. Note that although the notion of liquid crystals being “synthetic muscles” appears in numerous publications, there is in fact little resemblance in the way the actuation takes place as skeletal muscles expand and contract as a result of numerous complex biochemical and metabolic processes.266 Nonetheless, a few notable examples take advantage of the ability of liquid crystals to anisotropically change the local volume they occupy through their orientation, 12879

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 40. (a) Schematic representation of the molecular organization of azobenzene-based LCEs containing a chiral dopant and (b) schematics and pictures of the ribbons from the parent film that spontaneously curls depending on the cutting angle. (c) Ribbons of opposite helicity joined at a kink exhibit opposite curling upon irradiation. Adapted with permission from ref 273. Copyright 2014 Macmillan Publishers Ltd.: Nature Chemistry.

could convert the mechanical force from the bending film into electrical power. Furthermore, imitating the curling of plant tendrils, a long ribbon of the BHSB-containing hydrogels was shown to uncoil and expand upon irradiation, a behavior that was also replicated by exposing the material to a flow of humid air.

the kink that, upon alternating UV and visible irradiation, also moved with the kink and was shown to be able to move another magnet placed near the tendril-mimicking device. An acidochromic fluorophore, namely 1,4-bis(phydroxystyryl)benzene (BHSB), was incorporated in an agarose-based hydrogel that was shown to exhibit reversible pH-responsive actuating properties.275 The guest molecule, BHSB, was embedded in the agarose matrix at a concentration of 1% w/w, and a film was prepared which, on account of the intrinsic properties of BHSB, was shown to be able to convert both light and humidity into mechanical work. At low pH values, BHSB displays blue fluorescence (ca. 432 nm), while at high pH values yellow fluorescence (ca. 530 nm), when excited with UV irradiation; however, when embedded in the polymer matrix, irradiation with UV light induced the macroscopic bending of the film which was attributed to the isomerization of BHSB. Reminiscing of the behavior previously discussed for liquid crystalline elastomers, it was proposed that indeed the alignment of the BHSB and subsequent trans to cis isomerization upon irradiation was responsible for the type of ensuing motion on account of an anisotropic deformation of the matrix. The process was shown to be slowly reversible, upon irradiation with visible light. Due to the hydrophilic nature of the hydrogel matrix, the material was also shown to respond to humidity, a property that was harnessed by exposing the film to a humidity gradient, allowing its implementation in a piezoelectric device, which

4.4. Actuating Hydrogels Based on Compositional Drift

Swelling of plant cells bestows motion though the osmotic flow of water, a property that can be replicated in the synthetic world by hydrogels276 (i.e., three-dimensional cross-linked polymeric networks swollen with water). Indeed, such materials have been widely employed in actuators due to the fact that they undergo large volume changes in relatively narrow ranges of changes in conditions (such as temperature, ionic strength, and pH).277 Perhaps their major drawback is their size- and geometrydependent rate of response, as it is almost exclusively a result of the diffusion of small molecules through its structure.278 One of the key parameters that determine hydrogel properties is the cross-linking density, which not only dictates the swelling limitations of the material overall but also locally. As such, the variation in cross-link density has been employed to achieve controlled movement.279 A hydrogel with a gradient cross-link density composed primarily of PNIPAM was demonstrated to fold upon increasing the temperature above the LCST of the polymer (Figure 41).280 The material was prepared by hydrothermal reaction of 4-hydroxybutyl acrylate (HBA) with 12880

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 41. (a) Schematic illustration of the synthetic process toward gradient porous hydrogels showing the copolymerization of HBA and NIPAm, and the simultaneous precipitation and cross-linking and the resulting gradient porosity. The latter was observed by (b) scanning electron microscopy images of cross sections of the hydrogels. (c) An eight-point star-shaped hydrogel sliced into thin layers which close after being triggered by thermal stimulus to a different extent. Reproduced with permission from ref 280. Copyright 2015 John Wiley & Sons, Inc.

increased above the LCST of the polymer. The effect of the gradient was demonstrated by slicing the star along the gradient axis thus forming thinner star-shaped hydrogels that, upon heating, folded to a different extent (Figure 41c). Further to this initial observation, poly(pyrrole) nanoparticles were embedded in the hydrogel, thus allowing the photothermal actuation of the material with NIR irradiation. As a result of the gradient porous structure of the hydrogel, regardless of the direction of the irradiation, the bending of the material was always toward the larger pore side. Inspired by the movement of octopuses, the middle part of a porous hydrogel strip was irradiated resulting in its folding in the direction of the larger pores, in a manner similar to the trailing arms of the octopus. It is noteworthy that

NIPAM in the presence of ammonium persulfate, thus resulting in a hydroxyl-functional PNIPAM copolymer, which simultaneously precipitated and cross-linked the latter as a result of an intermolecular dihydroxylation. As a result, a gradient crosslinking density was obtained, which macroscopically manifested itself by a dense structure at the bottom of the material which gradually turned into an open “porous” structure toward the top (Figure 41, panels a and b). The formed gradient porous polymer was shown to bend at temperatures above the LCST of NIPAM with the response being rapid (ca. 35 s) and fully reversible, upon cooling of the aqueous solution. It was proposed that the hydrogel could perform as a soft robot: a star-shaped gradient hydrogel was shown to reversibly fold when the temperature was 12881

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 42. (a) Schematic representation of the proposed mechanism leading to the reversible floating of a copolymer hydrogel upon heating on account of the density switching upon crystallization or melting of the alkyl chains of the polymer. (b) Photographs demonstrating the floating/sinking of hydrogels with different compositions (left: 53% stearyl acrylate; right: 82% stearyl acrylate) upon changing the water temperature: the latter does not reach a density greater than that of water, hence no sinking is observed. (c) Dependency of the hydrogel density on temperature with respect to the density of water shown in green. (d) Differential scanning calorimetry of samples of different compositions indicating the extent of crystallization of the alkyl chains. Reproduced with permission from ref 281. Copyright 2015 John Wiley & Sons, Inc.

Figure 43. (a) Schematic representation of the double curved hydrogels with embedded microfluidic channels and their actuation mechanism upon uptake of the solvent. The inset is an SEM image showing the channels. (b) Photographs and schematic representation of the jumping device showing the time-dependent accumulation and release of elastic energy upon exposure to solvent. Reproduced with permission from ref 282. Copyright 2010 The Royal Society of Chemistry.

propulsion was possible because of the rapid photoresponse, thus rendering the propulsive force stronger than the drag force from

water resistance. The irradiation process was repeated to displace the gel in length scales larger than the material.280 12882

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Figure 44. (a) Schematic representation of a composite patterned (striped) gel composed of PNIPAM/PAMPS interpenetrating strips and its adopted helical shape upon action of a stimulus, such as a NaCl solution. (b) Photographs demonstrating the handedness and pitch of gels with stripes at different angles after incubation in saline solution. (c) Dependence of the number of turns (N) and pitch (p) of the actuated gels on the solution salinity. Reproduced with permission from ref 284. Copyright 2013 Macmillan Publishers Ltd.: Nature Communications.

which glass fibers were partially embedded.223 Owing to the highly water-absorbing PDMA core, exposure to humidity resulted in the swelling of the hydrogel and subsequent spreading of the glass fibers. This process was shown to be reversible upon drying. Polymeric interpenetrating networks have been the focus of studies aiming at improving the mechanical properties of hydrogels.82 This principle was exploited in an attempt to mimic the helical transitions displayed upon drying by tissue fibers in various plants by stimulating a patterned interpenetrating hydrogel strip.283 The material was prepared by impregnating a PNIPAM hydrogel sheet with NIPAM, a sulfonic acid acrylamide (2-acrylamido-2-methylpropanesulfonic acid, AMPS), a cross-linker (N,N-methylene bis(acrylamide), MBAA), and a radical initiator, and it was exposed to UV irradiation under a striped photomask to initiate polymerization in the exposed areas. Upon immersion of the film in a saline solution, a twisting into a helix motion was observed the pitch (p) and number of turns (N) of which was found to be related to the concentration of NaCl in the solution (Figure 44c). Furthermore, the helicity of the twist was shown to be tunable by altering the angle of the hydrogel stripes (Figure 44b). Contrary to a neat PNIPAM gel, the patterned hydrogels showed no sharp transitions in dimensions or Young’s modulus, which was attributed to the retention of water by the PAMPS component. On the basis of this observation, a mathematical model was generated that could predict the folding of striped hydrogels based on the thickness of the film and the thickness of the respective stripes. As such, the programming of complex structures was shown to be possible. In a three-step photopolymerization, two layers of oppositely striped PNIPAM hydrogels that were embedded in a PAA polymer network were prepared.284,285 Upon immersion in water, the material adopts a slightly twisted shape as a result of water uptake, while increasing the pH above the pKa of PAA results in the adoption of a compact right-handed helix. This was shown to be a result of the different swelling ratios of the two components, while the respective mechanical properties were shown to be dependent on the pH. Indeed, the Young’s modulus of the neat PNIPAM component was shown to be virtually unaffected by the pH (ca. 97 kPa at pH 1 and ca. 87 kPa at pH 9), while in the case of PAA it decreased significantly (from ca. 111

A fascinating example of a bioinspired stimuli-responsive actuator was reported by Wang et al., who copolymerized stearyl acrylate and methacrylic acid in the presence of reduced graphene oxide to create a material that altered its effective density in response to temperature changes.281 The pendant alkyl chains of the stearyl acrylate crystallize into a dense-ordered structure; melting of the latter causes a decrease of the (local) density. With dependence on the copolymer composition, the density of the overall material was shown to be tunable to a value greater than that of water, thus the material was shown to “dive” when placed in water, while it would float upon increasing the temperature above the melting point (Figure 42). Exploiting the NIR absorption of the reduced graphene oxide content of the hydrogel, a similar density changing behavior was shown when the sample was irradiated as a result of the photothermal effect inducing the melting of the alkyl chain and the subsequent decrease in density. Similar to the way Venus flytraps snap, a double-curved PEGbased hydrogel sheet with embedded channels was prepared via stereolithography.282 The convex curvature of the hydrogel imparts elastic instability that, upon stimulation, is rapidly released. Three microfluidic channels were also incorporated into the body of the hydrogel, which resulted in the increase of the surface area of the gel and permitted fast delivery of solvent across the body of the polymer, thus overcoming slow diffusion constraints (Figure 43). The directional swelling of the doubly curved hydrogel was achieved through the vertical alignment of the microfluidic channels. Upon uptake of solvent from the channels, it is diffused both laterally and along the channels, although the vertical diffusion is significantly faster. As a result, local swelling around the channels is responsible for the directional swelling of the material and, as a result, snap-buckling occurs. To demonstrate the extent of the fast water uptake, a device composed of a body and two legs made of doubly curved hydrogels with embedded channels was prepared. When exposing one leg to the solvent, capillary forces rapidly transport the solvent throughout the material resulting in its bending and accumulation of elastic energy. Upon drying, the energy is released and the device snaps into its original shape resulting in a leap. Mimicking the opening of the pappi of dandelions upon hydration, an acrylamide-based hydrogel was prepared into 12883

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

contingent on the polymeric counterpart. Some recent such examples involve the use of cardiomyocytes on a polymer film. The bilayers deflect in 3D shapes depending on the direction of the biological tissue.286−288

kPa at pH 1 to ca. 26 at pH 9), a behavior that was translated in the case of the interpenetrating gel (ca. 7100 kPa at pH 1 and ca. 1900 kPa at pH 9). This approach was taken a step further by preparing a layered striped hydrogel composed of four different cross-linked polymers: a layer of alternating PAA and PNIPAM and a layer of alternating poly(1-vinylimidazole-co-acrylamide) (PVI-AAM) and PNIPAM stripes (Figure 45). The PVI-AAM

