Advertisement

Multiscale Modeling of Biological Protein Materials – Deformation and Failure

  • Sinan Keten
  • Jeremie Bertaud
  • Dipanjan Sen
  • Zhiping Xu
  • Theodor Ackbarow
  • Markus J. BuehlerEmail author
Chapter
First Online:
Part of the Challenges and Advances in Computational Chemistry and Physics book series (COCH, volume 9)

Abstract

Multi-scale properties of biological protein materials have been the focal point of extensive investigations over the past decades, leading to formation of a research field that connects biology and materials science, referred to as materiomics. In this chapter we review atomistic based modeling approaches applied to study the scale-dependent mechanical behavior of biological protein materials, focused on mechanical deformation and failure properties. Specific examples are provided to illustrate the application of numerical methods that link atomistic to mesoscopic and larger continuum scales. The discussion includes the formulation of atomistic simulation methods, as well as examples that demonstrate their application in case studies focused on size effects of the fracture behavior of protein materials. The link of atomistic scale features of molecular structures to structural scales at length-scales of micrometers will be discussed in the analysis of the mechanics of a simple model of the nuclear lamin network, revealing how protein networks with structural flaws cope with mechanical load

Keywords

Hierarchical material   Nanomechanics   Biological protein materials   Fracture Deformation Experiment Simulation Materiomics Multi-scale modeling 
This is a preview of subscription content, log in to check access.

References

  1. 1.
    Alberts, B., et al., Molecular Biology of the Cell. 2002, New York: Taylor & Francis.Google Scholar
  2. 2.
    Astbury, W.T. and A. Street, X-ray studies of the structures of hair, wool and related fibres. I. General. Transactions of the Royal Society of London A, 1931. 230: 75–101.CrossRefGoogle Scholar
  3. 3.
    Weiner, S. and H.D. Wagner, The material bone: Structure mechanical function relations. Annual Review of Materials Science, 1998. 28: 271–298.CrossRefGoogle Scholar
  4. 4.
    Currey, J.D., Bones: Structure and Mechanics. 2002, Princeton, NJ: Princeton University Press.Google Scholar
  5. 5.
    Lakes, R., Materials with structural hierarchy. Nature, 1993. 361(6412): 511–515.CrossRefGoogle Scholar
  6. 6.
    Wegst, U.G.K. and M.F. Ashby, The mechanical efficiency of natural materials. Philosophical Magazine, 2004. 84(21): 2167–2181.CrossRefGoogle Scholar
  7. 7.
    Vincent, J.F.V., Structural Biomaterials, Edited by Anonymous. 1990, Princeton, NJ: Princeton University Press, p. 244.Google Scholar
  8. 8.
    Fratzl, P. and R. Weinkamer, Nature’s hierarchical materials. Progress in Materials Science, 2007. 52(8): 1263–1334.CrossRefGoogle Scholar
  9. 9.
    Aizenberg, J., et al., Skeleton of Euplectella sp.: Structural hierarchy from the nanoscale to the macroscale. Science, 2005. 309(5732): 275–278.CrossRefGoogle Scholar
  10. 10.
    Courtney, T.H., Mechanical Behavior of Materials. 1990, New York, USA: McGraw-Hill.Google Scholar
  11. 11.
    Broberg, K.B., Cracks and Fracture. 1990, London: Academic Press.Google Scholar
  12. 12.
    Hirth, J.P. and J. Lothe, Theory of Dislocations. 1982, New York: Wiley-Interscience.Google Scholar
  13. 13.
    Fraser, P. and Bickmore, W., Nuclear organization of the genome and the potential for gene regulation. Nature, 2007. 447(7143): 413–417.CrossRefGoogle Scholar
  14. 14.
    Engler, A.J., et al., Matrix elasticity directs stem cell lineage specification. Cell, 2006. 126(4): 677–689.CrossRefGoogle Scholar
  15. 15.
