Editorial Cite This: Chem. Rev. 2017, 117, 12581-12583
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Introduction: Bioinspired and Biomimetic Materials
T
largely emanate from the evolutionary arms race, the process of natural selection.12 For instance, the light emitted from the sun has influenced the course of natural selection on the earth. The ability to see and perceive further led to the development of camouflaging abilities as a means of survival, while some species have developed a magnificent color palette as a consequence of mating preferences, visual communication, and signaling. In addition to the remarkable color contrast that nature offers, there is an enormous diversity in the optical structures and signal transduction mechanisms that led to more sophisticated visual cues like UV and infrared vision, polarized vision, and night vision. Interestingly, despite the use of a limited materials palette, nature exhibits spectacular optical phenomena including tailored absorption and transparency, diffraction, interference, reflection and antireflection, scattering, light harvesting, waveguiding and lensing, camouflage, and bioluminescence that are responsible for the unique optical properties of materials and structures found in biology. Apart from discussing the optical materials and phenomena in biology, the review also provides examples of synthetic optical materials that are inspired by the structure, properties, and/or functionality of natural optical materials. A critical need for biomimetic materials in cellular biology is functional systems to control and quantify the biophysics and differentiation of cells. A key challenge here, as described by Xu and co-workers, is tailoring bulk material properties that represent remote boundary conditions for cells while simultaneously controlling the biophysics and biochemistry of the extracellular microenvironment.13 In this review, a broad literature of contributions reporting dynamic, time-evolving “four dimensional” materials for this purpose is described. However, with a few exceptions, the state of the art suffers from a trade-off that remains to be addressed, namely a trade-off between achieving physiologically representative stiffness and a physiologically relevant fibrous microenvironment. While highlighting several systems for characterizing the spatiotemporal evolution in cellular microenvironments, the review also notes broad gaps in our knowledge of what is present in the four-dimensional cell microenvironment in vivo and the associated need for new materials to characterize this. Biological systems are dynamic, and living organisms exhibit an ability to change structure and properties as a means to adapt to their environment and survive. The reversible mechanical morphing in many living organisms in response to a stimulus is a striking example of smart materials found in nature. Weder and co-workers summarize bioinspired stimuliresponsive materials that exhibit tunable mechanical properties.14 Materials with tunable mechanical properties pave the way for the development of complex material systems ranging from active dampening systems to soft robotics. Reversible transformation in the mechanical properties in many natural and synthetic material systems is a result of hierarchical
he process of natural selection has led to the evolution of numerous materials, structures, models, systems, and processes that have been optimized for a broad range of functions. Biomimicry or bioinspiration involves learning nature’s design principles in building highly complex and sophisticated engineering models at various length scales and utilizing the wealth of knowledge to solve the critical challenges faced by humanity.1−3 Considering that natural materials and systems have evolved to perform a broad variety of functions including structural support, signal transduction, actuation, sensing, catalysis, trafficking, gating, light-harvesting, charge transfer, molecular recognition, self-assembly, self-organization, self-replication, or combinations of two or more of these functions, nature’s “solution manual” is quite exhaustive. Learning from this exhaustive solution manual and gaining inspiration or even directly applying the design principles can be a highly effective approach to solving various critical global challenges such as food, water, homeland security, public health, and clean energy. The reviews in this special issue focus on some of the topics related to bioinspired and biomimetic materials. Molecular recognition and self-assembly is vital for the structure, properties, and function of numerous materials and systems in the natural world. In this issue, two reviews exclusively focus on the biorecognition and self-assembly of biological materials. DNA has emerged as a powerful building block at the nanoscale. Phenomenal progress has been made in past 10 years in using this biological building block to realize various intricate structures at the nanoscale.4 The self-assembling abilities of DNA have been harnessed to realize tailored assemblies of functional nanostructures.5 The review by Yan and co-workers provides a comprehensive survey of the recent developments in DNA origami (folding DNA into a desired shape).6 The complex nanoscale structures enabled by DNA origami are finding numerous applications in electronics, nanophotonics, and reaction networks. Understanding the mechanistic aspects of the formation and (self-)assembly of biomaterials would greatly benefit the design and fabrication of biomimetic materials with tailored properties and function. One of the biomimetic approaches pertaining to materials fabrication relies on using peptides that are believed to bind with growing inorganic surfaces and direct the growth of the inorganic materials.7,8 Knecht and Walsh elucidate the biointerfacial structure/property/function relationships of peptides and nanomaterials.9 Understanding the molecular structure of the peptides adsorbed on material systems and their influence on the formation of biointerfaces is challenging and can provide insights into the mechanism of formation various functional materials in nature. By exploiting these biointerfacial interactions and designing specific biomolecules, functional materials derived from interfacing peptides with inorganic materials have found applications in assembly, catalysis, energy, and medicine.10,11 The review by Singamaneni and co-workers provides a summary of the optical materials and phenomena in nature that © 2017 American Chemical Society
