Acta Mechanica Solida Sinica

, Volume 23, Issue 6, pp 471–483 | Cite as

Multiscale mechanics of biological and biologically inspired materials and structures

Article

Abstract

The world of natural materials and structures provides an abundance of applications in which mechanics is a critical issue for our understanding of functional material properties. In particular, the mechanical properties of biological materials and structures play an important role in virtually all physiological processes and at all scales, from the molecular and nanoscale to the macroscale, linking research fields as diverse as genetics to structural mechanics in an approach referred to as materiomics. Example cases that illustrate the importance of mechanics in biology include mechanical support provided by materials like bone, the facilitation of locomotion capabilities by muscle and tendon, or the protection against environmental impact by materials as the skin or armors. In this article we review recent progress and case studies, relevant for a variety of applications that range from medicine to civil engineering. We demonstrate the importance of fundamental mechanistic insight at multiple time- and length-scales to arrive at a systematic understanding of materials and structures in biology, in the context of both physiological and disease states and for the development of de novo biomaterials. Three particularly intriguing issues that will be discussed here include: First, the capacity of biological systems to turn weakness to strength through the utilization of multiple structural levels within the universality-diversity paradigm. Second, material breakdown in extreme and disease conditions. And third, we review an example where the hierarchical design paradigm found in natural protein materials has been applied in the development of a novel biomaterial based on amyloid protein.

Key words

biological materials materiomics mechanics mechanical properties mutability tunability deformation failure 