    Buehler, M.J., Atomistic and continuum modeling of mechanical properties of collagen: Elasticity, fracture and self-assembly. Journal of Materials Research, 2006. 21(8): 1947–1961.CrossRefGoogle Scholar
  16. 16.
    Buehler, M.J., Nature designs tough collagen: Explaining the nanostructure of collagen fibrils. Proceedings of the National Academy of Sciences of the United States of America, 2006. 103(33): 12285–12290.CrossRefGoogle Scholar
  17. 17.
    Fratzl, P., et al., Structure and mechanical quality of the collagen-mineral nano-composite in bone. Journal of Materials Chemistry, 2004. 14: 2115–2123.CrossRefGoogle Scholar
  18. 18.
    An, K.N., Y.L. Sun, and Z.P. Luo, Flexibility of type I collagen and mechanical property of connective tissue. Biorheology, 2004. 41(3–4): 239–246.Google Scholar
  19. 19.
    Ramachandran, G.N. and G. Kartha, Structure of collagen. Nature, 1955. 176: 593–595.CrossRefGoogle Scholar
  20. 20.
    Doyle, J., Rules of engagement. Nature, 2007. 446: 860.CrossRefGoogle Scholar
  21. 21.
    Kitano, H., Computational systems biology. Nature, 2002. 420(6912): 206–210.CrossRefGoogle Scholar
  22. 22.
    Kitano, H., Systems biology: A brief overview. Science, 2002. 295(5560): 1662–1664.CrossRefGoogle Scholar
  23. 23.
    Gautieri, A., S. Uzel, S. Vesentini, A. Redaelli, M.J. Buehler, Molecular and mesoscale disease mechanisms of Osteogenesis Imperfecta. Biophysical Journal, 2009. 97(3): 857–865.Google Scholar
  24. 24.
    Suresh, S., et al., Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria. Acta Biomaterialia, 2005. 1(1): 15–30.CrossRefGoogle Scholar
  25. 25.
    Cross, S.E., et al., Nanomechanical analysis of cells from cancer patients. Nature Nanotechnology, 2007. 2: 780–783.CrossRefGoogle Scholar
  26. 26.
    Smith, B.L., et al., Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature, 1999. 399(6738): 761–763.CrossRefGoogle Scholar
  27. 27.
    Prater, C.B., H.J. Butt, and P.K. Hansma, Atomic force microscopy. Nature, 1990. 345(6278): 839–840.CrossRefGoogle Scholar
  28. 28.
    Sun, Y.L., et al., Stretching type II collagen with optical tweezers. Journal of Biomechanics, 2004. 37(11): 1665–1669.CrossRefGoogle Scholar
  29. 29.
    Dao, M., C.T. Lim, and S. Suresh, Mechanics of the human red blood cell deformed by optical tweezers. Journal of the Mechanics and Physics of Solids, 2003. 51(11–12): 2259–2280.CrossRefGoogle Scholar
  30. 30.
    Tai, K., F.J. Ulm, and C. Ortiz, Nanogranular origins of the strength of bone. Nano Letters, 2006. 11: 2520–2525CrossRefGoogle Scholar
  31. 31.
    Lim, C.T., et al., Experimental techniques for single cell and single molecule biomechanics. Materials Science & Engineering C-Biomimetic and Supramolecular Systems, 2006. 26(8): 1278–1288.Google Scholar
  32. 32.
    Goddard, W.A., A perspective of materials modeling in Handbook of Materials Modeling, Edited by S. Yip. 2006, Berlin: Springer.Google Scholar
  33. 33.
    Csete, M.E. and J.C. Doyle, Reverse engineering of biological complexity. Science, 2002. 295(5560): 1664.CrossRefGoogle Scholar
  34. 34.
    Stelling, J., et al., Robustness of cellular functions. Cell, 2004. 118(6): 675–685.CrossRefGoogle Scholar
  35. 35.