Special Issue: Bioinspired and Biomimetic Materials Published: October 25, 2017 12581
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structuring and the modulation of interactions between the key components. The modulation of mechanical properties in most biomimetic materials is due to the presence of energy absorbing domains, sacrificial supramolecular structures, shape-memory, actuation, reorientation of reinforcing components, or strain hardening. Despite numerous successful demonstrations of responsive biomimetic materials, the extent of actuation is a trade-off between the dynamics of the switching and the modulation in the mechanical properties. A review by Chen and co-workers summarizes the materials and flexible electronic device designs inspired by natural materials and living organisms.20 Special attention is paid to nature inspired structural materials that accommodate large mechanical deformation while maintaining the functionality of the devices designed for various application such as mechanical sensing and energy harvesting. Moving beyond biomimetic and bioinspired materials, bioinspiration and biomimetic approaches are finding numerous applications in the smart design of advanced devices such as chemical and biological sensors, actuators, photonics and plasmonic devices, and flexible electronic devices.15−17 A review by Tsukruk and co-workers describes the design, synthesis, and application of hierarchical nanostructures for biological sensors.18 The review provides an extensive summary of numerous hybrid nanostructures and tailored bioconjugation procedures that have been developed over the past few years for the highly sensitive and selective biosensing in noisy biological environments. As justly pointed out by Prof. Whitesides, bioinspiration is a virtually limitless source of ideas and it has “something for everyone”.19 Notwithstanding the 14 000+ papers published since 2010, the field of bioinspiration and biomimicry is still considered to be young and offers enormous potential for surprising discoveries, which are almost certain to inspire the design and fabrication of novel materials with intriguing properties and function. Bioinspired materials and strategies have certainly opened new venues for the fabrication of optical devices, sensors, and materials. However, the lack of defined design rules, incompatibility of biomaterials and processes with existing fabrication techniques limit their application. The recent development of 3D printing techniques and other additive fabrication techniques allows one to mimic biological structures and introduce biological functions using biobased inks. These developments take us a step closer to truly achieving the promise of bioinspired materials and structures for real-world applications. Emerging areas such as synthetic biology can enhance our ability to develop designer molecules, synthesize defined biopolymers, and achieve molecular control of biological machines. Combining advanced fabrication techniques with synthetic biology could result in the construction of integrated systems across multiple length scales achieving hierarchical structures that are dynamic and responsive similar to their natural counterparts. It is our hope that the reviews in this special issue will serve as excellent references in their respective areas and inspire many aspiring researchers to contribute to this very exciting field of bioinspired and biomimetic materials. More importantly, spurring innovative minds by applying multidisciplinary approaches, cutting edge tools, and techniques to harvest the enormous potential offered by biological systems to address societal challenges.
711th Human Performance Wing, Air Force Research Laboratory, Wright−Patterson Air Force Base, Dayton, Ohio 45433, United States
Srikanth Singamaneni*
Department of Mechanical Engineering and Materials Science and Institute of Materials Science and Engineering, Washington University in St. Louis, St. Louis, Missouri 63130, United States
AUTHOR INFORMATION Corresponding Author
*Phone: 314-935-5407. E-mail:
[email protected]. ORCID
Rajesh R. Naik: 0000-0002-7677-928X Srikanth Singamaneni: 0000-0002-7203-2613 Notes
Views expressed in this editorial are those of the authors and not necessarily the views of the ACS. Biographies Rajesh R. Naik obtained his B.S. in Microbiology from the University of Bombay, India, in 1990 and a Ph.D. in the field of Molecular Biology from Carnegie-Mellon University, Pittsburgh, PA, in 1998. He later worked as a Howard Hughes Research Fellow at the Center for Advanced Biotechnology and Medicine at Rutgers University. He joined Materials and Manufacturing Directorate at the Air Force Research Laboratory, Dayton, Ohio, in 1999 as a research scientist, where he was assigned the position of Biotechnology Group Leader. In 2007, he was appointed the technology advisor for biotechnology in the Nanostructure and Biological Materials Branch. He also served as the Chair for AFRL's Bio-X Strategic Technology Team from 2008 to 2011. Currently, he is the Chief Scientist of the 711th Human Performance Wing of the Air Force Research Laboratory, Air Force Materiel Command. His research interests include biologically enabled routes to advanced inorganic and composite materials, protein engineering, bioelectronics, biomimetic sensors for chem−bio detection, and the interface between biological and nanomaterials. Srikanth Singamaneni obtained his Bachelors in electronics and communication engineering from Nagarjuna University in 2002 and masters in electrical engineering in electrical engineering from Western Michigan University in 2004. He received his Ph.D. in polymer materials science and engineering from Georgia Institute of Technology in 2009. He was an assistant professor in the Department of Mechanical Engineering and Materials Science at Washington University in St. Louis from 2010 to 2015. Currently, he is an associate professor in the Department of Mechanical Engineering and Materials Science. His research interests include the design, synthesis, and selfassembly of plasmonic nanostructures for various biomedical applications, multifunctional materials based on nanocellulose, metalorganic frameworks for biopreservation, bioinspired structural and functional materials, polymer surfaces and interfaces, responsive and adaptive materials and scanning probe microscopy, and surface force spectroscopy of soft and biological materials.
