Perspective pubs.acs.org/Langmuir
The Present and Future of Biologically Inspired Adhesive Interfaces and Materials Carrie E. Brubaker*,†,∥,⊥,▽ and Phillip B. Messersmith*,†,‡,§,∥,⊥,# †
Biomedical Engineering Department, ‡Materials Science and Engineering Department, §Chemical and Biological Engineering Department, and ∥the Chemistry of Life Processes Institute, Northwestern University, Evanston, Illinois 60208, United States ⊥ The Institute for BioNanotechnology in Medicine and #the Robert H. Lurie Comprehensive Cancer Center, Northwestern University, Chicago, Illinois 60611, United States ABSTRACT: The natural world provides many examples of robust, permanent adhesive platforms. Synthetic adhesive interfaces and materials inspired by mussels of genus Mytulis have been extensively applied, and it is expected that characterization and adaptation of several other biological adhesive strategies will follow the Mytilus edulis model. These candidate species will be introduced, along with a discussion of the adhesive behaviors that make them attractive for synthetic adaptation. While significant progress has been made in the development of biologically inspired adhesive interfaces and materials, persistent questions, current challenges, and emergent areas of research will be also be discussed.
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INTRODUCTION Adhesion across multiple length scales is integral to survival in the natural world. Significant efforts have been undertaken both to characterize the broad array of adhesive mechanisms utilized by biological organisms in their natural environments, and to mimic such adhesive performance through synthetic platforms. These activities are carried out with the expectation that biologically inspired adhesives and coatings should find beneficial and lucrative applications in medicine, technology, and industry. Furthermore, simplified synthetic mimics of biological adhesives facilitate better understanding of the systems from which they are derived, by allowing systematic analysis of adhesion parameters. In this Perspective, we will discuss the seminal findings and current status within the area of biologically inspired adhesive interfaces and materials, specifically those that are nonreversible and intended for permanent bulk and/or interfacial adhesion. We will introduce almost one dozen organisms that have inspired synthetic adhesive materials, or are expected to yield such materials in the near future. As such, promising emergent research areas and applications of biologically inspired adhesive interfaces and materials will be addressed throughout our discussion. Common experience tells us that adhesives and water do not mix: bandages fall off during bathing and household glues do not work underwater. Therefore, it is unexpected and intriguing that so many biologically inspired synthetic adhesives and coatings are motivated by organisms inhabiting aquatic environments. Extensive research efforts have permitted sufficient characterization of the adhesive mechanisms utilized by marine mussel species such as Mytilus edulis to engineer mussel-inspired adhesive interfaces, coatings, and sealant materials. While many questions remain to be answered, the © 2012 American Chemical Society
path by which characterization of marine mussel adhesion has led to innovative synthetic adhesives represents a model for development of adhesive materials inspired by organisms such as the sandcastle worm (Phragmatopoma californica), barnacle, caddisfly larvae, and others. This underscores the first thematic section of this Perspective, namely, the central importance of characterizing candidate species. The remaining sections will address novel adhesive platforms, hybrid systems, and potential applications of nonreversible biologically inspired adhesive approaches. In addition to introducing approaches presently under development, current challenges and future directions will be emphasized, including basic research questions that remain to be answered.