    Aizenberg, J., et al., Skeleton of Euplectella sp.: Structural hierarchy from the nanoscale to the macroscale. American Association for the Advancement of Science, 2005. 309: 275–278.Google Scholar
  36. 36.
    Currey, J.D., Materials science: Hierarchies in biomineral structures. Science, 2005. 309: 253–254.CrossRefGoogle Scholar
  37. 37.
    Woesz, A., et al., Micromechanical properties of biological silica in skeletons of deep-sea sponges. Journal of Materials Research, 2006. 21(8): 2069.CrossRefGoogle Scholar
  38. 38.
    Horn, J., N. Nafpliotis, and D.E. Goldberg, A niched Pareto genetic algorithm for multiobjective optimization. Evolutionary Computation, 1994. IEEE World Congress on Computational Intelligence, Proceedings of the First IEEE Conference on 1994, pp. 82–87.Google Scholar
  39. 39.
    Ackbarow, T., et al., Hierarchies, multiple energy barriers and robustness govern the fracture mechanics of alpha-helical and beta-sheet protein domains. Proceedings of the National Academy of Sciences of the United States of America, 2007. 104: 16410–16415CrossRefGoogle Scholar
  40. 40.
    Ackbarow, T. and M.J. Buehler, Hierarchical coexistence of universality and diversity controls robustness and multi-functionality in protein materials. Theoretical and Computational Nanoscience, 2008. 5(7): 1193–1204.CrossRefGoogle Scholar
  41. 41.
    Buehler, M.J., S. Keten, and T. Ackbarow, Theoretical and computational hierarchical nanomechanics of protein materials: Deformation and fracture. Progress in Materials Science, 2008. 53(8): 1101–1241.Google Scholar
  42. 42.
    Tang, Z., et al., Nanostructured artificial nacre. Nature Materials, 2003. 2(6): 413–418.CrossRefGoogle Scholar
  43. 43.
    Vashishta, P., R.K. Kalia, and A. Nakano, Large-scale atomistic simulations of dynamic fracture. Computing in Science and Engineering, 1999. 1 (5): 56–65.CrossRefGoogle Scholar
  44. 44.
    Rountree, C.L., et al., Atomistic aspects of crack propagation in brittle materials: Multimillion atom molecular dynamics simulations. Annual Review of Materials Research, 2002. 32: 377–400.CrossRefGoogle Scholar
  45. 45.
    Buehler, M.J., Atomistic Modeling of Materials Failure. 2008, New York: Springer.CrossRefGoogle Scholar
  46. 46.
    Buehler, M.J. and H.J. Gao, Dynamical fracture instabilities due to local hyperelasticity at crack tips. Nature, 2006. 439(7074): 307–310.CrossRefGoogle Scholar
  47. 47.
    Buehler, M.J., F.F. Abraham, and H. Gao, Hyperelasticity governs dynamic fracture at a critical length scale. Nature, 2003. 426: 141–146.CrossRefGoogle Scholar
  48. 48.
    Buehler, M.J. and H. Gao, Ultra large scale atomistic simulations of dynamic fracture in Handbook of Theoretical and Computational Nanotechnology, Edited by W. Schommers and A. Rieth. 2006, Stevenson Ranch, CA: American Scientific Publishers (ASP).Google Scholar
  49. 49.
    Buehler, M.J., A.C.T.v. Duin, and W.A. Goddard, Multi-paradigm modeling of dynamical crack propagation in silicon using the ReaxFF reactive force field. Physical Review Letters, 2006. 96(9): 095505.CrossRefGoogle Scholar
  50. 50.
    Buehler, M.J., et al., Threshold crack speed controls dynamical fracture of silicon single crystals. Physical Review Letters, 2007. 99: 165502CrossRefGoogle Scholar
  51. 51.
    Wang, W., et al., Biomolecular simulations: Recent developments in force fields, simulations of enzyme catalysis, protein-ligand, protein-protein, and protein-nucleic acid noncovalent interactions. Annual Review of Biophysics and Biomolecular Structure, 2001. 30: 211–243.CrossRefGoogle Scholar
  52. 52.