5. CONCLUSIONS AND OUTLOOK The majority of the artificial mechanically adaptive systems discussed here gather inspiration from various hierarchical nanostructures found in nature. As in biological systems, the presence of secondary (or higher) structures enables the combination of (in principle) orthogonal functionalities such as toughness and stiffness. Such mechanically adaptive materials take advantage of energetically insignificant stimuli to alter these properties; however, the resulting effect can be quite dramatic. With respect to sea cucumber mimics, it is evident that interactions of the stiffening components are key to direct the macroscopic observed, and although these are often weak (e.g., hydrogen bonding), one can consider the extent of the mechanical contrast and reflect on the possible implications of the reversible switching of stronger interactions. Concerning the development of polymers that display reversible strain hardening, remarkably high toughness due to the presence of energyabsorbing folded nanodomains or sacrificial supramolecular links was shown. Indeed, hydrogen bonds and metal−ligand complexes play a key role in many of the discussed materials; these supramolecular interactions are excellent reversible links to access a variety of functions, including stiffness-modulation, shape-memory, actuation, and strain-hardening. The hysteresis and slow recovery displayed by many of the reviewed systems is perhaps their most important drawback if one thinks about future applications. However, this is an intrinsic limitation of supramolecular polymers, in which a trade-off between fast dynamics and acceptable mechanical properties must be made. Alternative approaches will thus be required to access mechanically adaptive materials with very fast responses. Furthermore, while it is wellunderstood that the (re)orientation of these reinforcing components can induce macroscopic movement of the overall material, only few examples have coupled the mechanical properties with the extent of the actuation. When actuation was shown to be a result of anisotropic deformation of the material, one typical drawback was the slow effect of the stimulus, often as a result of diffusion restrictions. Nonetheless, a few ways to overcome these have surfaced in recent literature reports, and it is not inconceivable that more such studies will emerge. Despite the potential of mechanically adaptive materials for various technological applications, the great majority of the works collected in this review have a fundamental motivation. This may point to the necessity to first develop a better understanding of structure−property relationships in these materials before actual devices can be developed in a rational manner; however, this review demonstrates that a wealth of knowledge in the field is already at hand. In fact, a few examples clearly hint to interesting applications such as minimally invasive shape-memory medical devices, the toughening of rubbers through the introduction of reversible sacrificial bonds, or the development of interfacing robots with biological tissues. It is therefore not unreasonable to expect that within the next few years the sprouting of exciting technologies based on mechanically adaptive polymer-based materials will be in the forefront of research.

Figure 45. Shape transformations of composite hydrogels with different responsive polymers patterned in the upper and bottom layers. At pH 9, the PAA at the bottom of the hydrogel swells inducing a right-handed helix formation. At pH 1, P(VI-co-AAM) at the top of the hydrogel swells and drives the (a) formation of a left-handed helix, (b) rolls, or (c) a right-handed helix, depending on the orientation of the stripes. The green, brown, and gray stripes in the schemes correspond to PAA, P(VIco-AAM), and PNIPAM gels. Reproduced with permission from ref 284. Copyright 2016 The Royal Society of Chemistry.

copolymer introduces another level of complexity as it swells at low pH values. Thus, by altering the orientation of the stripes and the pH, the hydrogel composite was shown to curl into different chirality and pitch helices, depending on the relative swelling of the components. Although the mechanism behind natural actuators is not always understood, the basic principles have been shown to be an inspiration toward the preparation of a wide range of actuators, some of which have been outlined herein. By simplifying the model often encountered in natural actuators whereby cellulose acts as an anisotropic filler that regulates the water-induced swelling of the matrix (c.f. section 4.1), a variety of synthetic actuators relying on the premises of directional swelling introduced by a rigid component were investigated. In some cases, the alignment and orientation of the rigid filler was shown to dramatically affect the stimuli-responsive actuation of the material. Also mimicking a simplified model of natural actuators, numerous synthetic actuators were discussed that relied on multilayered (mostly bilayered) films. The differential swelling of the components introduces local stresses that effectively are responsible for the actuation of the material. While many of these actuators were based on polymer hydrogels, it was shown that in some cases, hydrogels can also be actuated. In this case, a gradient is introduced to the material, thus allowing the anisotropic swelling of the polymer and thus its directional deformation. It is apparent that novel and efficient actuators are constantly developed while advances in “smart” polymers are largely responsible for the progress of the field. Another noteworthy direction for advanced polymer-based actuators is that of biohybrid actuators. Such materials rely on a biological component to provide motion; however, their properties are 12884

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

AUTHOR INFORMATION

National Center of Competence in Research Bio-Inspired Materials.

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected].

REFERENCES (1) Lepora, N. F.; Verschure, P.; Prescott, T. J. The State of the Art in Biomimetics. Bioinspiration Biomimetics 2013, 8 (1), 013001. (2) Bauer, S.; Bauer-Gogonea, S.; Graz, I.; Kaltenbrunner, M.; Keplinger, C.; Schwödiauer, R. 25th Anniversary Article: A Soft Future: From Robots and Sensor Skin to Energy Harvesters. Adv. Mater. 2014, 26 (1), 149−162. (3) Nessim, M. A. Biomimetic Architecture as a New Approach for Energy Efficient Buildings through Smart Building Materials. J. Green Build. 2015, 10 (4), 73−86. (4) Kar, A. K. Bio Inspired Computing − a Review of Algorithms and Scope of Applications. Expert Syst. Appl. 2016, 59, 20−32. (5) Forterre, Y.; Skotheim, J. M.; Dumais, J.; Mahadevan, L. How the Venus Flytrap Snaps. Nature 2005, 433 (7024), 421−425. (6) Allen, J. J.; Bell, G. R. R.; Kuzirian, A. M.; Hanlon, R. T. Cuttlefish Skin Papilla Morphology Suggests a Muscular Hydrostatic Function for Rapid Changeability. J. Morphol. 2013, 274 (6), 645−656. (7) Schirhagl, R.; Weder, C.; Lei, J.; Werner, C.; Textor, H. M. Bioinspired Surfaces and Materials. Chem. Soc. Rev. 2016, 45 (2), 234− 236. (8) Heinzmann, C.; Weder, C.; de Espinosa, L. M. Supramolecular Polymer Adhesives: Advanced Materials Inspired by Nature. Chem. Soc. Rev. 2016, 45 (2), 342−358. (9) Stuart, M. A. C.; Huck, W. T. S.; Genzer, J.; Muller, M.; Ober, C.; Stamm, M.; Sukhorukov, G. B.; Szleifer, I.; Tsukruk, V. V.; Urban, M.; et al. Emerging Applications of Stimuli-Responsive Polymer Materials. Nat. Mater. 2010, 9 (2), 101−113. (10) Roy, D.; Cambre, J. N.; Sumerlin, B. S. Future Perspectives and Recent Advances in Stimuli-Responsive Materials. Prog. Polym. Sci. 2010, 35 (1−2), 278−301. (11) Gil, E. S.; Hudson, S. M. Stimuli-Reponsive Polymers and Their Bioconjugates. Prog. Polym. Sci. 2004, 29 (12), 1173−1222. (12) Saavedra Flores, E. I.; Friswell, M. I.; Xia, Y. Variable Stiffness Biological and Bio-Inspired Materials. J. Intell. Mater. Syst. Struct. 2013, 24 (5), 529−540. (13) Studart, A. R. Biologically Inspired Dynamic Material Systems. Angew. Chem., Int. Ed. 2015, 54 (11), 3400−3416. (14) Cousins, W. J. Young’s Modulus of Hemicellulose as Related to Moisture Content. Wood Sci. Technol. 1978, 12 (3), 161−167. (15) Fleischer, A.; O’Neill, M. A.; Ehwald, R. The Pore Size of NonGraminaceous Plant Cell Walls Is Rapidly Decreased by Borate Ester Cross-Linking of the Pectic Polysaccharide Rhamnogalacturonan II. Plant Physiol. 1999, 121 (3), 829−838. (16) O’Neill, M. A.; Eberhard, S.; Albersheim, P.; Darvill, A. G. Requirement of Borate Cross-Linking of Cell Wall Rhamnogalacturonan II for Arabidopsis Growth. Science 2001, 294 (5543), 846−849. (17) Zhang, Z.; Zhang, Y.-W.; Gao, H. On Optimal Hierarchy of LoadBearing Biological Materials. Proc. R. Soc. London, Ser. B 2011, 278 (1705), 519−525. (18) Luz, G. M.; Mano, J. F. Biomimetic Design of Materials and Biomaterials Inspired by the Structure of Nacre. Philos. Trans. R. Soc., A 2009, 367 (1893), 1587−1605. (19) Wanasekara, N. D.; Korley, L. T. J. Toward Tunable and Adaptable Polymer Nanocomposites. J. Polym. Sci., Part B: Polym. Phys. 2013, 51 (7), 463−467. (20) Studart, A. R. Towards High-Performance Bioinspired Composites. Adv. Mater. 2012, 24 (37), 5024−5044. (21) Stone, D. A.; Korley, L. T. J. Bioinspired Polymeric Nanocomposites. Macromolecules 2010, 43 (22), 9217−9226. (22) Xia, Z. Adaptive and Self-Shaping Materials. In Biomimetic Principles and Design of Advanced Engineering Materials; John Wiley & Sons, Ltd, 2016; pp 79−100. (23) Oliver, K.; Seddon, A.; Trask, R. S. Morphing in Nature and Beyond: A Review of Natural and Synthetic Shape-Changing Materials and Mechanisms. J. Mater. Sci. 2016, 51 (24), 10663−10689.

ORCID

Dafni Moatsou: 0000-0002-3497-719X Christoph Weder: 0000-0001-7183-1790 Notes

The authors declare no competing financial interest. Biographies Dr. Lucas Montero de Espinosa is a Swiss National Science Foundation Ambizione researcher and team leader at the Adolphe Merkle Institute (AMI) of the University of Fribourg (Switzerland). Lucas studied Chemistry at the Universidad Complutense de Madrid (Spain), obtained his Ph.D. degree from the Universitat Rovira i Virgili (Tarragona, Spain), and held postdoctoral positions at the University of Potsdam (Germany), the Karlsruhe Institute of Technology (Germany), and the AMI. Since 2014, he has worked in the group of Christoph Weder, where he leads a team that focuses on the study of structure−property relationships in supramolecular polymers. Worarin Meesorn received his BSc degree in Chemistry in 2012 from Chiang Mai University (Thailand) and his MSc in Polymer Science in 2014 from the Petroleum and Petrochemical College at Chulalongkorn University in Bangkok (Thailand). He is currently a Ph.D. student in Polymer Chemistry and Materials at the Adolphe Merkle Institute (AMI) of the University of Fribourg (Switzerland) under the supervision of Lucas Montero and Christoph Weder. His research focuses on new approaches for the development of bioinspired nanocomposites with stimulus-responsive mechanical properties. Dr. Dafni Moatsou studied Materials Science and Technology at the University of Crete (Greece) and obtained a Ph.D. in Chemistry from the University of Warwick (United Kingdom) in 2015 working on precision polymer synthesis, polymer−protein bioconjugates, and functional nanoparticles. She is currently working as a Marie Skłodowska-Curie postdoctoral fellow at the Adolphe Merkle Institute (Switzerland), where her research in the group of Christoph Weder focuses on novel supramolecular polymers and bioinspired adaptive materials. Prof. Dr. Christoph Weder is Director of the Adolphe Merkle Institute (AMI) at the University of Fribourg (Switzerland) and leads the Swiss National Center of Competence in Research Bio-Inspired Materials. Chris was educated at ETH Zurich and held positions at the Massachusetts Institute of Technology, ETH Zurich, and Case Western Reserve University, before joining the AMI as Professor for Polymer Chemistry and Materials in 2009. His research interests include the design, synthesis, and investigation of bioinspired stimuli-responsive polymers and nanomaterials. He is a member of the Swiss Academy of Engineering Sciences and serves as associate editor for ACS Macro Letters and coeditor of the RSC Book Series Polymer Chemistry.