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CHARACTERIZING AND MIMICKING NATIVE ADHESIVES Prior to developing engineered, biologically inspired adhesive interfaces and materials, it is necessary to identify an organism of interest and initiate the process of characterizing its adhesive mechanisms. The exploration of Mytilus edulis, its relatives M. californianus and M. galloprovincialis, and other fresh- and saltwater mussels, has progressed over many, many years.1,2 Subsequently, these efforts have yielded a broad array of synthetic mimics and derivatives, to be highlighted here; the approach now represents a reliable model for understanding the native systems and engineering biologically inspired materials, as follows. Attachment and adhesion by the organism are first observed in the native environment. Thereafter, upon isolation Special Issue: Bioinspired Assemblies and Interfaces Received: January 4, 2012 Published: January 5, 2012 2200
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modified amino acid that presents a dihydroxybenzyl, or catechol, moiety. Following secretion of the proteinaceous byssal adhesive precursor solution, DOPA catechol oxidation to quinone occurs at the alkaline pH of seawater, or possibly by redox or enzymatic mechanisms. DOPA is a potent effector of interfacial adhesion, as both the unoxidized and oxidized (quinone) forms of DOPA catechol demonstrate covalent and noncovalent bonding capabilities with a broad range of organic, inorganic, and metallic substrates.17 For example, characterization of DOPA catechol interaction with Ti by single molecule force spectroscopy identified a reversible, noncovalent bond strength of several hundred piconewtons.18 Further, DOPA-quinone covalently couples with primary amines via Michael or Schiff reactions.19 Indeed, general reactivity to nucleophiles such as thiols and imidazoles is surmised, and identification of 5-S-cysteinylDOPA in the mussel byssus supports this hypothesis.20 Promiscuity of substrate adhesion likely represents a valuable performance characteristic of native adhesives, and one that should be emphasized in the design of synthetic engineered catechol-containing materials. In addition to general substrate adhesion, another remarkable characteristic of DOPA and its catechol is structural simplicity: DOPA and DOPA analogues are small and easily incorporated into materials destined for adhesion to a wide variety of substrates. As such, catechol-containing small molecules and polymers have been applied in numerous platforms as adhesive interfaces and materials. For example, surface-anchored, catechol-presenting initiator species have been utilized for surface-initiated polymerization techniques, including atom transfer radical polymerization (ATRP),21 ring-opening metathesis polymerization22 (ROMP), and reversible addition− fragmentation chain transfer (RAFT) polymerization;23 proposed applications of the surface-initiated approach include engineering of surfaces demonstrating excellent protein and cell fouling resistance.24,25 Using the “graft to” technique, fouling resistance of modified surfaces has also been explored with catechol-modified poly(ethylene glycol) (PEG) polymers,26,27 peptoid oligomers,28 and DOPA-containing mfp-1-mimetic peptides.29 Substrate-independent catechol adhesion was exploited in efficient layer-by-layer (LbL) assembly of catechol-modified poly(ethylenimine) and hyaluronic acid polymers on Au, SiOx, and poly(methyl methacrylate) substrates.30 Photopolymerized DOPA-containing block copolymer hydrogels have shown good adhesion to Ti in an aqueous environment,31 and DOPA modification imparts improved mucoadhesive properties to physical gels derived from thermosensitive block copolymers.32 In addition to these mussel-inspired adhesive interfaces generated on “ideal” or homogeneous surfaces, oxidatively cross-linked branched PEGs terminally modified with DOPA-mimetic 3,4-dihydroxyhydrocinnamic acid have shown robust, nontoxic adhesion to human fetal membrane ex vivo33 and to murine adipose tissue in vivo.34 The finding that this catechol-PEG (cPEG) adhesive hydrogel remains intact and adherent to underlying tissue 1 year following implantation34 highlights an important concern regarding the long-term stability of the adhesive materials described in this and subsequent sections. Namely, as novel adhesive interfaces and materials are inspired from mussel and other candidate species, it will be necessary to address both the lifetime of adhesive performance, and the environmental or biological mechanisms of adhesive failure, especially in materials destined for commercial use.