    Mackerell, A.D., Empirical force fields for biological macromolecules: Overview and issues. Journal of Computational Chemistry, 2004. 25(13): 1584–1604.CrossRefGoogle Scholar
  53. 53.
    Deniz, A.A., S. Mukhopadhyay, and E.A. Lemke, Single-molecule biophysics: at the interface of biology, physics and chemistry. Journal of the Royal Society Interface, 2008. 5(18): 15–45.CrossRefGoogle Scholar
  54. 54.
    Scheraga, H.A., M. Khalili, and A. Liwo, Protein-folding dynamics: Overview of molecular simulation techniques. Annual Review of Physical Chemistry, 2007. 58: 57–83.CrossRefGoogle Scholar
  55. 55.
    Van der Spoel, D., et al., GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 2005. 26(16): 1701–1718.CrossRefGoogle Scholar
  56. 56.
    Nelson, M.T., et al., NAMD: A parallel, object oriented molecular dynamics program. International Journal of Supercomputer Applications and High Performance Computing, 1996. 10(4): 251–268.CrossRefGoogle Scholar
  57. 57.
    Ponder, J. and D. Case, Force fields for protein simulations. Protein Simulations, 2003. 66: 27–85.CrossRefGoogle Scholar
  58. 58.
    MacKerell, A.D., et al., All-atom empirical potential for molecular modeling and dynamics studies of proteins. Journal of Physical Chemistry B, 1998. 102(18): 3586–3616.CrossRefGoogle Scholar
  59. 59.
    Mayo, S.L., B.D. Olafson, and W.A. Goddard, Dreiding – A generic force-field for molecular simulations. Journal of Physical Chemistry, 1990. 94(26): 8897–8909.CrossRefGoogle Scholar
  60. 60.
    Rappe, A.K., et al., Uff, a full periodic-table force-field for molecular mechanics and molecular-dynamics simulations. Journal of the American Chemical Society, 1992. 114(25): 10024–10035.CrossRefGoogle Scholar
  61. 61.
    Pearlman, D.A., et al., Amber, a package of computer-programs for applying molecular mechanics, normal-mode analysis, molecular-dynamics and free-energy calculations to simulate the structural and energetic properties of molecules. Computer Physics Communications, 1995. 91(1–3): 1–41.CrossRefGoogle Scholar
  62. 62.
    Gao, H., A theory of local limiting speed in dynamic fracture. Journal of the Mechanics and Physics of Solids, 1996. 44(9): 1453–1474.CrossRefGoogle Scholar
  63. 63.
    Duin, A.C.T.v., et al., ReaxFF: A reactive force field for hydrocarbons. Journal of Physical Chemistry A, 2001. 105: 9396–9409.CrossRefGoogle Scholar
  64. 64.
    Brenner, D.W., et al., A second-generation reactive empirical bond order (REBO) potential energy expression for hydrocarbons. Journal of Physics-Condensed Matter, 2002. 14(4): 783–802.CrossRefGoogle Scholar
  65. 65.
    Stuart, S.J., A.B. Tutein, and J.A. Harrison, A reactive potential for hydrocarbons with intermolecular interactions. Journal of Chemical Physics, 2000. 112(14): 6472–6486.CrossRefGoogle Scholar
  66. 66.
    Strachan, A., et al., Shock waves in high-energy materials: The initial chemical events in nitramine RDX. Physical Review Letters, 2003. 91(9): 098301-1–098301-4.CrossRefGoogle Scholar
  67. 67.
    Nielson, K.D., et al., Development of the ReaxFF reactive force field for describing transition metal catalyzed reactions, with application to the initial stages of the catalytic formation of carbon nanotubes. Journal of Physical Chemistry A, 2005. 109: 49.CrossRefGoogle Scholar
  68. 68.