ACKNOWLEDGMENTS This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie Grant 704734 and the Adolphe Merkle Foundation. L.M.E. is thankful for funding through the Ambizione program of the Swiss National Science Foundation (SNF), W.M. thanks the Swiss Confederation for a doctoral scholarship, and C.W. appreciates funding from the Swiss 12885

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

(44) Mercanzini, A.; Cheung, K.; Buhl, D.; Boers, M.; Maillard, A.; Colin, P.; Bensadoun, J. C.; Bertsch, A.; Carleton, A.; Renaud, P. 2007 IEEE 20th International Conference on Micro Electro Mechanical Systems (MEMS), Hyogo, Japan, Jan 21−25, 2007; p 573−576. (45) Arreaga-Salas, D. E.; Avendaño-Bolívar, A.; Simon, D.; Reit, R.; Garcia-Sandoval, A.; Rennaker, R. L.; Voit, W. Integration of HighCharge-Injection-Capacity Electrodes onto Polymer Softening Neural Interfaces. ACS Appl. Mater. Interfaces 2015, 7 (48), 26614−26623. (46) Shanmuganathan, K.; Capadona, J. R.; Rowan, S. J.; Weder, C. Biomimetic Mechanically Adaptive Nanocomposites. Prog. Polym. Sci. 2010, 35 (1−2), 212−222. (47) Shanmuganathan, K.; Capadona, J. R.; Rowan, S. J.; Weder, C. Bio-Inspired Mechanically-Adaptive Nanocomposites Derived from Cotton Cellulose Whiskers. J. Mater. Chem. 2010, 20 (1), 180−186. (48) Shanmuganathan, K.; Capadona, J. R.; Rowan, S. J.; Weder, C. Stimuli-Responsive Mechanically Adaptive Polymer Nanocomposites. ACS Appl. Mater. Interfaces 2010, 2 (1), 165−174. (49) Dagnon, K. L.; Shanmuganathan, K.; Weder, C.; Rowan, S. J. Water-Triggered Modulus Changes of Cellulose Nanofiber Nanocomposites with Hydrophobic Polymer Matrices. Macromolecules 2012, 45 (11), 4707−4715. (50) Capadona, J. R.; Van Den Berg, O.; Capadona, L. A.; Schroeter, M.; Rowan, S. J.; Tyler, D. J.; Weder, C. A Versatile Approach for the Processing of Polymer Nanocomposites with Self-Assembled Nanofibre Templates. Nat. Nanotechnol. 2007, 2 (12), 765−769. (51) Annamalai, P. K.; Dagnon, K. L.; Monemian, S.; Foster, E. J.; Rowan, S. J.; Weder, C. Water-Responsive Mechanically Adaptive Nanocomposites Based on Styrene−Butadiene Rubber and Cellulose NanocrystalsProcessing Matters. ACS Appl. Mater. Interfaces 2014, 6 (2), 967−976. (52) Jorfi, M.; Roberts, M. N.; Foster, E. J.; Weder, C. Physiologically Responsive, Mechanically Adaptive Bio-Nanocomposites for Biomedical Applications. ACS Appl. Mater. Interfaces 2013, 5 (4), 1517−1526. (53) Liu, M.; Peng, Q.; Luo, B.; Zhou, C. The Improvement of Mechanical Performance and Water-Response of Carboxylated SBR by Chitin Nanocrystals. Eur. Polym. J. 2015, 68, 190−206. (54) Way, A. E.; Hsu, L.; Shanmuganathan, K.; Weder, C.; Rowan, S. J. pH-Responsive Cellulose Nanocrystal Gels and Nanocomposites. ACS Macro Lett. 2012, 1 (8), 1001−1006. (55) Wanasekara, N. D.; Stone, D. A.; Wnek, G. E.; Korley, L. T. J. Stimuli-Responsive and Mechanically-Switchable Electrospun Composites. Macromolecules 2012, 45 (22), 9092−9099. (56) Stone, D. A.; Wanasekara, N. D.; Jones, D. H.; Wheeler, N. R.; Wilusz, E.; Zukas, W.; Wnek, G. E.; Korley, L. T. J. All-Organic, StimuliResponsive Polymer Composites with Electrospun Fiber Fillers. ACS Macro Lett. 2012, 1 (1), 80−83. (57) McKee, J. R.; Hietala, S.; Seitsonen, J.; Laine, J.; Kontturi, E.; Ikkala, O. Thermoresponsive Nanocellulose Hydrogels with Tunable Mechanical Properties. ACS Macro Lett. 2014, 3 (3), 266−270. (58) Arvidson, S. A.; Lott, J. R.; McAllister, J. W.; Zhang, J.; Bates, F. S.; Lodge, T. P.; Sammler, R. L.; Li, Y.; Brackhagen, M. Interplay of Phase Separation and Thermoreversible Gelation in Aqueous Methylcellulose Solutions. Macromolecules 2013, 46 (1), 300−309. (59) Lott, J. R.; McAllister, J. W.; Arvidson, S. A.; Bates, F. S.; Lodge, T. P. Fibrillar Structure of Methylcellulose Hydrogels. Biomacromolecules 2013, 14 (8), 2484−2488. (60) Das, P.; Malho, J.-M.; Rahimi, K.; Schacher, F. H.; Wang, B.; Demco, D. E.; Walther, A. Nacre-Mimetics with Synthetic Nanoclays up to Ultrahigh Aspect Ratios. Nat. Commun. 2015, 6, 5967. (61) Espinosa, H. D.; Rim, J. E.; Barthelat, F.; Buehler, M. J. Merger of Structure and Material in Nacre and Bone − Perspectives on De Novo Biomimetic Materials. Prog. Mater. Sci. 2009, 54 (8), 1059−1100. (62) Nassif, N.; Pinna, N.; Gehrke, N.; Antonietti, M.; Jäger, C.; Cölfen, H. Amorphous Layer around Aragonite Platelets in Nacre. Proc. Natl. Acad. Sci. U. S. A. 2005, 102 (36), 12653−12655. (63) Zhu, B.; Noack, M.; Merindol, R.; Barner-Kowollik, C.; Walther, A. Light-Adaptive Supramolecular Nacre-Mimetic Nanocomposites. Nano Lett. 2016, 16 (8), 5176−5182.

(24) Moatsou, D.; Weder, C. Mechanically Adaptive Nanocomposites Inspired by Sea Cucumbers. In Bio-Inspired Polymers; The Royal Society of Chemistry: London, 2017; Chapter 12, pp 402−428. (25) Thurmond, F.; Trotter, J. Morphology and Biomechanics of the Microfibrillar Network of Sea Cucumber Dermis. J. Exp. Biol. 1996, 199 (8), 1817−1828. (26) Motokawa, T. The Stiffness Change of the Holothurian Dermis Caused by Chemical and Electrical Stimulation. Comp. Biochem. Physiol., C: Comp. Pharmacol. 1981, 70 (1), 41−48. (27) Motokawa, T. Effects of Ionic Environment on Viscosity of Triton-Extracted Catch Connective Tissue of a Sea Cucumber Body Wall. Comp. Biochem. Physiol., B 1994, 109 (4), 613−622. (28) Motokawa, T.; Tsuchi, A. Dynamic Mechanical Properties of Body-Wall Dermis in Various Mechanical States and Their Implications for the Behavior of Sea Cucumbers. Biol. Bull. 2003, 205 (3), 261−275. (29) Szulgit, G. K.; Shadwick, R. E. Dynamic Mechanical Characterization of a Mutable Collagenous Tissue: Response of Sea Cucumber Dermis to Cell Lysis and Dermal Extracts. J. Exp. Biol. 2000, 203 (10), 1539−1550. (30) Trotter, J.; Koob, T. Evidence That Calcium-Dependent Cellular Processes Are Involved in the Stiffening Response of Holothurian Dermis and That Dermal Cells Contain an Organic Stiffening Factor. J. Exp. Biol. 1995, 198 (9), 1951−1961. (31) Trotter, J. A.; Lyons-Levy, G.; Chino, K.; Koob, T. J.; Keene, D. R.; Atkinson, M. A. L. Collagen Fibril Aggregation-Inhibitor from Sea Cucumber Dermis. Matrix Biol. 1999, 18 (6), 569−578. (32) Trotter, J. A.; Lyons-Levy, G.; Luna, D.; Koob, T. J.; Keene, D. R.; Atkinson, M. A. L. Stiparin: A Glycoprotein from Sea Cucumber Dermis That Aggregates Collagen Fibrils. Matrix Biol. 1996, 15 (2), 99−110. (33) Koob, T. J.; Koob-Emunds, M. M.; Trotter, J. A. Cell-Derived Stiffening and Plasticizing Factors in Sea Cucumber (Cucumaria Frondosa) Dermis. J. Exp. Biol. 1999, 202, 2291−2301. (34) Tipper, J. P.; Lyons-Levy, G.; Atkinson, M. A. L.; Trotter, J. A. Purification, Characterization and Cloning of Tensilin, the CollagenFibril Binding and Tissue-Stiffening Factor from Cucumaria Frondosa Dermis. Matrix Biol. 2002, 21 (8), 625−635. (35) Capadona, J. R.; Shanmuganathan, K.; Tyler, D. J.; Rowan, S. J.; Weder, C. Stimuli-Responsive Polymer Nanocomposites Inspired by the Sea Cucumber Dermis. Science 2008, 319 (5868), 1370−1374. (36) Eichhorn, S. J.; Dufresne, A.; Aranguren, M.; Marcovich, N. E.; Capadona, J. R.; Rowan, S. J.; Weder, C.; Thielemans, W.; Roman, M.; Renneckar, S.; et al. Review: Current International Research into Cellulose Nanofibres and Nanocomposites. J. Mater. Sci. 2010, 45 (1), 1−33. (37) Sacui, I. A.; Nieuwendaal, R. C.; Burnett, D. J.; Stranick, S. J.; Jorfi, M.; Weder, C.; Foster, E. J.; Olsson, R. T.; Gilman, J. W. Comparison of the Properties of Cellulose Nanocrystals and Cellulose Nanofibrils Isolated from Bacteria, Tunicate, and Wood Processed Using Acid, Enzymatic, Mechanical, and Oxidative Methods. ACS Appl. Mater. Interfaces 2014, 6 (9), 6127−6138. (38) Favier, V.; Chanzy, H.; Cavaille, J. Y. Polymer Nanocomposites Reinforced by Cellulose Whiskers. Macromolecules 1995, 28 (18), 6365−6367. (39) Dufresne, A. Dynamic Mechanical Analysis of the Interphase in Bacterial Polyester/Cellulose Whiskers Natural Composites. Compos. Interfaces 2000, 7 (1), 53−67. (40) Dufresne, A.; Kellerhals, M. B.; Witholt, B. Transcrystallization in Mcl-PHAs/Cellulose Whiskers Composites. Macromolecules 1999, 32 (22), 7396−7401. (41) Ruiz, M. M.; Cavaillé, J. Y.; Dufresne, A.; Gérard, J. F.; Graillat, C. Processing and Characterization of New Thermoset Nanocomposites On the basis of Cellulose Whiskers. Compos. Interfaces 2000, 7 (2), 117− 131. (42) Jorfi, M.; Skousen, J. L.; Weder, C.; Capadona, J. R. Progress Towards Biocompatible Intracortical Microelectrodes for Neural Interfacing Applications. J. Neural. Eng. 2015, 12 (1), 011001. (43) Capadona, J. R.; Tyler, D. J.; Zorman, C. A.; Rowan, S. J.; Weder, C. Mechanically Adaptive Nanocomposites for Neural Interfacing. MRS Bull. 2012, 37 (06), 581−589. 12886