of sufficient quantities of putative adhesive secretions, analytical techniques in chemistry and biochemistry are harnessed to characterize the macromolecular (i.e., protein and/or polysaccharide content) and molecular components of the material (i.e., amino acid sequence, post-translational modifications), as well as addressing the role of trace components such as ionic species and metals. Additional topics to address include pH- or redox-dependent behaviors, and in the case of heterogeneous secretions, the role of intermolecular interactions in adhesive performance. Where possible, a broad range of analytical techniques should be brought to bear on the unique adhesive mechanisms employed by biological organisms. As exemplified in the case of studies on native mussel glue, further characterization by physical techniques such as atomic force microscopy (AFM), surface forces apparatus (SFA), quartz crystal microbalance (QCM), scanning electron microscopy (SEM), rheology, and mass spectrometry provide further insight into the fundamental behavior of secreted biological adhesives. Engineered adhesive interfaces and materials inspired by nature typically evolve in parallel with characterization of the native platforms. As summarized in several excellent recent reviews,3−6 the mussel byssus is composed of a collection of threads terminated by adhesive plaques. It represents the interface with the underlying substrate and is fabricated from macromolecular components represented by several protein families: mussel foot protein (mfp)-1 through -6, and the preCOLs. Early in the development of mussel-inspired adhesive materials, Yamamoto and colleagues utilized N-carboxyanhydride (NCA) solution-phase polymerization and covalent crosslinking of 10-mers to generate mfp-1-mimetic polypeptides.7,8 As mfp amino acid sequences were further elucidated, recombinant mfp protein production was performed in Saccharomyces cerevisiae9 and Escherichia coli.10,11 One challenge of recombinant platforms is faithfully recapitulating the native mfp post-translational modifications, which are known to play a central role in the adhesive behavior of the byssal terminal plaque. For example, mfp-3 and mfp-5 are concentrated at the plaque/substrate interface and contain 20−30 mol % 3,4dihydroxyphenylalanine (DOPA),12,13 implicating this amino acid in the robust interfacial adhesion demonstrated by the plaque. Other post-translational modifications identified in mfp's include phosphoserine, hydroxyarginine, and dihydroxyproline.4 Optimization of recombinant mussel adhesive proteins has been proposed as an affordable method for scaling up production of mussel-mimetic and other protein adhesives.14 Recently, the first example of recombinant mfp production in eukaryotic insect cells was achieved, permitting in situ post-translational modifications.15 Whether through recombinant or fully synthetic platforms, the ability to scale affordably provides a significant challenge in the area of adhesive interfaces and materials. Additionally, the mussel byssus is a complex and heterogeneous macromolecular microenvironment composed of a handful of proteins with unique composition. It will be important to determine the impact, if any, of interprotein reactions, and how these interactions may be reconstituted in a synthetic approach. For example, Waite and colleagues have proposed that thiols present in mfp-6 can reduce oxidized (quinone) DOPA in mfp3 back to the catechol form, improving mfp-3 interfacial adhesion to inorganic substrates.16 DOPA is generated via hydroxylation of tyrosine by the enzyme tyrosine hydroxylase, to yield a post-translationally 2201
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relies upon a hybrid, biomineralized secretion containing calcium carbonate bound within a cross-linked protein matrix.55 Both of these organisms may inspire organic−inorganic composite adhesive materials. Two relevant nonaquatic species have recently been identified as candidates from which biologically inspired adhesive mechanisms may be derived: the Australian frog of genus Notaden and gastropods such as snails and slugs. Whereas Notaden bennetti secretes a yellow-colored, proteinbased tacky adhesive only upon provocation, many gastropods achieve adhesive locomotion on a thin layer of sticky mucus on walls and ceilings, even upside-down. Frog glue is a protein hydrogel that contains hydroxyproline but lacks DOPA.56 The native glue has undergone mechanical testing, as well as in vitro, ex vivo, and in vivo analyses of performance and toxicity.57−60 Looking ahead, once sequences are available, recombinant frog glue protein could offer a route to avoid the cytotoxic effects of trace nonprotein compounds found in native frog glue. Gastropod pedal mucus contains both protein and polysaccharide components, and its intriguing nonlinear rheological properties have been explored.61 Thus the engineering of gastropod-mimetic adhesive substrates permitting locomotion along the interface presents very interesting research questions. As described in this section, a remarkable effort has been invested in the identification, characterization, and mimicry of adhesive-producing organisms, toward the goal of generating novel materials and platforms for adhesion. Nevertheless, there is much fodder for future research efforts. For example, there is present debate about the role of metal ions such as Fe3+ in intra- and intermolecular protein cross-linking in the mussel byssus. Surface forces analysis has confirmed that Fe3+ plays a role in mussel foot cohesion,62 the basis of this mechanical effect being attributed to metal chelation by DOPA catechol and formation of coordination complexes,63,64 or covalent cross-linking.65 Given the fundamentally different mechanical behavior that arises from covalent versus coordination crosslinking,66 more thorough examination of these mechanisms will permit the engineering of Fe3+-containing polymer platforms with interesting adhesive or mechanical properties. As introduced above, it will be worthwhile to further explore the role of amyloid in barnacle adhesion and determine whether this structural model might be incorporated into barnacleinspired adhesive materials. The central importance of posttranslational modifications in some of the systems introduced here presents a challenge for preparing recombinant protein mimics; polymer and polysaccharide engineering should also be emphasized. Lastly, several other species deserve more thorough characterization. As yet there is only a single publication that posits a role for microbial exopolysaccharides as adhesive materials;67 further expansion of these efforts could lead to new opportunities for natural and engineered polysaccharides as adhesives. Indeed, close attention must be paid to research in the basic biological and biochemical sciences, as biologically inspired research efforts may only be performed on a foundation of basic understanding.