    Duin, A.C.T.v., et al., ReaxFF SiO: Reactive force field for silicon and silicon oxide systems. Journal of Physical Chemistry A, 2003. 107: 3803–3811.CrossRefGoogle Scholar
  69. 69.
    Han, S.S., et al., Optimization and application of lithium parameters for the reactive force field, ReaxFF. Journal of Physical Chemistry A, 2005. 109(20): 4575–4582.CrossRefGoogle Scholar
  70. 70.
    Chenoweth, K., et al., Simulations on the thermal decomposition of a poly(dimethylsiloxane) polymer using the ReaxFF reactive force field. Journal of the American Chemical Society, 2005. 127(19): 7192–7202.CrossRefGoogle Scholar
  71. 71.
    Strachan, A., et al., Thermal decomposition of RDX from reactive molecular dynamics. Journal of Chemical Physics, 2005. 122(5): 054502CrossRefGoogle Scholar
  72. 72.
    Cheung, S., et al., ReaxFF(MgH) reactive force field for magnesium hydride systems. Journal of Physical Chemistry A, 2005. 109(5): 851–859.CrossRefGoogle Scholar
  73. 73.
    Chenoweth, K., et al., Development and application of a ReaxFF reactive force field for oxidative dehydrogenation on vanadium oxide catalysts. Journal of Physical Chemistry C, 2005. 112: 14645–14654.Google Scholar
  74. 74.
    Buehler, M.J., Hierarchical chemo-nanomechanics of stretching protein molecules: Entropic elasticity, protein unfolding and molecular fracture. Journal of Mechanics of Materials and Structures, 2007. 2(6): 1019–1057.CrossRefGoogle Scholar
  75. 75.
    Datta, D., A.C.T.v. Duin, and W.A. Goddard, Extending ReaxFF to Biomacromolecules. Unpublished, 2005.Google Scholar
  76. 76.
    Buehler, M.J., et al., The Computational Materials Design Facility (CMDF): A powerful framework for multiparadigm multi-scale simulations. Materials Research Society Proceedings, 2006. 894: LL3.8.Google Scholar
  77. 77.
    Tozzini, V., Coarse-grained models for proteins. Current Opinion in Structural Biology, 2005. 15(2): 144–150.CrossRefGoogle Scholar
  78. 78.
    Tirion, M., Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Physical Review Letters, 1996. 77(9): 1905–1908.CrossRefGoogle Scholar
  79. 79.
    Haliloglu, T., I. Bahar, and B. Erman, Gaussian dynamics of folded proteins. Physical Review Letters, 1997. 79(16): 3090–3093.CrossRefGoogle Scholar
  80. 80.
    Hayward, S. and N. Go, Collective variable description of native protein dynamics. Annual Review of Physical Chemistry, 1995. 46: 223–250.CrossRefGoogle Scholar
  81. 81.
    West, D.K., et al., Mechanical resistance of proteins explained using simple molecular models. Biophysical Journal, 2006. 90(1): 287–297.CrossRefGoogle Scholar
  82. 82.
    Dietz, H. and M. Rief, Elastic bond network model for protein unfolding mechanics. Physical Review Letters, 2008. 1(9): 098101-1–098101-4.Google Scholar
  83. 83.
    Sulkowska, J.I. and M. Cieplak, Mechanical stretching of proteins – a theoretical survey of the Protein Data Bank. Journal of Physics-Condensed Matter, 2007. 19(28): 283201.CrossRefGoogle Scholar
  84. 84.
    Bathe, M., A finite element framework for computation of protein normal modes and mechanical response. Proteins-Structure Function and Bioinformatics, 2008. 70(4): 1595–1609.CrossRefGoogle Scholar
  85. 85.
    Bahar, I. and R. Jernigan, Inter-residue potentials in globular proteins and the dominance of highly specific hydrophilic interactions at close separation. Journal of Molecular Biology, 1997. 266(1): 195–214.CrossRefGoogle Scholar
  86. 86.