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References

  1. [1]
    Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. and Walter, P., Molecular Biology of the Cell. New York: Taylor & Francis, 2002.Google Scholar
  2. [2]
    Fratzl, P. and Weinkamer, R., Nature’s hierarchical materials. Progress in Materials Science, 2007, 52: 1263–1334.CrossRefGoogle Scholar
  3. [3]
    Meyers, M.A., Chen, P.Y., Lin, A.Y.M. and Seki, Y., Biological materials: Structure and mechanical properties. Progress in Materials Science, 2008, 53(1): 1–206.CrossRefGoogle Scholar
  4. [4]
    Lakes, R., Materials with structural hierarchy. Nature, 1993, 361(6412): 511–515.CrossRefGoogle Scholar
  5. [5]
    Buehler, M.J., Tu(r)ning weakness to strength. Nano Today, 2010, 5(5): 379–383.CrossRefGoogle Scholar
  6. [6]
    Buehler, M.J. and Yung, Y.C., Deformation and failure of protein materials in physiologically extreme conditions and disease. Nature Materials, 2009, 8(3): 175–188.CrossRefGoogle Scholar
  7. [7]
    Buehler, M.J. and Yung, Y.C., How protein materials balance strength, robustness and adaptability. HFSP Journal, 2010, 4(1): 26–40.CrossRefGoogle Scholar
  8. [8]
    Cranford, S. and Buehler, M.J., Materiomics: biological protein materials, from nano to macro. Journal of Nanotechnology, Science and Applications, 2010, 3: 127–148.Google Scholar
  9. [9]
    Buehler, M.J., Strength in numbers. Nature Nanotechnology, 2010, 5(3): 172–174.CrossRefGoogle Scholar
  10. [10]
    Paparcone, R., Cranford, S.W. and Buehler, M.J., Self-folding and aggregation of amyloid fibrils. in submission.Google Scholar
  11. [11]
    Buehler, M.J. and Keten, S., Failure of molecules, bones, and the earth itself. Reviews of Modern Physics, 2010, 82: 1459–1487.CrossRefGoogle Scholar
  12. [12]
    Prockop, D.J. and Kivirikko, K.I., Collagens: molecular biology, diseases, and potentials for therapy. Annual Review of Biochemistry, 1995, 64: 403–434.CrossRefGoogle Scholar
  13. [13]
    Byers, P.H., Wallis, G.A. and Willing, M.C., Osteogenesis imperfecta: translation of mutation to phenotype. Journal of Medical Genetics, 1991, 28(7): 433–442.CrossRefGoogle Scholar
  14. [14]
    Gautieri, A., Vesentini, S., Redaelli, A. and Buehler, M.J., Single molecule effects of osteogenesis imperfecta mutations in tropocollagen protein domains. Protein Science, 2009, 18(1): 161–168.Google Scholar
  15. [15]
    Gautieri, A., Uzel, S., Vesentini, S., Redaelli, A. and Buehler, M.J., Molecular and mesoscale mechanisms of osteogenesis imperfecta disease in collagen fibrils. Biophysical Journal, 2009, 97(3): 857–865.CrossRefGoogle Scholar
  16. [16]
    Hudson, B.G., Tryggvason, K., Sundaramoorthy, M. and Neilson, E.G., Alport’s syndrome, goodpasture’s syndrome, and type IV collagen. New England Journal of Medicine, 2003, 348(25): 2543–2556.CrossRefGoogle Scholar
  17. [17]
    Godsel, L.M., Hobbs, R.P. and Green, K.J., Intermediate filament assembly: dynamics to disease. Trends in Cell Biology, 2008, 18(1): 28–37.CrossRefGoogle Scholar
  18. [18]
    Buehler, M.J., Atomistic Modeling of Materials Failure. New York: Springer, 2008.CrossRefGoogle Scholar
  19. [19]
    Dahl, K.N., Kahn, S.M., Wilson, K.L. and Discher, D.E., The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. Journal of Cell Science, 2004, 117(20): 4779–4786.CrossRefGoogle Scholar
  20. [20]
    Gumbsch, P., Riedle, J., Hartmaier, A. and Fischmeister, H.F., Controlling factors for the brittle-to-ductile transition in Tungsten single crystals. Science, 1998, 282(5392): 1293–1295.CrossRefGoogle Scholar
  21. [21]
    Dietz, H. and Rief, M., Elastic bond network model for protein unfolding mechanics. Physical Review Letters, 2008, 100(9): 4.CrossRefGoogle Scholar
  22. [22]
    Rauch, F. and Glorieux, F.H., Osteogenesis imperfecta. Lancet, 2004, 363(9418): 1377–1385.CrossRefGoogle Scholar
  23. [23]
    Miller, E., Delos, D., Baldini, T., Wright, T.M. and Camacho, N.P., Abnormal mineral-matrix interactions are a significant contributor to fragility in oim/oim bone. Calcified Tissue International, 2007, 81(3): 206–214.CrossRefGoogle Scholar
  24. [24]
    Buehler, M.J. and Keten, S., Elasticity, strength and resilience: A comparative study on mechanical signatures of α-helix, β-sheet and tropocollagen domains. Nano Research, 2008, 1(1): 63–71.CrossRefGoogle Scholar
  25. [25]
    Buehler, M.J., Nature designs tough collagen: Explaining the nanostructure of collagen fibrils. Roceedings Of the National Academy of Sciences of the United States of America, 2006, 103(33): 12285–12290.CrossRefGoogle Scholar
  26. [26]
    Gao, H., Ji, B., Jäger, I.L., Arzt, E. and Fratzl, P., Materials become insensitive to flaws at nanoscale: lessons from nature. Roceedings of the National Academy of Sciences of the United States of America, 2003, 100(10): 5597–5600.CrossRefGoogle Scholar
  27. [27]