Progress achieved in the characterization and mimicry of marine mussel adhesion is just one example of biomimetic efforts underway. Here we introduce other organisms currently under investigation; it is anticipated that the development and evolution of mussel-inspired adhesive interfaces and materials will serve as a model for engineering analogous platforms inspired by these organisms. The sandcastle worm Phragmatopoma californica has also inspired adhesive materials. This polychaete generates its tubelike shelter by gluing together environmental inorganic particulate matter. Pc-1 and Pc-2 are two basic protein components of sandcastle worm cement displaying significant lysine and DOPA content.35 The acidic protein Pc-3 is a family of protein variants containing 60−90 mol % serine, much of which is phosphorylated.36 In the presence of divalent cations Mg2+ and Ca2+, simultaneous secretion of these highly polar proteins is thought to result in complex coacervation followed by pH-dependent hardening into a porous glue.37,38 Synthetic amine-presenting Pc-1 and phosphate- and DOPA-presenting Pc-3 mimics have been prepared; when mixed, these polymers generate a surfaceadherent and water immiscible complex coacervate, which demonstrated in vitro bonding performance over several months between samples of bovine cortical bone.39 Mixing Pc-3 analogue and an amine-presenting modified gelatin permitted thermally triggered coacervation at 36 °C and pH 7.4.40 These sandcastle worm mimetic adhesives have been studied in the repair of rat craniofacial defects.41 Sandcastle worm cement provides a wealth of synthetic adhesive design parameters to explore, including polymer charge density, pHdependent behaviors, divalent cation concentration, and temperature. Complementary DNA (cDNA) sequencing from an adhesive gland library42 and morphological analysis of the sandcastle worm adhesive system43 will provide new insights into engineered coacervate mimics.44 Like the sandcastle worm, the caddisfly larva is another aquatic organism that builds its tube-shaped shelter from environmental particulate matter, using a secreted silk-like adhesive glue. This silk adhesive contains a (SX)n repeat unit in which half of the serines are phosphorylated and a significant portion of their paired amino acids are basic.45 As in mussels and sandcastle worms, it appears that phosphate plays a valuable role in interfacial adhesion and may provide a mechanism for promoting interfacial adhesion of synthetic materials on metallic surfaces. Barnacles attach to marine surfaces by secreting an insoluble multiprotein adhesive complex at the interface of their ventral surface and the underlying substrate. A combination of hydrophobic interactions/aggregation, enzyme-dependent protein cross-linking, and disulfide bonding is likely responsible for the chemical nature of barnacle adhesion and cohesion, whereas no spectroscopic evidence for DOPA has been found.46−48 Nanoscale globular protein domains and amyloid structures have been observed in native barnacle adhesive,49−51 and putative barnacle adhesive proteins Cp19k, Cp20k, Cp52k, and Cp68k have been sequenced: their amino acid content supports the role of hydrophobic interactions and hydrogen bonding in interfacial adhesion.4,52,53 In Balanus improvises, adhesive chemical content and mechanical stiffness are substratedependent,54 providing an intriguing design challenge for barnacle-inspired adhesives. In the future, successful mimics of barnacle adhesion may chart the path toward incorporation of amyloid-mimetic structural components, although their reticent solubility presents a technical challenge. As in barnacle adhesion, it was recently determined that oyster adhesion
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REDUCTIONIST AND HYBRID SYSTEMS Even the most sophisticated of the biologically inspired synthetic materials described above are simple compared to complex natural adhesives. However, sometimes even the most primitive biologically inspired material can provide powerful results, as can previously unimagined combinations of 2202