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

(64) Lendlein, A.; Kelch, S. Shape-Memory Polymers. Angew. Chem., Int. Ed. 2002, 41 (12), 2034−2057. (65) Liu, C.; Qin, H.; Mather, P. T. Review of Progress in ShapeMemory Polymers. J. Mater. Chem. 2007, 17 (16), 1543−1558. (66) Leng, J.; Lan, X.; Liu, Y.; Du, S. Shape-Memory Polymers and Their Composites: Stimulus Methods and Applications. Prog. Mater. Sci. 2011, 56 (7), 1077−1135. (67) Mendez, J.; Annamalai, P. K.; Eichhorn, S. J.; Rusli, R.; Rowan, S. J.; Foster, E. J.; Weder, C. Bioinspired Mechanically Adaptive Polymer Nanocomposites with Water-Activated Shape-Memory Effect. Macromolecules 2011, 44 (17), 6827−6835. (68) Zhu, Y.; Hu, J.; Luo, H.; Young, R. J.; Deng, L.; Zhang, S.; Fan, Y.; Ye, G. Rapidly Switchable Water-Sensitive Shape-Memory Cellulose/ Elastomer Nano-Composites. Soft Matter 2012, 8 (8), 2509−2517. (69) Wu, T.; Frydrych, M.; O’Kelly, K.; Chen, B. Poly(Glycerol Sebacate Urethane)−Cellulose Nanocomposites with Water-Active Shape-Memory Effects. Biomacromolecules 2014, 15 (7), 2663−2671. (70) Guan, Z. Supramolecular Design in Biopolymers and Biomimetic Polymers for Advanced Mechanical Properties. Polym. Int. 2007, 56 (4), 467−473. (71) Oroudjev, E.; Soares, J.; Arcidiacono, S.; Thompson, J. B.; Fossey, S. A.; Hansma, H. G. Segmented Nanofibers of Spider Dragline Silk: Atomic Force Microscopy and Single-Molecule Force Spectroscopy. Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 6460−6465. (72) Li, X.; Chang, W.-C.; Chao, Y. J.; Wang, R.; Chang, M. Nanoscale Structural and Mechanical Characterization of a Natural Nanocomposite Material: The Shell of Red Abalone. Nano Lett. 2004, 4 (4), 613−617. (73) Marszalek, P. E.; Lu, H.; Li, H.; Carrion-Vazquez, M.; Oberhauser, A. F.; Schulten, K.; Fernandez, J. M. Mechanical Unfolding Intermediates in Titin Modules. Nature 1999, 402 (6757), 100−103. (74) Guzmán, D. L.; Randall, A.; Baldi, P.; Guan, Z. Computational and Single-Molecule Force Studies of a Macro Domain Protein Reveal a Key Molecular Determinant for Mechanical Stability. Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (5), 1989−1994. (75) Thompson, J. B.; Kindt, J. H.; Drake, B.; Hansma, H. G.; Morse, D. E.; Hansma, P. K. Bone Indentation Recovery Time Correlates with Bond Reforming Time. Nature 2001, 414 (6865), 773−776. (76) Rief, M.; Gautel, M.; Oesterhelt, F.; Fernandez, J. M.; Gaub, H. E. Reversible Unfolding of Individual Titin Immunoglobulin Domains by AFM. Science 1997, 276 (5315), 1109−1112. (77) Li, H.; Oberhauser, A. F.; Fowler, S. B.; Clarke, J.; Fernandez, J. M. Atomic Force Microscopy Reveals the Mechanical Design of a Modular Protein. Proc. Natl. Acad. Sci. U. S. A. 2000, 97 (12), 6527−6531. (78) Becker, N.; Oroudjev, E.; Mutz, S.; Cleveland, J. P.; Hansma, P. K.; Hayashi, C. Y.; Makarov, D. E.; Hansma, H. G. Molecular Nanosprings in Spider Capture-Silk Threads. Nat. Mater. 2003, 2 (4), 278−283. (79) Smith, B. L.; Schaffer, T. E.; Viani, M.; Thompson, J. B.; Frederick, N. A.; Kindt, J.; Belcher, A.; Stucky, G. D.; Morse, D. E.; Hansma, P. K. Molecular Mechanistic Origin of the Toughness of Natural Adhesives, Fibres and Composites. Nature 1999, 399 (6738), 761−763. (80) Salib, I. G.; Kolmakov, G. V.; Bucior, B. J.; Peleg, O.; Kröger, M.; Savin, T.; Vogel, V.; Matyjaszewski, K.; Balazs, A. C. Using Mesoscopic Models to Design Strong and Tough Biomimetic Polymer Networks. Langmuir 2011, 27 (22), 13796−13805. (81) Creton, C.; Ciccotti, M. Fracture and Adhesion of Soft Materials: A Review. Rep. Prog. Phys. 2016, 79 (4), 046601. (82) Gong, J. P. Why Are Double Network Hydrogels So Tough? Soft Matter 2010, 6 (12), 2583−2590. (83) Ducrot, E.; Chen, Y.; Bulters, M.; Sijbesma, R. P.; Creton, C. Toughening Elastomers with Sacrificial Bonds and Watching Them Break. Science 2014, 344 (6180), 186−189. (84) Chen, Q.; Chen, H.; Zhu, L.; Zheng, J. Engineering of Tough Double Network Hydrogels. Macromol. Chem. Phys. 2016, 217 (9), 1022−1036. (85) Guan, Z.; Roland, J. T.; Bai, J. Z.; Ma, S. X.; McIntire, T. M.; Nguyen, M. Modular Domain Structure: A Biomimetic Strategy for

Advanced Polymeric Materials. J. Am. Chem. Soc. 2004, 126 (7), 2058− 2065. (86) Roland, J. T.; Guan, Z. Synthesis and Single-Molecule Studies of a Well-Defined Biomimetic Modular Multidomain Polymer Using a Peptidomimetic B-Sheet Module. J. Am. Chem. Soc. 2004, 126 (44), 14328−14329. (87) Kushner, A. M.; Gabuchian, V.; Johnson, E. G.; Guan, Z. Biomimetic Design of Reversibly Unfolding Cross-Linker to Enhance Mechanical Properties of 3D Network Polymers. J. Am. Chem. Soc. 2007, 129 (46), 14110−14111. (88) Shi, Z.-M.; Huang, J.; Ma, Z.; Zhao, X.; Guan, Z.; Li, Z.-T. Foldamers as Cross-Links for Tuning the Dynamic Mechanical Property of Methacrylate Copolymers. Macromolecules 2010, 43 (14), 6185− 6192. (89) Yuan, J.; Zhang, H.; Hong, G.; Chen, Y.; Chen, G.; Xu, Y.; Weng, W. Using Metal-Ligand Interactions to Access Biomimetic Supramolecular Polymers with Adaptive and Superb Mechanical Properties. J. Mater. Chem. B 2013, 1 (37), 4809−4818. (90) Fang, X.; Zhang, H.; Chen, Y.; Lin, Y.; Xu, Y.; Weng, W. Biomimetic Modular Polymer with Tough and Stress Sensing Properties. Macromolecules 2013, 46 (16), 6566−6574. (91) Burnworth, M.; Tang, L.; Kumpfer, J. R.; Duncan, A. J.; Beyer, F. L.; Fiore, G. L.; Rowan, S. J.; Weder, C. Optically Healable Supramolecular Polymers. Nature 2011, 472 (7343), 334−337. (92) Kushner, A. M.; Vossler, J. D.; Williams, G. A.; Guan, Z. A Biomimetic Modular Polymer with Tough and Adaptive Properties. J. Am. Chem. Soc. 2009, 131 (25), 8766−8768. (93) Davis, D. A.; Hamilton, A.; Yang, J.; Cremar, L. D.; Van Gough, D.; Potisek, S. L.; Ong, M. T.; Braun, P. V.; Martinez, T. J.; White, S. R.; et al. Force-Induced Activation of Covalent Bonds in Mechanoresponsive Polymeric Materials. Nature 2009, 459 (7243), 68−72. (94) Zhang, H.; Chen, Y.; Lin, Y.; Fang, X.; Xu, Y.; Ruan, Y.; Weng, W. Spiropyran as a Mechanochromic Probe in Dual Cross-Linked Elastomers. Macromolecules 2014, 47 (19), 6783−6790. (95) Schuetz, J.-H.; Wentao, P.; Vana, P. Titin-Mimicking Polycyclic Polymers with Shape Regeneration and Healing Properties. Polym. Chem. 2015, 6 (10), 1714−1726. (96) Schuetz, J.-H.; Sandbrink, L.; Vana, P. Insights into the RingExpansion Polymerization of Thiiranes with 2,4-Thiazolidinedione. Macromol. Chem. Phys. 2013, 214 (13), 1484−1495. (97) van Beek, J. D.; Hess, S.; Vollrath, F.; Meier, B. H. The Molecular Structure of Spider Dragline Silk: Folding and Orientation of the Protein Backbone. Proc. Natl. Acad. Sci. U. S. A. 2002, 99 (16), 10266−10271. (98) Swanson, B. O.; Blackledge, T. A.; Beltrán, J.; Hayashi, C. Y. Variation in the Material Properties of Spider Dragline Silk across Species. Appl. Phys. A: Mater. Sci. Process. 2006, 82 (2), 213−218. (99) Calvert, P. Materials Science: Silk and Sequence. Nature 1998, 393 (6683), 309−311. (100) Xu, M.; Lewis, R. V. Structure of a Protein Superfiber: Spider Dragline Silk. Proc. Natl. Acad. Sci. U. S. A. 1990, 87 (18), 7120−7124. (101) van Hest, J. C. M.; Tirrell, D. A. Protein-Based Materials, toward a New Level of Structural Control. Chem. Commun. 2001, 19, 1897− 1904. (102) Hendrich, M.; Lewerdomski, L.; Vana, P. Biomimetic Triblock and Multiblock Copolymers Containing L-Phenylalanine Moieties Showing Healing and Enhanced Mechanical Properties. J. Polym. Sci., Part A: Polym. Chem. 2015, 53 (24), 2809−2819. (103) Rathore, O.; Sogah, D. Y. Nanostructure Formation through BSheet Self-Assembly in Silk-Based Materials. Macromolecules 2001, 34 (5), 1477−1486. (104) Huang, H.; Hu, J.; Zhu, Y. Shape-Memory Biopolymers Based on B-Sheet Structures of Polyalanine Segments Inspired by Spider Silks. Macromol. Biosci. 2013, 13 (2), 161−166. (105) Ashton, N. N.; Stewart, R. J. Self-Recovering Caddisfly Silk: Energy Dissipating, Ca2+-Dependent, Double Dynamic Network Fibers. Soft Matter 2015, 11 (9), 1667−1676. (106) Ashton, N. N.; Roe, D. R.; Weiss, R. B.; Cheatham, T. E.; Stewart, R. J. Self-Tensioning Aquatic Caddisfly Silk: Ca2+-Dependent 12887