REFERENCES (1) Bhushan, B. Biomimetics: lessons from nature - an overview. Philos. Trans. R. Soc., A 2009, 367, 1445−1486. (2) Lepora, N. F.; Verschure, P.; Prescott, T. J. The state of the art in biomimetics. Bioinspiration Biomimetics 2013, 8, 013001. (3) Wegst, U. G. K.; Bai, H.; Saiz, E.; Tomsia, A. P.; Ritchie, R. O. Bioinspired structural materials. Nat. Mater. 2015, 14, 23−36.
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(4) Rothemund, P. W. K. Folding DNA to create nanoscale shapes and patterns. Nature 2006, 440, 297−302. (5) Jones, M. R.; Seeman, N. C.; Mirkin, C. A. Programmable materials and the nature of the DNA bond. Science 2015, 347, 1260901. (6) Hong, F.; Zhang, F.; Liu, Y.; Yan, H. DNA Origami: Scaffolds for Creating Higher Order Structures. Chem. Rev. 2017, 117, 20 10.1021/ acs.chemrev.6b00825. (7) Dickerson, M. B.; Sandhage, K. H.; Naik, R. R. Protein- and Peptide-Directed Syntheses of Inorganic Materials. Chem. Rev. 2008, 108, 4935−4978. (8) Sarikaya, M.; Tamerler, C.; Jen, A. K. Y.; Schulten, K.; Baneyx, F. Molecular biomimetics: nanotechnology through biology. Nat. Mater. 2003, 2, 577−585. (9) Walsh, T. R.; Knecht, M. R. Biointerface Structural Effects on the Properties and Applications of Bioinspired Peptide-Based Nanomaterials. Chem. Rev. 2017, 117, 20 10.1021/acs.chemrev.7b00139. (10) Coppage, R.; Slocik, J. M.; Ramezani-Dakhel, H.; Bedford, N. M.; Heinz, H.; Naik, R. R.; Knecht, M. R. Exploiting Localized Surface Binding Effects to Enhance the Catalytic Reactivity of Peptide-Capped Nanoparticles. J. Am. Chem. Soc. 2013, 135, 11048−11054. (11) Pacardo, D. B.; Sethi, M.; Jones, S. E.; Naik, R. R.; Knecht, M. R. Biomimetic Synthesis of Pd Nanocatalysts for the Stille Coupling Reaction. ACS Nano 2009, 3, 1288−1296. (12) Tadepalli, S.; Slocik, J.; Gupta, M.; Naik, R. R.; Singamaneni, S. Bio-optics and Bioinspired Optical Materials. Chem. Rev. 2017, 117, 20, 10.1021/acs.chemrev.7b00153. (13) Huang, G.; Li, F.; Zhao, X.; Ma, Y.; Li, Y.; Lin, M.; Jin, G.; Lu, T. J.; Genin, G.; Xu, F. Functional and Biomimetic Materials for Engineering of the Three-Dimensional Cell Microenvironment. Chem. Rev. 2017, 117, 20, 10.1021/acs.chemrev.7b00094. (14) Montero de Espinosa, L.; Meesorn, W.; Moatsou, D.; Weder, C. Bioinspired Polymer Systems with Stimuli-Responsive Mechanical Properties. Chem. Rev. 2017, 117, 20, 10.1021/acs.chemrev.7b00168. (15) Ko, H.; Javey, A. Smart Actuators and Adhesives for Reconfigurable Matter. Acc. Chem. Res. 2017, 50, 691−702. (16) Choi, M. K.; Park, O. K.; Choi, C.; Qiao, S.; Ghaffari, R.; Kim, J.; Lee, D. J.; Kim, M.; Hyun, W.; Kim, S. J.; Hwang, H. J.; Kwon, S.H.; Hyeon, T.; Lu, N.; Kim, D.-H. Cephalopod-Inspired Miniaturized Suction Cups for Smart Medical Skin. Adv. Healthcare Mater. 2016, 5, 80−87. (17) McConney, M. E.; Anderson, K. D.; Brott, L. L.; Naik, R. R.; Tsukruk, V. V. Bioinspired Material Approaches to Sensing. Adv. Funct. Mater. 2009, 19, 2527−2544. (18) Zhang, S.; Geryak, R.; Geldmeier, J.; Kim, S.; Tsukruk, V. V.; Synthesis, Assembly, and Applications of Hybrid Nanostructures for Biosensing. Chem. Rev. 2017 117, 20, 10.1021/acs.chemrev.7b00088. (19) Whitesides, G. M. Bioinspiration: something for everyone. Interface Focus 2015, 5, 20150031. (20) Liu, Y.; He, K.; Chen, G.; Leow, W. R.; Chen, X. NatureInspired Structural Materials for Flexible Electronic Devices. Chem. Rev. 2017, 117, 20, 10.1021/acs.chemrev.7b00291.
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