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under investigation, the potential applications of biologically inspired adhesive materials are constantly expanding. One major area of interest is the use of coatings in biological or medical applications. For example, a suspension of native mfps1, -2, and -3 dissolved in 5% acetic acid (Cell-Tak) is commercially available as an in vitro cell attachment promoter; similarly, Kollodis, Inc. provides commercial recombinant fusion mussel foot proteins. Catechol-presenting small molecules and macromolecules, as well as pDA-mediated surface coatings, may be utilized to promote or prevent cellular adhesion on materials or surfaces relevant to the biomedical device industry. For example, coatings of mfp polypeptide mimics permit stent endothelialization,84 hyaluronic acid and recombinant mfp coacervates promote osteoblast proliferation on Ti,85 and pDA coatings facilitate mammalian cell adhesion on atypical materials such as PTFE.86 For fouling prevention, Au surfaces coated with catechol-presenting zwitterionic polymers show excellent resistance to fibrinogen and lysozyme deposition,87 urinary stents coated with catechol-presenting PEG-based polymers effectively resist E. coli deposition in vivo,88 and DA-modified heparin deposited on polyurethane inhibited blood coagulation and platelet adhesion.89 In medical imaging applications, iron oxide nanoparticles modified via DOPA or DA have been utilized for targeted magnetic resonance imaging (MRI),90,91 and Au nanoparticles coated with DOPA-conjugated heparin have been applied for liverspecific computed tomography (CT) scanning.92 Musselinspired adhesive interfaces have also expanded into biotechnology applications: pDA-mediated coatings have been explored as novel surfaces for protein capillary electrophoresis,93 and catechol-presenting copolymers have been utilized as anchoring substrates for preparation of DNA microarrays.94 It is envisioned that the species addressed in this Perspective will also provide biologically inspired, high-performance adhesive interfaces with important military or industrial applications. Barnacles are notorious marine foulers, whose attachment to boat hulls decreases naval cruising speeds and increases fuel and cleaning costs.95,96 Ironically, the same routes utilized to characterize barnacle adhesion and identify future adhesive materials may permit the design of surface-adherent nonfouling coatings to prevent barnacle attachment. Indeed, the finding that silicones disrupt barnacle adhesive curing97 could point the way toward synthetic, silicone-presenting adhesive coatings for marine fouling resistance. In an application relevant to industrial processing and environmental concerns, bisphosphonate-linked DA surfaces have been tested for removal of uranyl ions from water,98 and other heavy metal removal platforms are sought. The capability of pDA to increase interfacial adhesion has been applied in composite materials; for example, pDA-coated clay has been utilized for reinforcement of epoxy resin.99 Mussel-inspired coatings easily modify polymer membranes: pDA coatings increase hydrophilicity and improve the performance of reverse osmosis membranes,100 and a poly(DOPA) coating permits heparin modification of a common hemodialysis membrane (PVDF) for improved blood compatibility.101 Although this selection of current applications is by no means exhaustive, these highlights are provided to demonstrate the array of potential uses for biologically inspired adhesive interfaces and materials sought from novel candidate organisms.
otherwise disparate adhesive strategies. Again we turn to the marine mussel for representative examples. While the presence of DOPA in the mussel byssus was known relatively early on,68 subsequent elucidation of the primary amino acid sequences of mfp-3 and mfp-5 revealed that a significant percentage of the DOPA amino acids in these two proteins are flanked by basic residues such as lysine.12,13 Given that mfp-3 and mfp-5 localize to the interface between the mussel terminal plaque and the underlying substrate, it was hypothesized that combining DOPA and Lys residues in synthetic polymer platforms would facilitate good interfacial adhesion.69 