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Structure, Strength, and Load Cycle Hysteresis. Biomacromolecules 2013, 14 (10), 3668−3681. (107) Lane, D. D.; Kaur, S.; Weerasakare, G. M.; Stewart, R. J. Toughened Hydrogels Inspired by Aquatic Caddisworm Silk. Soft Matter 2015, 11 (35), 6981−6990. (108) Reinecke, A.; Bertinetti, L.; Fratzl, P.; Harrington, M. J. Cooperative Behavior of a Sacrificial Bond Network and Elastic Framework in Providing Self-Healing Capacity in Mussel Byssal Threads. J. Struct. Biol. 2016, 196 (3), 329−339. (109) Harrington, M. J.; Gupta, H. S.; Fratzl, P.; Waite, J. H. Collagen Insulated from Tensile Damage by Domains That Unfold Reversibly: In Situ X-Ray Investigation of Mechanical Yield and Damage Repair in the Mussel Byssus. J. Struct. Biol. 2009, 167 (1), 47−54. (110) Deming, T. J. Mussel Byssus and Biomolecular Materials. Curr. Opin. Chem. Biol. 1999, 3 (1), 100−105. (111) Schmitt, C. N. Z.; Politi, Y.; Reinecke, A.; Harrington, M. J. Role of Sacrificial Protein−Metal Bond Exchange in Mussel Byssal Thread Self-Healing. Biomacromolecules 2015, 16 (9), 2852−2861. (112) Ryou, M.-H.; Kim, J.; Lee, I.; Kim, S.; Jeong, Y. K.; Hong, S.; Ryu, J. H.; Kim, T.-S.; Park, J.-K.; Lee, H.; et al. Mussel-Inspired Adhesive Binders for High-Performance Silicon Nanoparticle Anodes in LithiumIon Batteries. Adv. Mater. 2013, 25 (11), 1571−1576. (113) Skelton, S.; Bostwick, M.; O’Connor, K.; Konst, S.; Casey, S.; Lee, B. P. Biomimetic Adhesive Containing Nanocomposite Hydrogel with Enhanced Materials Properties. Soft Matter 2013, 9 (14), 3825− 3833. (114) Liu, Y.; Meng, H.; Konst, S.; Sarmiento, R.; Rajachar, R.; Lee, B. P. Injectable Dopamine-Modified Poly(Ethylene Glycol) Nanocomposite Hydrogel with Enhanced Adhesive Property and Bioactivity. ACS Appl. Mater. Interfaces 2014, 6 (19), 16982−16992. (115) Ding, X.; Vegesna, G. K.; Meng, H.; Winter, A.; Lee, B. P. NitroGroup Functionalization of Dopamine and Its Contribution to the Viscoelastic Properties of Catechol-Containing Nanocomposite Hydrogels. Macromol. Chem. Phys. 2015, 216 (10), 1109−1119. (116) Liu, Y.; Lee, B. P. Recovery Property of Double-Network Hydrogel Containing a Mussel-Inspired Adhesive Moiety and NanoSilicate. J. Mater. Chem. B 2016, 4 (40), 6534−6540. (117) Zeng, H.; Hwang, D. S.; Israelachvili, J. N.; Waite, J. H. Strong Reversible Fe3+-Mediated Bridging between Dopa-Containing Protein Films in Water. Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (29), 12850− 12853. (118) Lee, H.; Scherer, N. F.; Messersmith, P. B. Single-Molecule Mechanics of Mussel Adhesion. Proc. Natl. Acad. Sci. U. S. A. 2006, 103 (35), 12999−13003. (119) Nabavi, S. S.; Harrington, M. J.; Fratzl, P.; Hartmann, M. A. Influence of Sacrificial Bonds on the Mechanical Behaviour of Polymer Chains. Bioinspired, Biomimetic Nanobiomater. 2014, 3 (3), 139−145. (120) Chung, J.; Kushner, A. M.; Weisman, A. C.; Guan, Z. Direct Correlation of Single-Molecule Properties with Bulk Mechanical Performance for the Biomimetic Design of Polymers. Nat. Mater. 2014, 13 (11), 1055−1062. (121) Zhang, X.; Tang, Z.; Guo, B.; Zhang, L. Enabling Design of Advanced Elastomer with Bioinspired Metal−Oxygen Coordination. ACS Appl. Mater. Interfaces 2016, 8 (47), 32520−32527. (122) Niu, D.; Jiang, W.; Liu, H.; Zhao, T.; Lei, B.; Li, Y.; Yin, L.; Shi, Y.; Chen, B.; Lu, B. Reversible Bending Behaviors of Photomechanical Soft Actuators Based on Graphene Nanocomposites. Sci. Rep. 2016, 6, 27366. (123) Huang, J.; Zhang, L.; Tang, Z.; Wu, S.; Ning, N.; Sun, H.; Guo, B. Bioinspired Design of a Robust Elastomer with Adaptive Recovery Via Triazolinedione Click Chemistry. Macromol. Rapid Commun. 2017, 38, 1600678. (124) Tang, Z.; Huang, J.; Guo, B.; Zhang, L.; Liu, F. Bioinspired Engineering of Sacrificial Metal−Ligand Bonds into Elastomers with Supramechanical Performance and Adaptive Recovery. Macromolecules 2016, 49 (5), 1781−1789. (125) Qin, G.; Hu, X.; Cebe, P.; Kaplan, D. L. Mechanism of Resilin Elasticity. Nat. Commun. 2012, 3, 1003.

(126) Weis-fogh, T. A Rubber-Like Protein in Insect Cuticle. J. Exp. Biol. 1960, 37 (4), 889−907. (127) Elvin, C. M.; Carr, A. G.; Huson, M. G.; Maxwell, J. M.; Pearson, R. D.; Vuocolo, T.; Liyou, N. E.; Wong, D. C. C.; Merritt, D. J.; Dixon, N. E. Synthesis and Properties of Crosslinked Recombinant Pro-Resilin. Nature 2005, 437 (7051), 999−1002. (128) Charati, M. B.; Ifkovits, J. L.; Burdick, J. A.; Linhardt, J. G.; Kiick, K. L. Hydrophilic Elastomeric Biomaterials Based on Resilin-Like Polypeptides. Soft Matter 2009, 5 (18), 3412−3416. (129) Li, L.; Teller, S.; Clifton, R. J.; Jia, X.; Kiick, K. L. Tunable Mechanical Stability and Deformation Response of a Resilin-Based Elastomer. Biomacromolecules 2011, 12 (6), 2302−2310. (130) Wang, Z.; Yuan, L.; Jiang, F.; Zhang, Y.; Wang, Z.; Tang, C. Bioinspired High Resilient Elastomers to Mimic Resilin. ACS Macro Lett. 2016, 5 (2), 220−223. (131) Elkins, C. L.; Park, T.; McKee, M. G.; Long, T. E. Synthesis and Characterization of Poly(2-Ethylhexyl Methacrylate) Copolymers Containing Pendant, Self-Complementary Multiple-Hydrogen-Bonding Sites. J. Polym. Sci., Part A: Polym. Chem. 2005, 43 (19), 4618−4631. (132) Kokil, A.; Saito, T.; Depolo, W.; Elkins, C. L.; Wilkes, G. L.; Long, T. E. Introduction of Multiple Hydrogen Bonding for Enhanced Mechanical Performance of Polymer-Carbon Nanotube Composites. J. Macromol. Sci., Part A: Pure Appl.Chem. 2011, 48 (12), 1016−1021. (133) Luo, M.-C.; Zeng, J.; Xie, Z.-T.; Wei, L.-Y.; Huang, G.; Wu, J. Impact of Hydrogen Bonds Dynamics on Mechanical Behavior of Supramolecular Elastomer. Polymer 2016, 105, 221−226. (134) Luo, M.-C.; Zeng, J.; Fu, X.; Huang, G.; Wu, J. Toughening Diene Elastomers by Strong Hydrogen Bond Interactions. Polymer 2016, 106, 21−28. (135) Hosono, N.; Pitet, L. M.; Palmans, A. R. A.; Meijer, E. W. The Effect of Pendant Benzene-1,3,5-Tricarboxamides in the Middle Block of Aba Triblock Copolymers: Synthesis and Mechanical Properties. Polym. Chem. 2014, 5 (4), 1463−1470. (136) Hayashi, M.; Noro, A.; Matsushita, Y. Highly Extensible Supramolecular Elastomers with Large Stress Generation Capability Originating from Multiple Hydrogen Bonds on the Long Soft Network Strands. Macromol. Rapid Commun. 2016, 37 (8), 678−684. (137) Gold, B. J.; Hövelmann, C. H.; Weiss, C.; Radulescu, A.; Allgaier, J.; Pyckhout-Hintzen, W.; Wischnewski, A.; Richter, D. Sacrificial Bonds Enhance Toughness of Dual Polybutadiene Networks. Polymer 2016, 87, 123−128. (138) Hayashi, M.; Matsushima, S.; Noro, A.; Matsushita, Y. Mechanical Property Enhancement of Aba Block Copolymer-Based Elastomers by Incorporating Transient Cross-Links into Soft Middle Block. Macromolecules 2015, 48 (2), 421−431. (139) Song, G.; Zhang, L.; He, C.; Fang, D.-C.; Whitten, P. G.; Wang, H. Facile Fabrication of Tough Hydrogels Physically Cross-Linked by Strong Cooperative Hydrogen Bonding. Macromolecules 2013, 46 (18), 7423−7435. (140) Myung, D.; Koh, W.; Ko, J.; Hu, Y.; Carrasco, M.; Noolandi, J.; Ta, C. N.; Frank, C. W. Biomimetic Strain Hardening in Interpenetrating Polymer Network Hydrogels. Polymer 2007, 48 (18), 5376−5387. (141) Harrass, K.; Kruger, R.; Möller, M.; Albrecht, K.; Groll, J. Mechanically Strong Hydrogels with Reversible Behaviour under Cyclic Compression with MPa Loading. Soft Matter 2013, 9 (10), 2869−2877. (142) Wang, L.; Shan, G.; Pan, P. Highly Enhanced Toughness of Interpenetrating Network Hydrogel by Incorporating Poly(Ethylene Glycol) in First Network. RSC Adv. 2014, 4 (108), 63513−63519. (143) Zhang, X.; Zhao, C.; Xiang, N.; Li, W. Chain Entanglements and Hydrogen Bonds in Carbopol Microgel Reinforced Hydrogel. Macromol. Chem. Phys. 2016, 217 (19), 2139−2144. (144) Yang, J.; Han, C.-R.; Zhang, X.-M.; Xu, F.; Sun, R.-C. Cellulose Nanocrystals Mechanical Reinforcement in Composite Hydrogels with Multiple Cross-Links: Correlations between Dissipation Properties and Deformation Mechanisms. Macromolecules 2014, 47 (12), 4077−4086. (145) Chen, Y.; Wu, W.; Wang, J.; Jiang, H.; Gao, Y. Synthesis and Properties of Thermoreversible Crosslinking Supramolecular Polymer with Weak Multiple-Hydrogen Bonds and Small Chemical Network 12888

