Materiomics: Biological Protein Materials, from Nano to Macro

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Materiomics: Biological Protein Materials, from Nano to Macro Materiomics: biological protein materials, from nano to macro The MIT Faculty has made this article openly available. Please share how this access benefits you. Your story matters. Citation Buehler, Markus J., and Cranford. “Materiomics: Biological Protein Materials, from Nano to Macro.” Nanotechnology, Science and Applications (2010): 127. As Published http://dx.doi.org/10.2147/NSA.S9037 Publisher Dove Medical Press Version Final published version Citable link http://hdl.handle.net/1721.1/73614 Terms of Use Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. Nanotechnology, Science and Applications Dovepress open access to scientific and medical research Open Access Full Text Article REVIEW Materiomics: biological protein materials, from nano to macro Steven Cranford Abstract: Materiomics is an emerging field of science that provides a basis for multiscale material Markus J Buehler system characterization, inspired in part by natural, for example, protein-based materials. Here we outline the scope and explain the motivation of the field of materiomics, as well as demonstrate Center for Materials Science and Engineering, Laboratory for Atomistic the benefits of a materiomic approach in the understanding of biological and natural materials as and Molecular Mechanics, Department well as in the design of de novo materials. We discuss recent studies that exemplify the impact of Civil and Environmental Engineering, Massachusetts Institute of materiomics – discovering Nature’s complexity through a materials science approach that of Technology, Cambridge, MA, USA merges concepts of material and structure throughout all scales and incorporates feedback loops that facilitate sensing and resulting structural changes at multiple scales. The development and application of materiomics is illustrated for the specific case of protein-based materials, which constitute the building blocks of a variety of biological systems such as tendon, bone, skin, spider silk, cells, and tissue, as well as natural composite material systems (a combination of protein- based and inorganic constituents) such as nacre and mollusk shells, and other natural multiscale systems such as cellulose-based plant and wood materials. An important trait of these materials is that they display distinctive hierarchical structures across multiple scales, where molecular details are exhibited in macroscale mechanical responses. Protein materials are intriguing examples of materials that balance multiple tasks, representing some of the most sustainable material solu- tions that integrate structure and function despite severe limitations in the quality and quantity of material building blocks. However, up until now, our attempts to analyze and replicate Nature’s materials have been hindered by our lack of fundamental understanding of these materials’ intri- cate hierarchical structures, scale-bridging mechanisms, and complex material components that bestow protein-based materials their unique properties. Recent advances in analytical tools and experimental methods allow a holistic view of such a hierarchical biological material system. The integration of these approaches and amalgamation of material properties at all scale levels to develop a complete description of a material system falls within the emerging field of mate- riomics. Materiomics is the result of the convergence of engineering and materials science with experimental and computational biology in the context of natural and synthetic materials. Through materiomics, fundamental advances in our understanding of structure–property–process relations Correspondence: Markus J Buehler of biological systems contribute to the mechanistic understanding of certain diseases and facilitate Laboratory for Atomistic and Molecular Mechanics, Department of Civil and the development of novel biological, biologically inspired, and completely synthetic materials for Environmental Engineering, Massachusetts applications in medicine (biomaterials), nanotechnology, and engineering. Institute of Technology, 77 Massachusetts Keywords: biological materials, hierarchies, multiscale, materiomics, deformation, failure, Ave Room 1-235 A&B, Cambridge, MA, USA; Center for Materials Science and functional material properties, protein, peptide, universality, diversity Engineering, Massachusetts Institute of Technology, 77 Massachusetts Ave, Cambridge, MA, USA; Introduction: motivated by Nature Tel +1 617 452 2750 Advances in imaging methods over the past decades have revealed that biology cre- Fax +1 617 324 4014 Email [email protected] ates intricate hierarchical structures, which when initiated at nanoscales, result in submit your manuscript | www.dovepress.com Nanotechnology, Science and Applications 2010:3 127–148 127 Dovepress © 2010 Cranford and Buehler, publisher and licensee Dove Medical Press Ltd. This is an Open Access DOI: 10.2147/NSA.S9037 article which permits unrestricted noncommercial use, provided the original work is properly cited. Cranford and Buehler Dovepress macro or physiological multifunctional materials to provide scale and how this relates to macroscopic phenomena such structural support, force generation, catalytic properties, or as cell mechanics, tissue behavior, or functions provided by energy conversion.1–5 This is exemplified in a rather wide entire organisms. This has resulted in the cross-disciplinary range of biological materials such as hair, skin, bone, spider investigation of protein materials and structures, diseases, silk, or cells, which play important roles in providing key as well as the development of novel treatment and diag- functions to biological systems.6 Yet conventional engineering nostics methods.10–15 There is an accelerated progression methods, focused often on analyses at single or few scales and convergence of biology, chemistry, materials science, (encompassing such fields as structural analysis and con- and engineering, each contributing different aspects of the tinuum theory, eg, continuum mechanics), typically lack complexity of Nature’s design. The merger of such per- the framework required for the complexities introduced by spectives is mutually beneficial: materials scientists have multiscale interactions, the materials’ discrete hierarchi- extensive experience in treating structures, processes, and cal composition, and structure–property dependencies at properties of materials systematically and with rigorous all scales as found in many natural materials. Mechanical mathematical methods, whereas biologists have gained a notions of stress and strain, fracture and plasticity, and detailed understanding of biological systems and structures toughness and robustness are inherently linked to material and related functions by utilizing both physiological models behavior at the nanoscale. Similarly, chemical and biological and powerful statistical correlations between, for example, techniques (including such fields as microbiology, proteom- genetics and physiology and pathology. ics, and condensed matter physics) shed vast insights on There is accelerating interest in the discovery and nanoscale phenomena, such as the chemical composition of understanding of Nature’s structural design rules, in par- materials or the interactions of residues, but lack the associa- ticular for nanoscopic hierarchical molecular structures, tion with mechanical properties. Significant advances have and to make them available to engineers to pave the way for been made in many disciplines and research areas, ranging tomorrow’s supermaterials (eg, mechanomutable materials, throughout a variety of scales, from atomistic and molecular advanced composites, low-density low-energy structural to continuum. In tandem, experimental studies have attained materials, etc.), seamlessly blending synthetic materials with nanoscale precision, lending insights into molecular defects biological systems (eg, tissue and biomedical engineering), and mechanisms. As a result of these advances in disparate and using basic biological systems as templates for design fields of science, a fully integrated and holistic paradigm (eg, biomimetic and bio-inspired materials). There is also a now emerges as a powerful approach that can be broadly surprizing relationship between these material design issues applied to elucidate Nature’s design principles, to facilitate and the understanding (or rather lack thereof) of genetic the design of novel materials with exceptional material diseases and disorders, where structural changes are due properties, and to understand a variety of diseases from a to mutations on the molecular level which lead to changed fundamental point of view. chemical and mechanical properties, which in turn lead The study of material properties of biological protein to a malfunction of the protein network under mechanical materials has witnessed an exciting development over the load. This type of effort, the linking of mechanisms across past several years, partly due to the emergence of physical multiple scales by using a materials science approach to pro- science-based approaches in the biological sciences. Specifi- vide structure–property–process (SPP) links, characterizes cally, there has been significant effort directed toward the the emerging field of materiomics.16 The term materiomics explanation and control of observed macroscopic mechanical has been proposed with various definitions in the past (see and optical
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