    Nguyen, H. and C. Hall, Molecular dynamics simulations of spontaneous fibril formation by random-coil peptides. Proceedings of the National Academy of Sciences of the United States of America, 2004. 101(46): 16180–16185.CrossRefGoogle Scholar
  87. 87.
    Nguyen, H. and C. Hall, Spontaneous fibril formation by polyalanines: Discontinuous molecular dynamics simulations. Journal of the American Chemical Society, 2006. 128(6): 1890–1901.CrossRefGoogle Scholar
  88. 88.
    Arkhipov, A., P. L. Freddolino, et al., Coarse-grained molecular dynamics simulations of a rotating bacterial flagellum. Biophysical Journal, 2006. 91(12): 4589–4597.Google Scholar
  89. 89.
    Buehler, M.J., Nature designs tough collagen: Explaining the nanostructure of collagen fibrils. Proceedings of the National Academy of Sciences of the United States of America, 2006. 103(33): 12285–12290.CrossRefGoogle Scholar
  90. 90.
    Buehler, M., Molecular nanomechanics of nascent bone: fibrillar toughening by mineralization. Nanotechnology, 2007. 18(29): 295102.CrossRefGoogle Scholar
  91. 91.
    Chen, J., W. Im, and C. Brooks, Balancing solvation and intramolecular interactions: Toward a consistent generalized born force field. Journal of the American Chemical Society, 2006. 128(11): 3728–3736.CrossRefGoogle Scholar
  92. 92.
    Chen, J., C. Brooks, and J. Khandogin, Recent advances in implicit solvent-based methods for biomolecular simulations. Current Opinion in Structural Biology, 2008. 18(2): 140–148.Google Scholar
  93. 93.
    Roux, B. and T. Simonson, Implicit solvent models. Biophysical Chemistry, 1999. 78(1–2): 1–20.CrossRefGoogle Scholar
  94. 94.
    Bertaud, J., Z. Qin, M.J. Buehler, Atomistically informed mesoscale model of alpha-helical protein domains, I International Journal for Multiscale Computational Engineering, 2009. 7(3): 237–250.Google Scholar
  95. 95.
    Ackbarow, T., D. Sen, C. Thaulow, and M.J. Buehler, Alpha-helical protein networks are self protective and flaw tolerant, PLoS ONE, 2009. 4(6): e6015.Google Scholar
  96. 96.
    Aebi, U., et al., The nuclear lamina is a meshwork of intermediate-type filaments. Nature, 1986. 323(6088): 560–564.CrossRefGoogle Scholar
  97. 97.
    Ackbarow, T. and M.J. Buehler, Superelasticity, energy dissipation and strain hardening of vimentin coiled-coil intermediate filaments: Atomistic and continuum studies. Journal of Materials Science, 2007 42(21): 8771–8787.CrossRefGoogle Scholar
  98. 98.
    Buehler, M.J. and S. Keten, 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
  99. 99.
    Fudge, D.S., et al., The mechanical properties of hydrated intermediate filaments: Insights from hagfish slime threads. Biophysical Journal, 2003. 85(3): 2015–2027.CrossRefGoogle Scholar
  100. 100.
    Fudge, D.S. and J.M. Gosline, Molecular design of the alpha-keratin composite: insights from a matrix-free model, hagfish slime threads. Proceedings of the Royal Society of London Series B-Biological Sciences, 2004. 271(1536): 291–299.CrossRefGoogle Scholar
  101. 101.
    Bell, G.I., Models for the specific adhesion of cells to cells. Science, 1978. 200(4342): 618–627.CrossRefGoogle Scholar
  102. 102.
    Hanggi, P., P. Talkner, and M. Borkovec, Reaction-rate theory: Fifty years after Kramers. Review of Modern Physics, 1990. 62(2): 251–341.CrossRefGoogle Scholar
  103. 103.