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Sites from Dimer Acid, Diamine and Sulfonyl Isocyanate. J. Polym. Res. 2011, 18 (6), 2325−2333. (146) Henderson, K. J.; Zhou, T. C.; Otim, K. J.; Shull, K. R. Ionically Cross-Linked Triblock Copolymer Hydrogels with High Strength. Macromolecules 2010, 43 (14), 6193−6201. (147) Bakarich, S. E.; Pidcock, G. C.; Balding, P.; Stevens, L.; Calvert, P.; in het Panhuis, M. Recovery from Applied Strain in Interpenetrating Polymer Network Hydrogels with Ionic and Covalent Cross-Links. Soft Matter 2012, 8 (39), 9985−9988. (148) Stevens, L.; Calvert, P.; Wallace, G. G.; Panhuis, M. i. h. IonicCovalent Entanglement Hydrogels from Gellan Gum, Carrageenan and an Epoxy-Amine. Soft Matter 2013, 9 (11), 3009−3012. (149) Wang, D.; Zhang, H.; Cheng, B.; Qian, Z.; Liu, W.; Zhao, N.; Xu, J. Dynamic Cross-Links to Facilitate Recyclable Polybutadiene Elastomer with Excellent Toughness and Stretchability. J. Polym. Sci., Part A: Polym. Chem. 2016, 54 (10), 1357−1366. (150) Liu, J.; Tang, Z.; Huang, J.; Guo, B.; Huang, G. Promoted StrainInduced-Crystallization in Synthetic Cis-1,4-Polyisoprene Via Constructing Sacrificial Bonds. Polymer 2016, 97, 580−588. (151) Rose, S.; Dizeux, A.; Narita, T.; Hourdet, D.; Marcellan, A. Time Dependence of Dissipative and Recovery Processes in Nanohybrid Hydrogels. Macromolecules 2013, 46 (10), 4095−4104. (152) Senses, E.; Akcora, P. An Interface-Driven Stiffening Mechanism in Polymer Nanocomposites. Macromolecules 2013, 46 (5), 1868−1874. (153) Hu, J.; Zhu, Y.; Huang, H.; Lu, J. Recent Advances in Shape− Memory Polymers: Structure, Mechanism, Functionality, Modeling and Applications. Prog. Polym. Sci. 2012, 37 (12), 1720−1763. (154) Meng, H.; Li, G. A Review of Stimuli-Responsive Shape Memory Polymer Composites. Polymer 2013, 54 (9), 2199−2221. (155) Yan, X.; Wang, F.; Zheng, B.; Huang, F. Stimuli-Responsive Supramolecular Polymeric Materials. Chem. Soc. Rev. 2012, 41 (18), 6042−6065. (156) Ware, T.; Hearon, K.; Lonnecker, A.; Wooley, K. L.; Maitland, D. J.; Voit, W. Triple-Shape Memory Polymers Based on SelfComplementary Hydrogen Bonding. Macromolecules 2012, 45 (2), 1062−1069. (157) Guo, M.; Pitet, L. M.; Wyss, H. M.; Vos, M.; Dankers, P. Y. W.; Meijer, E. W. Tough Stimuli-Responsive Supramolecular Hydrogels with Hydrogen-Bonding Network Junctions. J. Am. Chem. Soc. 2014, 136 (19), 6969−6977. (158) Chang, R.; Shan, G.; Bao, Y.; Pan, P. Enhancement of Crystallizability and Control of Mechanical and Shape-Memory Properties for Amorphous Enantiopure Supramolecular Copolymers Via Stereocomplexation. Macromolecules 2015, 48 (21), 7872−7881. (159) Chen, H.; Li, Y.; Tao, G.; Wang, L.; Zhou, S. Thermo- and Water-Induced Shape Memory Poly(Vinyl Alcohol) Supramolecular Networks Crosslinked by Self-Complementary Quadruple Hydrogen Bonding. Polym. Chem. 2016, 7 (43), 6637−6644. (160) Li, J.; Viveros, J. A.; Wrue, M. H.; Anthamatten, M. ShapeMemory Effects in Polymer Networks Containing Reversibly Associating Side-Groups. Adv. Mater. 2007, 19 (19), 2851−2855. (161) Li, J.; Lewis, C. L.; Chen, D. L.; Anthamatten, M. Dynamic Mechanical Behavior of Photo-Cross-Linked Shape-Memory Elastomers. Macromolecules 2011, 44 (13), 5336−5343. (162) Xie, F.; Huang, C.; Wang, F.; Huang, L.; Weiss, R. A.; Leng, J.; Liu, Y. Carboxyl-Terminated Polybutadiene−Poly(Styrene-co-4-Vinylpyridine) Supramolecular Thermoplastic Elastomers and Their Shape Memory Behavior. Macromolecules 2016, 49 (19), 7322−7330. (163) Chen, S.; Yuan, H.; Chen, S.; Yang, H.; Ge, Z.; Zhuo, H.; Liu, J. Development of Supramolecular Liquid-Crystalline Polyurethane Complexes Exhibiting Triple-Shape Functionality Using a One-Step Programming Process. J. Mater. Chem. A 2014, 2 (26), 10169−10181. (164) Chen, H.; Liu, Y.; Gong, T.; Wang, L.; Zhao, K.; Zhou, S. Use of Intermolecular Hydrogen Bonding to Synthesize Triple-Shape Memory Supermolecular Composites. RSC Adv. 2013, 3 (19), 7048−7056. (165) Chen, S.; Hu, J.; Zhuo, H.; Yuen, C.; Chan, L. Study on the Thermal-Induced Shape Memory Effect of Pyridine Containing Supramolecular Polyurethane. Polymer 2010, 51 (1), 240−248.

(166) Chen, S.; Hu, J.; Yuen, C.-w.; Chan, L. Supramolecular Polyurethane Networks Containing Pyridine Moieties for Shape Memory Materials. Mater. Lett. 2009, 63 (17), 1462−1464. (167) Chen, Y.-N.; Peng, L.; Liu, T.; Wang, Y.; Shi, S.; Wang, H. Poly(Vinyl Alcohol)−Tannic Acid Hydrogels with Excellent Mechanical Properties and Shape Memory Behaviors. ACS Appl. Mater. Interfaces 2016, 8 (40), 27199−27206. (168) Kumpfer, J. R.; Rowan, S. J. Thermo-, Photo-, and ChemoResponsive Shape-Memory Properties from Photo-Cross-Linked Metallo-Supramolecular Polymers. J. Am. Chem. Soc. 2011, 133 (32), 12866−12874. (169) Wang, Z.; Fan, W.; Tong, R.; Lu, X.; Xia, H. Thermal-Healable and Shape Memory Metallosupramolecular Poly(N-Butyl Acrylate-coMethyl Methacrylate) Materials. RSC Adv. 2014, 4 (49), 25486−25493. (170) Weiss, R. A.; Izzo, E.; Mandelbaum, S. New Design of Shape Memory Polymers: Mixtures of an Elastomeric Ionomer and Low Molar Mass Fatty Acids and Their Salts. Macromolecules 2008, 41 (9), 2978− 2980. (171) Dong, J.; Weiss, R. A. Effect of Crosslinking on Shape-Memory Behavior of Zinc Stearate/Ionomer Compounds. Macromol. Chem. Phys. 2013, 214 (11), 1238−1246. (172) Hao, J.; Weiss, R. A. Mechanically Tough, Thermally Activated Shape Memory Hydrogels. ACS Macro Lett. 2013, 2 (1), 86−89. (173) Han, D.-D.; Zhang, Y.-L.; Liu, Y.; Liu, Y.-Q.; Jiang, H.-B.; Han, B.; Fu, X.-Y.; Ding, H.; Xu, H.-L.; Sun, H.-B. Bioinspired Graphene Actuators Prepared by Unilateral UV Irradiation of Graphene Oxide Papers. Adv. Funct. Mater. 2015, 25 (28), 4548−4557. (174) Ö lander, A. The crystal structure of AuCd. Z. Kristallogr. - Cryst. Mater. 1932, 83 (1), 145−148. (175) Mohd Jani, J.; Leary, M.; Subic, A.; Gibson, M. A. A Review of Shape Memory Alloy Research, Applications and Opportunities. Mater. Des. 2014, 56, 1078−1113. (176) Chang, L. C.; Read, T. A. Plastic Deformation and Diffusionless Phase Changes in Metals: the Gold-Cadmium Beta-Phase. JOM 1951, 3 (1), 47−52. (177) Studart, A. R.; Erb, R. M. Bioinspired Materials That Self-Shape through Programmed Microstructures. Soft Matter 2014, 10 (9), 1284− 1294. (178) Ahn, S.-k.; Kasi, R. M.; Kim, S.-C.; Sharma, N.; Zhou, Y. StimuliResponsive Polymer Gels. Soft Matter 2008, 4 (6), 1151−1157. (179) Geryak, R.; Tsukruk, V. V. Reconfigurable and Actuating Structures from Soft Materials. Soft Matter 2014, 10 (9), 1246−1263. (180) Ionov, L. Actively-Moving Materials Based on StimuliResponsive Polymers. J. Mater. Chem. 2010, 20 (17), 3382−3390. (181) Cheng, L.-J.; Chang, H.-C. Switchable pH Actuators and 3D Integrated Salt Bridges as New Strategies for Reconfigurable Microfluidic Free-Flow Electrophoretic Separation. Lab Chip 2014, 14 (5), 979−987. (182) Zhou, J.; Sheiko, S. S. Reversible Shape-Shifting in Polymeric Materials. J. Polym. Sci., Part B: Polym. Phys. 2016, 54 (14), 1365−1380. (183) Kong, L.; Chen, W. Carbon Nanotube and Graphene-Based Bioinspired Electrochemical Actuators. Adv. Mater. 2014, 26 (7), 1025− 1043. (184) Kosidlo, U.; Omastová, M.; Micusík, M.; Ć irić-Marjanović, G.; Randriamahazaka, H.; Wallmersperger, T.; Aabloo, A.; Kolaric, I.; Bauernhansl, T. Nanocarbon Based Ionic Actuatorsa Review. Smart Mater. Struct. 2013, 22 (10), 104022. (185) Li, S.; Wang, K. W. Plant-Inspired Adaptive Structures and Materials for Morphing and Actuation: A Review. Bioinspiration Biomimetics 2017, 12 (1), 011001. (186) Randall, C. L.; Gultepe, E.; Gracias, D. H. Self-Folding Devices and Materials for Biomedical Applications. Trends Biotechnol. 2012, 30 (3), 138−146. (187) Chen, D.; Yoon, J.; Chandra, D.; Crosby, A. J.; Hayward, R. C. Stimuli-Responsive Buckling Mechanics of Polymer Films. J. Polym. Sci., Part B: Polym. Phys. 2014, 52 (22), 1441−1461. (188) Ionov, L. Soft Microorigami: Self-Folding Polymer Films. Soft Matter 2011, 7 (15), 6786−6791. 12889