A dramatically simplified mimic of the catechol and amine rich mfp-3 and mfp5 proteins exists in the form of dopamine (DA) and related small molecule catecholamines. Under basic conditions, DA rapidly polymerizes in a process similar to the biological production of melanin. Polydopamine (pDA) adheres to an astounding array of substrates: a wide range of polymers, metals, inorganics, and even “non-adherent” substrates such as poly(tetrafluoroethylene) (PTFE).70 Promiscuous pDA adhesion has revolutionized surface modification and adhesion at the interface, as pDA serves as a “primer” for further surface modifications. In the last year, pDA has been utilized to functionalize Au surfaces for neural interfaces,71 to conjugate bone morphogenetic protein 2 (BMP2) onto TiO2 nanotubes,72 for endothelial cell growth on pDA-coated electrospun poly(caprolactone) nanofibers,73 and for precise spatial control of cell adhesion and patterning,74 just to highlight the variety of potential substrates and applications. pDA coatings have even been used to encapsulate and modify the entire surface of yeast cells, with excellent cell survival.75 One of the challenges that must be addressed in this field revolves around the robustness of pDA coatings: although pDA modification permits broad substrate modification and a variety of functional properties, experience in our group has shown that pDA coatings are susceptible to mechanical abrasion. Ultimately, the stability of these coatings will have a direct impact on the extent to which surfaces modified by interfacial adhesion will be utilized in medical, consumer, or industrial applications. Another exciting aspect of synthetic, biologically inspired adhesive materials is the potential for hybrid systems, including those that combine contrasting biological adhesive strategies. For example, in addition to the nonreversible interfaces and materials emphasized in this Perspective, a significant body of work has explored reversible adhesives inspired by fibrillar biological adhesives such as those employed by the gecko.76 In a hybrid approach, mussel-mimetic coatings have been applied on gecko architectures to promote reversible adhesion to a range of substrates in both dry and wet conditions.77,78 There is remarkable potential for (bio)functionalization of nanoscale materials; recently, iron oxide nanoparticle surfaces have been modified with small molecule catechol-derivatized “click”able anchors,79 and pDA coatings have been used to immobilize functional enzyme.80 LbL assembly of clay and branched DOPA-presenting PEG yielded a nanocomposite mimic of seashell nacre.81 Climbing ivy (genus Hedera) produces an adhesive that contains nanoparticles,82,83 and it is anticipated that ivy-inspired composite adhesive materials will evolve as this organism is more thoroughly characterized.
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EXPANDING POTENTIAL APPLICATIONS Thanks to the broad range of surface modification approaches already achieved by mussel-inspired coatings and adhesives, and thanks to the promise of other biological organisms currently 2203
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(22) Ye, Q.; Wang, X.; Li, S.; Zhou, F. Macromolecules 2010, 43, 5554. (23) Zobrist, C.; Sobocinski, J.; Lyskawa, J.; Fournier, D.; Miri, V.; Traisnel, M.; Jimenez, M.; Woisel, P. Macromolecules 2011, 44, 5883. (24) Li, G.; Xue, H.; Cheng, G.; Chen, S.; Zhang, F.; Jiang, S. J. Phys. Chem. B 2008, 112, 15269. (25) Fan, X.; Lin, L.; Messersmith, P. B. Biomacromolecules 2006, 7, 2443. (26) Wach, J.-Y.; Malisova, B.; Bonazzi, S.; Tosatti, S.; Textor, M.; Zürcher, S.; Gademann, K. Chem.Eur. J. 2008, 14, 10579. (27) Dalsin, J. L.; Lin, L.; Tosatti, S.; Vörös, J.; Textor, M.; Messersmith, P. B. Langmuir 2004, 21, 640. (28) Statz, A. R.; Meagher, R. J.; Barron, A. E.; Messersmith, P. B. J. Am. Chem. Soc. 2005, 127, 7972. (29) Dalsin, J. L.; Hu, B.-H.; Lee, B. P.; Messersmith, P. B. J. Am. Chem. Soc. 2003, 125, 4253. (30) Lee, H.; Lee, Y.; Statz, A. R.; Rho, J.; Park, T. G.; Messersmith, P. B. Adv. Mater. 2008, 20, 1619. (31) Lee, B. P.; Chao, C.