    Hamm, C.E., Merkel, R., Springer, O., Jurkojc, P., Maier, C., Prechtel, K. and Smetacek, V., Architecture and material properties of diatom shells provide effective mechanical protection. Nature, 2003, 421(6925): 841–843.CrossRefGoogle Scholar
  28. [28]
    Garcia, A.P., Sen, D., and Buehler, M.J., Hierarchical silica nanostructures inspired by diatom algae yield superior deformability, toughness and strength. Metallurgical and Materials Transactions A-Physical Metallurgy and Materials Science, 2010, Doi: 10.1007/s11661-010-0477-y.CrossRefGoogle Scholar
  29. [29]
    Garcia, A.P. and Buehler, M.J., Bioinspired nanoporous silicon provides great toughness at great deformability. Computational Materials Science, 2010, 48(2): 303–309.CrossRefGoogle Scholar
  30. [30]
    Cranford, S. and Buehler, M.J., Mechanomutable carbon nanotube arrays. International Journal of Material and Structural Integrity, 2009, 3(2–3): 161–178.CrossRefGoogle Scholar
  31. [31]
    Trotter, J.A., Tipper, J., Lyons-Levy, G., Chino, K., Heuer, A.H., Liu, Z., Mrksich, M., Hodneland, C., Dillmore, W.S., Koob, T.J., Koob-Emunds, M.M., Kadler, K. and Holmes, D., Towards a fibrous composite with dynamically controlled stiffness: lessons from echinoderms. Biochemistry Society Transactions, 2000, 28(4): 357–362.CrossRefGoogle Scholar
  32. [32]
    Schmidt, D.J., Cebeci, F.C., Kalcioglu, Z.I., Wyman, S.G., Ortiz, C., Van Vliet, K.J. and Hammond, P.T., Electrochemically controlled swelling and mechanical properties of a polymer nanocomposite. ACS Nano, 2009, 3(8): 2207–2216.CrossRefGoogle Scholar
  33. [33]
    Cranford, S., Ortiz, C. and Buehler, M.J., Mechanomutable properties of a PAA/PAH polyelectrolyte complex: rate dependence and ionization effects on tunable adhesion strength. Soft Matter, 2010, 6: 4175–4188.CrossRefGoogle Scholar
  34. [34]
    Vollrath, F. and Porter, D., Spider silk as archetypal protein elastomer. Soft Matter, 2006, 2(5): 377–385.CrossRefGoogle Scholar
  35. [35]
    Rammensee, S., Slotta, U., Scheibel, T. and Bausch, A.R., Assembly mechanism of recombinant spider silk proteins. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(18): 6590–6595.CrossRefGoogle Scholar
  36. [36]
    Keten, S., Xu, Z., Ihle, B. and Buehler, M.J., Nanoconfinement controls stiffness, strength and mechanical toughness of beta-sheet crystals in silk. Nature Materials, 2010, 9(4): 359–367.CrossRefGoogle Scholar
  37. [37]
    Keten, S. and Buehler, M.J., Geometric confinement governs the rupture strength of H-bond assemblies at a critical length scale. Nano Letters, 2008, 8(2): 743–748.CrossRefGoogle Scholar
  38. [38]
    Nova, A., Keten, S., Pugno, N.M., Redaelli, A. and Buehler, M.J., Molecular and nanostructural mechanisms of deformation, strength and toughness of spider silk fibrils. Nano Letters, 2010, 10(7): 2626–2634.CrossRefGoogle Scholar
  39. [39]
    Xu, Z. and Buehler, M.J., Mechanical energy transfer and dissipation in fibrous beta-sheet-rich proteins. Physical Review E, 2010, 81: 061910.CrossRefGoogle Scholar
  40. [40]
    Keten, S. and Buehler, M.J., Nanostructure and molecular mechanics of spider dragline silk protein assemblies. Journal of the Royal Society Interface, 2010, 7(53): 1709–1721.CrossRefGoogle Scholar
  41. [41]
    Knowles, T.P.J., Oppenheim, T., Buell, A.K., Chirgadze, D.Y. and Welland, M.E., Nanostructured biofilms from hierarchical self-assembly of amyloidogenic proteins. Nature Nanotechnology, 2010, 5: 204–207.CrossRefGoogle Scholar
  42. [42]
    Chiti, F. and Dobson, C.M., Protein misfolding, functional amyloid, and human disease. Annual Review of Biochemistry, 2006, 75: 333–366.CrossRefGoogle Scholar
  43. [43]
    Mostaert, A.S., Giordani, C., Crockett, R., Karsten, U., Schumann, R. and Jarvis, S.P., Characterisation of amyloid nanostructures in the natural adhesive of unicellular subaerial algae. Journal of Adhesion, 2009, 85(8): 465–483.CrossRefGoogle Scholar
  44. [44]
    Ackbarow, T., Sen, D., Thaulow, C. and Buehler, M.J., Alpha-helical protein networks are self protective and flaw tolerant. PLoS ONE, 2009, 4(6): e6015.CrossRefGoogle Scholar
  45. [45]
    Kamien, R., Music: An Appreciation. McGraw-Hill Humanities/Social Sciences/Languages, 2007.Google Scholar
  46. [46]
    Dodge, C. and Jerse, T.A., Computer Music: synthesis, Composition, and Performance. Cengage Learning, 1997.Google Scholar

Copyright information

© The Chinese Society of Theoretical and Applied Mechanics and Technology 2010

Authors and Affiliations

  1. 1.Laboratory for Atomistic and Molecular Mechanics, Department of Civil and Environmental EngineeringMassachusetts Institute of TechnologyCambridgeUSA
  2. 2.Center for Computational EngineeringMassachusetts Institute of TechnologyCambridgeUSA
  3. 3.Center for Materials Science and EngineeringMassachusetts Institute of TechnologyCambridgeUSA

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