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

(189) Ionov, L. Polymer Origami: Programming the Folding with Shape. e-Polym. 2014, 14 (2), 109−114. (190) Ionov, L. Biomimetic 3D Self-Assembling Biomicroconstructs by Spontaneous Deformation of Thin Polymer Films. J. Mater. Chem. 2012, 22 (37), 19366−19375. (191) Chen, Z.; Huang, G.; Trase, I.; Han, X.; Mei, Y. Mechanical SelfAssembly of a Strain-Engineered Flexible Layer: Wrinkling, Rolling, and Twisting. Phys. Rev. Appl. 2016, 5 (1), 017001. (192) Ionov, L. Polymeric Actuators. Langmuir 2015, 31 (18), 5015− 5024. (193) Stoychev, G. V.; Ionov, L. Actuating Fibers: Design and Applications. ACS Appl. Mater. Interfaces 2016, 8 (37), 24281−24294. (194) Fan, X.; Chung, J. Y.; Lim, Y. X.; Li, Z.; Loh, X. J. Review of Adaptive Programmable Materials and Their Bioapplications. ACS Appl. Mater. Interfaces 2016, 8 (49), 33351−33370. (195) Ionov, L. 3D Microfabrication Using Stimuli-Responsive SelfFolding Polymer Films. Polym. Rev. (Philadelphia, PA, U. S.) 2013, 53 (1), 92−107. (196) Burgert, I.; Fratzl, P. Actuation Systems in Plants as Prototypes for Bioinspired Devices. Philos. Trans. R. Soc., A 2009, 367 (1893), 1541−1557. (197) Fratzl, P.; Barth, F. G. Biomaterial Systems for Mechanosensing and Actuation. Nature 2009, 462 (7272), 442−448. (198) Kempaiah, R.; Nie, Z. From Nature to Synthetic Systems: Shape Transformation in Soft Materials. J. Mater. Chem. B 2014, 2 (17), 2357− 2368. (199) Gracias, D. H. Stimuli Responsive Self-Folding Using Thin Polymer Films. Curr. Opin. Chem. Eng. 2013, 2 (1), 112−119. (200) Hilber, W. Stimulus-Active Polymer Actuators for NextGeneration Microfluidic Devices. Appl. Phys. A: Mater. Sci. Process. 2016, 122 (8), 751. (201) Wehner, M.; Truby, R. L.; Fitzgerald, D. J.; Mosadegh, B.; Whitesides, G. M.; Lewis, J. A.; Wood, R. J. An Integrated Design and Fabrication Strategy for Entirely Soft, Autonomous Robots. Nature 2016, 536 (7617), 451−455. (202) Fusco, S.; Sakar, M. S.; Kennedy, S.; Peters, C.; Bottani, R.; Starsich, F.; Mao, A.; Sotiriou, G. A.; Pané, S.; Pratsinis, S. E.; et al. An Integrated Microrobotic Platform for on-Demand, Targeted Therapeutic Interventions. Adv. Mater. 2014, 26 (6), 952−957. (203) Baek, K.; Jeong, J. H.; Shkumatov, A.; Bashir, R.; Kong, H. In Situ Self-Folding Assembly of a Multi-Walled Hydrogel Tube for Uniaxial Sustained Molecular Release. Adv. Mater. 2013, 25 (39), 5568−5573. (204) Elango, N.; Faudzi, A. A. M. A Review Article: Investigations on Soft Materials for Soft Robot Manipulations. Int. J. Adv. Manuf. Technol. 2015, 80 (5), 1027−1037. (205) Rus, D.; Tolley, M. T. Design, Fabrication and Control of Soft Robots. Nature 2015, 521 (7553), 467−475. (206) Hines, L.; Petersen, K.; Lum, G. Z.; Sitti, M. Soft Actuators for Small-Scale Robotics. Adv. Mater. 2017, 29, 1603483. (207) Kim, S.; Laschi, C.; Trimmer, B. Soft Robotics: A Bioinspired Evolution in Robotics. Trends Biotechnol. 2013, 31 (5), 287−294. (208) Braam, J. In Touch: Plant Responses to Mechanical Stimuli. New Phytol. 2005, 165 (2), 373−389. (209) Egan, P.; Sinko, R.; LeDuc, P. R.; Keten, S. The Role of Mechanics in Biological and Bio-Inspired Systems. Nat. Commun. 2015, 6, 7418. (210) Lachenbruch, B.; McCulloh, K. A. Traits, Properties, and Performance: How Woody Plants Combine Hydraulic and Mechanical Functions in a Cell, Tissue, or Whole Plant. New Phytol. 2014, 204 (4), 747−764. (211) Fratzl, P.; Elbaum, R.; Burgert, I. Cellulose Fibrils Direct Plant Organ Movements. Faraday Discuss. 2008, 139 (0), 275−282. (212) Rafsanjani, A.; Brulé, V.; Western, T. L.; Pasini, D. HydroResponsive Curling of the Resurrection Plant Selaginella Lepidophylla. Sci. Rep. 2015, 5, 8064. (213) Gerbode, S. J.; Puzey, J. R.; McCormick, A. G.; Mahadevan, L. How the Cucumber Tendril Coils and Overwinds. Science 2012, 337 (6098), 1087−1091.

(214) Aharoni, H.; Abraham, Y.; Elbaum, R.; Sharon, E.; Kupferman, R. Emergence of Spontaneous Twist and Curvature in Non-Euclidean Rods: Application to Erodium Plant Cells. Phys. Rev. Lett. 2012, 108 (23), 238106. (215) Evangelista, D.; Hotton, S.; Dumais, J. The Mechanics of Explosive Dispersal and Self-Burial in the Seeds of the Filaree, Erodium Cicutarium (Geraniaceae). J. Exp. Biol. 2011, 214 (4), 521−529. (216) Abraham, Y.; Tamburu, C.; Klein, E.; Dunlop, J. W. C.; Fratzl, P.; Raviv, U.; Elbaum, R. Tilted Cellulose Arrangement as a Novel Mechanism for Hygroscopic Coiling in the Stork’s Bill Awn. J. R. Soc., Interface 2012, 9 (69), 640−647. (217) Armon, S.; Efrati, E.; Kupferman, R.; Sharon, E. Geometry and Mechanics in the Opening of Chiral Seed Pods. Science 2011, 333 (6050), 1726−1730. (218) Bar-On, B.; Sui, X.; Livanov, K.; Achrai, B.; Kalfon-Cohen, E.; Wiesel, E.; Wagner, H. D. Structural Origins of Morphing in Plant Tissues. Appl. Phys. Lett. 2014, 105 (3), 033703. (219) Dawson, C.; Vincent, J. F. V.; Rocca, A.-M. How Pine Cones Open. Nature 1997, 390 (6661), 668−668. (220) Reyssat, E.; Mahadevan, L. Hygromorphs From Pine Cones to Biomimetic Bilayers. J. R. Soc., Interface 2009, 6 (39), 951−957. (221) Lin, S.; Xie, Y. M.; Li, Q.; Huang, X.; Zhou, S. On the Shape Transformation of Cone Scales. Soft Matter 2016, 12 (48), 9797−9802. (222) Harrington, M. J.; Razghandi, K.; Ditsch, F.; Guiducci, L.; Rueggeberg, M.; Dunlop, J. W. C.; Fratzl, P.; Neinhuis, C.; Burgert, I. Origami-Like Unfolding of Hydro-Actuated Ice Plant Seed Capsules. Nat. Commun. 2011, 2, 337. (223) Meng, Q.; Wang, Q.; Zhao, K.; Wang, P.; Liu, P.; Liu, H.; Jiang, L. Hydroactuated Configuration Alteration of Fibrous Dandelion Pappi: Toward Self-Controllable Transport Behavior. Adv. Funct. Mater. 2016, 26 (41), 7378−7385. (224) Elbaum, R.; Zaltzman, L.; Burgert, I.; Fratzl, P. The Role of Wheat Awns in the Seed Dispersal Unit. Science 2007, 316 (5826), 884− 886. (225) Elbaum, R.; Gorb, S.; Fratzl, P. Structures in the Cell Wall That Enable Hygroscopic Movement of Wheat Awns. J. Struct. Biol. 2008, 164 (1), 101−107. (226) Hodick, D.; Sievers, A. On the Mechanism of Trap Closure of Venus Flytrap (Dionaea Muscipula Ellis). Planta 1989, 179 (1), 32−42. (227) Volkov, A. G.; Pinnock, M.-R.; Lowe, D. C.; Gay, M. R. S.; Markin, V. S. Complete Hunting Cycle of Dionaea Muscipula: Consecutive Steps and Their Electrical Properties. J. Plant Physiol. 2011, 168 (2), 109−120. (228) Volkov, A. G.; Adesina, T.; Markin, V. S.; Jovanov, E. Kinetics and Mechanism of Dionaea Muscipula Trap Closing. Plant Physiol. 2007, 146 (2), 694−702. (229) Morimoto, T.; Ashida, F. Temperature-Responsive Bending of a Bilayer Gel. Int. J. Solids Struct. 2015, 56−57, 20−28. (230) Wang, M.; Tian, X.; Ras, R. H. A.; Ikkala, O. Sensitive HumidityDriven Reversible and Bidirectional Bending of Nanocellulose Thin Films as Bio-Inspired Actuation. Adv. Mater. Interfaces 2015, 2 (7), 1500080. (231) Zolfagharian, A.; Kouzani, A. Z.; Khoo, S. Y.; Moghadam, A. A. A.; Gibson, I.; Kaynak, A. Evolution of 3D Printed Soft Actuators. Sens. Actuators, A 2016, 250, 258−272. (232) Liu, Y.; Genzer, J.; Dickey, M. D. “2D or Not 2D”: ShapeProgramming Polymer Sheets. Prog. Polym. Sci. 2016, 52, 79−106. (233) Fan, X.; Chung, J. Y.; Lim, Y. X.; Li, Z.; Loh, X. J. Review of Adaptive Programmable Materials and Their Bioapplications. ACS Appl. Mater. Interfaces 2016, 8 (49), 33351−33370. (234) Timoshenko, S. Analysis of Bi-Metal Thermostats. J. Opt. Soc. Am. 1925, 11 (3), 233−255. (235) Le Duigou, A.; Castro, M. Evaluation of Force Generation Mechanisms in Natural, Passive Hydraulic Actuators. Sci. Rep. 2016, 6, 18105. (236) Stoychev, G.; Zakharchenko, S.; Turcaud, S.; Dunlop, J. W. C.; Ionov, L. Shape-Programmed Folding of Stimuli-Responsive Polymer Bilayers. ACS Nano 2012, 6 (5), 3925−3934. 12890