-Y.; Nunalee, F. N.; Motan, E.; Shull, K. R.; Messersmith, P. B. Macromolecules 2006, 39, 1740. (32) Huang, K.; Lee, B. P.; Ingram, D. R.; Messersmith, P. B. Biomacromolecules 2002, 3, 397. (33) Bilic, G.; Brubaker, C.; Messersmith, P. B.; Mallik, A. S.; Quinn, T. M.; Haller, C.; Done, E.; Gucciardo, L.; Zeisberger, S. M.; Zimmermann, R.; Deprest, J.; Zisch, A. H. Am. J. Obstet. Gynecol. 2010, 202, 85e1. (34) Brubaker, C. E.; Kissler, H.; Wang, L. J.; Kaufman, D. B.; Messersmith, P. B. Biomaterials 2010, 31, 420. (35) Waite, J. H.; Jensen, R. A.; Morse, D. E. Biochemistry 1992, 31, 5733. (36) Zhao, H.; Sun, C.; Stewart, R. J.; Waite, J. H. J. Biol. Chem. 2005, 280, 42938. (37) Stevens, M. J.; Steren, R. E.; Hlady, V.; Stewart, R. J. Langmuir 2007, 23, 5045. (38) Stewart, R. J.; Weaver, J. C.; Morse, D. E.; Waite, J. H. J. Exp. Biol. 2004, 207, 4727. (39) Shao, H.; Bachus, K. N.; Stewart, R. J. Macromol. Biosci. 2009, 9, 464. (40) Shao, H.; Stewart, R. J. Adv. Mater. 2010, 22, 729. (41) Winslow, B. D.; Shao, H.; Stewart, R. J.; Tresco, P. A. Biomaterials 2010, 31, 9373. (42) Endrizzi, B. J.; Stewart, R. J. J. Adhes. 2009, 85, 546. (43) Wang, C. S.; Svendsen, K. K.; Stewart, R. J. Biological Adhesive Systems; Byern, J., Grunwald, I., Eds.; Springer: Vienna, 2010; p 169. (44) Stewart, R. J.; Wang, C. S.; Shao, H. Adv. Colloid Interface Sci. 2011, 167, 85. (45) Stewart, R. J.; Wang, C. S. Biomacromolecules 2010, 11, 969. (46) Dickinson, G. H.; Vega, I. E.; Wahl, K. J.; Orihuela, B.; Beyley, V.; Rodriguez, E. N.; Everett, R. K.; Bonaventura, J.; Rittschof, D. J. Exp. Biol. 2009, 212, 3499. (47) Kamino, K.; Inoue, K.; Maruyama, T.; Takamatsu, N.; Harayama, S.; Shizuri, Y. J. Biol. Chem. 2000, 275, 27360. (48) Naldrett, M. J. J. Mar. Biol. Assoc. U.K. 1993, 73, 689. (49) Barlow, D. E.; Dickinson, G. H.; Orihuela, B.; Kulp, J. L.; Rittschof, D.; Wahl, K. J. Langmuir 2010, 26, 6549. (50) Sullan, R. M. A.; Gunari, N.; Tanur, A. E.; Yuri, C.; Dickinson, G. H.; Orihuela, B.; Rittschof, D.; Walker, G. C. Biofouling 2009, 25, 263. (51) Wiegemann, M.; Watermann, B. J. Adhes. Sci. Technol. 2003, 17, 1957. (52) Kamino, K. Mar. Biotechnol. 2008, 10, 111. (53) Kamino, K. In Biological Adhesives; Smith, A. M., Callow, J. A., Eds.; Springer: Berlin, 2006; p 145. (54) Berglin, M.; Gratenholm, P. Colloids Surf., B 2003, 28, 107. (55) Burkett, J. R.; Hight, L. M.; Kenny, P.; Wilker, J. J. J. Am. Chem. Soc. 2010, 132, 12531. (56) Graham, L. D.; Glattauer, V.; Huson, M. G.; Maxwell, J. M.; Knott, R. B.; White, J. W.; Vaughan, P. R.; Peng, Y.; Tyler, M. J.; Werkmeister, J. A.; Ramshaw, J. A. Biomacromolecules 2005, 6, 3300.
CONCLUSIONS While mussel-mimetic materials have dominated the area of biologically inspired wet adhesive platforms, similar efforts should also be focused on candidate species enjoying a lesser degree of characterization, such that new families of novel materials may develop. These organisms may provide alternatives to DOPA as a strategy around which to inspire synthetic adhesives. Important discoveries are in the near future for other types of post-translationally modified amino acids, for polysaccharide-based systems, for adhesion that depends on discrete structural units, and for multivalent or hybrid platforms. With the advent of nanoscale analytical techniques comes the necessity for more thorough characterization of adhesion at the nanoscale. These efforts will also contribute to better understanding of adhesive lifetime and adhesive failure, which will subsequently demand improved design and synthesis of molecules engineered to mimic biological adhesion. There exists a great deal of promise in this area of research, for developing adhesive interfaces and materials with pertinent biomedical, (bio)technological, industrial, consumer, and military applications.
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AUTHOR INFORMATION
Corresponding Author
*Tel: +1 847 467 5273. Fax: +1 847 491 4928. E-mail: philm@ northwestern.edu (P.M.);
[email protected] (C. B.). Present Address ▽
Laboratory for Regenerative Medicine and Pharmacobiology, Institute of Bioengineering, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland.
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