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

(237) Hu, Z.; Zhang, X.; Li, Y. Synthesis and Application of Modulated Polymer Gels. Science 1995, 269 (5223), 525−527. (238) Lee, S.-W.; Lee, D. Integrated Study of Water Sorption/ Desorption Behavior of Weak Polyelectrolyte Layer-by-Layer Films. Macromolecules 2013, 46 (7), 2793−2799. (239) Secrist, K. E.; Nolte, A. J. Humidity Swelling/Deswelling Hysteresis in a Polyelectrolyte Multilayer Film. Macromolecules 2011, 44 (8), 2859−2865. (240) Lee, S.-W.; Prosser, J. H.; Purohit, P. K.; Lee, D. Bioinspired Hygromorphic Actuator Exhibiting Controlled Locomotion. ACS Macro Lett. 2013, 2 (11), 960−965. (241) Zhang, K.; Geissler, A.; Standhardt, M.; Mehlhase, S.; Gallei, M.; Chen, L.; Marie Thiele, C. Moisture-Responsive Films of Cellulose Stearoyl Esters Showing Reversible Shape Transitions. Sci. Rep. 2015, 5, 11011. (242) Kelby, T. S.; Wang, M.; Huck, W. T. S. Controlled Folding of 2D Au−Polymer Brush Composites into 3D Microstructures. Adv. Funct. Mater. 2011, 21 (4), 652−657. (243) Duan, J.; Liang, X.; Zhu, K.; Guo, J.; Zhang, L. Bilayer Hydrogel Actuators with Tight Interfacial Adhesion Fully Constructed from Natural Polysaccharides. Soft Matter 2017, 13, 345−354. (244) Armon, S.; Aharoni, H.; Moshe, M.; Sharon, E. Shape Selection in Chiral Ribbons: From Seed Pods to Supramolecular Assemblies. Soft Matter 2014, 10 (16), 2733−2740. (245) Erb, R. M.; Libanori, R.; Rothfuchs, N.; Studart, A. R. Composites Reinforced in Three Dimensions by Using Low Magnetic Fields. Science 2012, 335 (6065), 199−204. (246) Erb, R. M.; Segmehl, J.; Charilaou, M.; Loffler, J. F.; Studart, A. R. Non-Linear Alignment Dynamics in Suspensions of Platelets under Rotating Magnetic Fields. Soft Matter 2012, 8 (29), 7604−7609. (247) Erb, R. M.; Sander, J. S.; Grisch, R.; Studart, A. R. Self-Shaping Composites with Programmable Bioinspired Microstructures. Nat. Commun. 2013, 4, 1712. (248) Zhang, L.; Chizhik, S.; Wen, Y.; Naumov, P. Directed Motility of Hygroresponsive Biomimetic Actuators. Adv. Funct. Mater. 2016, 26 (7), 1040−1053. (249) Le Duigou, A.; Castro, M. Moisture-Induced Self-Shaping FlaxReinforced Polypropylene Biocomposite Actuator. Ind. Crops Prod. 2015, 71, 1−6. (250) Deng, J.; Li, J.; Chen, P.; Fang, X.; Sun, X.; Jiang, Y.; Weng, W.; Wang, B.; Peng, H. Tunable Photothermal Actuators Based on a PreProgrammed Aligned Nanostructure. J. Am. Chem. Soc. 2016, 138 (1), 225−230. (251) Koerner, H.; Price, G.; Pearce, N. A.; Alexander, M.; Vaia, R. A. Remotely Actuated Polymer Nanocomposites−Stress-Recovery of Carbon-Nanotube-Filled Thermoplastic Elastomers. Nat. Mater. 2004, 3 (2), 115−120. (252) Chen, L.; Liu, C.; Liu, K.; Meng, C.; Hu, C.; Wang, J.; Fan, S. High-Performance, Low-Voltage, and Easy-Operable Bending Actuator Based on Aligned Carbon Nanotube/Polymer Composites. ACS Nano 2011, 5 (3), 1588−1593. (253) Chen, L. Z.; Liu, C. H.; Hu, C. H.; Fan, S. S. Electrothermal Actuation Based on Carbon Nanotube Network in Silicone Elastomer. Appl. Phys. Lett. 2008, 92 (26), 263104. (254) Sellinger, A. T.; Wang, D. H.; Tan, L.-S.; Vaia, R. A. Electrothermal Polymer Nanocomposite Actuators. Adv. Mater. 2010, 22 (31), 3430−3435. (255) Zhang, X.; Yu, Z.; Wang, C.; Zarrouk, D.; Seo, J.-W. T.; Cheng, J. C.; Buchan, A. D.; Takei, K.; Zhao, Y.; Ager, J. W.; et al. Photoactuators and Motors Based on Carbon Nanotubes with Selective Chirality Distributions. Nat. Commun. 2014, 5, 2983. (256) Lin, H.; Gong, J.; Eder, M.; Schuetz, R.; Peng, H.; Dunlop, J. W. C.; Yuan, J. Programmable Actuation of Porous Poly(Ionic Liquid) Membranes by Aligned Carbon Nanotubes. Adv. Mater. Interfaces 2017, 4, 1600768. (257) Zhao, Q.; Dunlop, J. W. C.; Qiu, X.; Huang, F.; Zhang, Z.; Heyda, J.; Dzubiella, J.; Antonietti, M.; Yuan, J. An Instant MultiResponsive Porous Polymer Actuator Driven by Solvent Molecule Sorption. Nat. Commun. 2014, 5, 4293.

(258) Lu, X.; Zhang, Z.; Li, H.; Sun, X.; Peng, H. Conjugated Polymer Composite Artificial Muscle with Solvent-Induced Anisotropic Mechanical Actuation. J. Mater. Chem. A 2014, 2 (41), 17272−17280. (259) Sun, X.; Chen, T.; Yang, Z.; Peng, H. The Alignment of Carbon Nanotubes: An Effective Route to Extend Their Excellent Properties to Macroscopic Scale. Acc. Chem. Res. 2013, 46 (2), 539−549. (260) Tseng, I. H.; Li, J.-J.; Chang, P.-Y. Mimosa Pudica Leaf-Like Rapid Movement and Actuation of Organosoluble Polyimide Blending with Sulfonated Polyaniline. Adv. Mater. Interfaces 2017, 4, 1600901. (261) Sydney Gladman, A.; Matsumoto, E. A.; Nuzzo, R. G.; Mahadevan, L.; Lewis, J. A. Biomimetic 4D Printing. Nat. Mater. 2016, 15 (4), 413−418. (262) Haraguchi, K.; Li, H.-J.; Matsuda, K.; Takehisa, T.; Elliott, E. Mechanism of Forming Organic/Inorganic Network Structures During in-Situ Free-Radical Polymerization in PNIPA−Clay Nanocomposite Hydrogels. Macromolecules 2005, 38 (8), 3482−3490. (263) Haraguchi, K.; Takehisa, T. Nanocomposite Hydrogels: A Unique Organic−Inorganic Network Structure with Extraordinary Mechanical, Optical, and Swelling/De-Swelling Properties. Adv. Mater. 2002, 14 (16), 1120−1124. (264) Compton, B. G.; Lewis, J. A. 3D-Printing of Lightweight Cellular Composites. Adv. Mater. 2014, 26 (34), 5930−5935. (265) Aharoni, H.; Sharon, E.; Kupferman, R. Geometry of Thin Nematic Elastomer Sheets. Phys. Rev. Lett. 2014, 113 (25), 257801. (266) Pette, D.; Staron, R. S. Cellular and Molecular Diversities of Mammalian Skeletal Muscle Fibers. In Reviews of Physiology, Biochemistry and Pharmacology; Springer Berlin Heidelberg: Berlin, 1990; Vol. 116, pp 1−76. (267) Ohm, C.; Brehmer, M.; Zentel, R. Liquid Crystalline Elastomers as Actuators and Sensors. Adv. Mater. 2010, 22 (31), 3366−3387. (268) Ikeda, T.; Mamiya, J.-i.; Yu, Y. Photomechanics of LiquidCrystalline Elastomers and Other Polymers. Angew. Chem., Int. Ed. 2007, 46 (4), 506−528. (269) de Haan, L. T.; Schenning, A. P. H. J.; Broer, D. J. Programmed Morphing of Liquid Crystal Networks. Polymer 2014, 55 (23), 5885− 5896. (270) Yang, H.; Ye, G.; Wang, X.; Keller, P. Micron-Sized Liquid Crystalline Elastomer Actuators. Soft Matter 2011, 7 (3), 815−823. (271) Mamiya, J.-i. Photomechanical Energy Conversion Based on Cross-Linked Liquid-Crystalline Polymers. Polym. J. (Tokyo, Jpn.) 2013, 45 (3), 239−246. (272) Barrett, C. J.; Mamiya, J.-i.; Yager, K. G.; Ikeda, T. PhotoMechanical Effects in Azobenzene-Containing Soft Materials. Soft Matter 2007, 3 (10), 1249−1261. (273) Iamsaard, S.; Aßhoff, S. J.; Matt, B.; Kudernac, T.; Cornelissen, J. J. L. M.; Fletcher, S. P.; Katsonis, N. Conversion of Light into Macroscopic Helical Motion. Nat. Chem. 2014, 6 (3), 229−235. (274) Iamsaard, S.; Villemin, E.; Lancia, F.; Aβhoff, S.-J.; Fletcher, S. P.; Katsonis, N. Preparation of Biomimetic Photoresponsive Polymer Springs. Nat. Protoc. 2016, 11 (10), 1788−1797. (275) Zhang, L.; Naumov, P. Light- and Humidity-Induced Motion of an Acidochromic Film. Angew. Chem., Int. Ed. 2015, 54 (30), 8642− 8647. (276) Ionov, L. Biomimetic Hydrogel-Based Actuating Systems. Adv. Funct. Mater. 2013, 23 (36), 4555−4570. (277) Holstov, A.; Bridgens, B.; Farmer, G. Hygromorphic Materials for Sustainable Responsive Architecture. Constr. Build Mater. 2015, 98, 570−582. (278) Ionov, L. Hydrogel-Based Actuators: Possibilities and Limitations. Mater. Today 2014, 17 (10), 494−503. (279) Guvendiren, M.; Yang, S.; Burdick, J. A. Swelling-Induced Surface Patterns in Hydrogels with Gradient Crosslinking Density. Adv. Funct. Mater. 2009, 19 (19), 3038−3045. (280) Luo, R.; Wu, J.; Dinh, N.-D.; Chen, C.-H. Gradient Porous Elastic Hydrogels with Shape-Memory Property and Anisotropic Responses for Programmable Locomotion. Adv. Funct. Mater. 2015, 25 (47), 7272−7279. (281) Wang, L.; Liu, Y.; Cheng, Y.; Cui, X.; Lian, H.; Liang, Y.; Chen, F.; Wang, H.; Guo, W.; Li, H.; et al. A Bioinspired Swimming and 12891

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892

Chemical Reviews

Review

Walking Hydrogel Driven by Light-Controlled Local Density. Adv. Sci. 2015, 2 (6), 1500084. (282) Lee, H.; Xia, C.; Fang, N. X. First Jump of Microgel; Actuation Speed Enhancement by Elastic Instability. Soft Matter 2010, 6 (18), 4342−4345. (283) Wu, Z. L.; Moshe, M.; Greener, J.; Therien-Aubin, H.; Nie, Z.; Sharon, E.; Kumacheva, E. Three-Dimensional Shape Transformations of Hydrogel Sheets Induced by Small-Scale Modulation of Internal Stresses. Nat. Commun. 2013, 4, 1586. (284) Wang, Z. J.; Zhu, C. N.; Hong, W.; Wu, Z. L.; Zheng, Q. Programmed Planar-to-Helical Shape Transformations of Composite Hydrogels with Bioinspired Layered Fibrous Structures. J. Mater. Chem. B 2016, 4 (44), 7075−7079. (285) Wang, F.; Jeon, J.-H.; Kim, S.-J.; Park, J.-O.; Park, S. An EcoFriendly Ultra-High Performance Ionic Artificial Muscle Based on Poly(2-Acrylamido-2-Methyl-1-Propanesulfonic Acid) and Carboxylated Bacterial Cellulose. J. Mater. Chem. B 2016, 4 (29), 5015−5024. (286) Nawroth, J. C.; Lee, H.; Feinberg, A. W.; Ripplinger, C. M.; McCain, M. L.; Grosberg, A.; Dabiri, J. O.; Parker, K. K. A TissueEngineered Jellyfish with Biomimetic Propulsion. Nat. Biotechnol. 2012, 30 (8), 792−797. (287) Feinberg, A. W.; Feigel, A.; Shevkoplyas, S. S.; Sheehy, S.; Whitesides, G. M.; Parker, K. K. Muscular Thin Films for Building Actuators and Powering Devices. Science 2007, 317 (5843), 1366−1370. (288) Chan, V.; Park, K.; Collens, M. B.; Kong, H.; Saif, T. A.; Bashir, R. Development of Miniaturized Walking Biological Machines. Sci. Rep. 2012, 2, 857.

12892

DOI: 10.1021/acs.chemrev.7b00168 Chem. Rev. 2017, 117, 12851−12892