    Zhurkov, S.N., Kinetic concept of the strength of solids. International Journal of Fracture Mechanics, 1965. 1: 311–323.Google Scholar
  104. 104.
    Evans, E. and K. Ritchie, Dynamic strength of molecular adhesion bonds. Biophysical Journal, 1997. 72(4): 1541–1555.CrossRefGoogle Scholar
  105. 105.
    Hyeon, C. and D. Thirumalai, Measuring the energy landscape roughness and the transition state location of biomolecules using single molecule mechanical unfolding experiments. Journal of Physics, Condensed Matter, 2007. 19(11): 113101.CrossRefGoogle Scholar
  106. 106.
    Seifert, U., Rupture of multiple parallel molecular bonds under dynamic loading. Physical Review Letters, 2000. 84(12): 2750–2753.CrossRefGoogle Scholar
  107. 107.
    Seifert, U., Dynamic strength of adhesion molecules: Role of rebinding and self-consistent rates. Europhysics Letters, 2002. 58(5): 792–798.CrossRefGoogle Scholar
  108. 108.
    Evans, E., Probing the relation between force-lifetime-and chemistry in single molecular bonds. Annual Reviews in Biophysics and Biomolecular Structure, 2001. 30(1): 105–128.CrossRefGoogle Scholar
  109. 109.
    Hummer, G. and A. Szabo, Kinetics from nonequilibrium single-molecule pulling experiments. Biophysical Journal, 2003. 85(1): 5–15.CrossRefGoogle Scholar
  110. 110.
    Walton, E.B., S. Lee, and K.J. Van Vliet, Extending Bell’s model: How force transducer stiffness alters measured unbinding forces and kinetics of molecular complexes. Biophysical Journal, 2008. 94(7): 2621.CrossRefGoogle Scholar
  111. 111.
    Zwanzig, R., Diffusion in a rough potential. Proceedings of the National Academy of Sciences of the United States of America, 1988. 85(7): 2029–2030.CrossRefGoogle Scholar
  112. 112.
    Erdmann, T. and U.S. Schwarz, Stability of adhesion clusters under constant force. Physical Review Letters, 2004. 92(10): 108102.CrossRefGoogle Scholar
  113. 113.
    Erdmann, T. and U.S. Schwarz, Bistability of cell-matrix adhesions resulting from nonlinear receptor-ligand dynamics. Biophysical Journal, 2006. 91(6): L60.CrossRefGoogle Scholar
  114. 114.
    Erdmann, T. and U.S. Schwarz, Stability of adhesion clusters under constant force. Physical Review Letters, 2004. 92(10): 4.CrossRefGoogle Scholar
  115. 115.
    Rief, M., J.M. Fernandez, and H.E. Gaub, Elastically coupled two-level systems as a model for biopolymer extensibility. Physical Review Letters, 1998. 81(21): 4764–4767.CrossRefGoogle Scholar
  116. 116.
    Dietz, H. and M. Rief, Elastic bond network model for protein unfolding mechanics. Physical Review Letters, 2008. 100(9): 98101.CrossRefGoogle Scholar
  117. 117.
    Buehler, M.J. and T. Ackbarow, Fracture mechanics of protein materials. Materials Today, 2007. 10(9): 46–58.CrossRefGoogle Scholar
  118. 118.
    Keten, S. and M.J. Buehler, Asymptotic strength limit of hydrogen bond assemblies in proteins at vanishing pulling rates. Physical Review Letters, 2008. 100: 198301.Google Scholar
  119. 119.
    Keten, S. and M.J. Buehler, Geometric confinement governs the rupture strength of H-bond assemblies at a critical length scale. Nano Letters, 2008. 8(2): 743–748.CrossRefGoogle Scholar
  120. 120.
    Yip, S., The strongest size. Nature, 1998. 391: 532–533.CrossRefGoogle Scholar
  121. 121.
    Wolf, D., et al., Deformation mechanism and inverse Hall-Petch behavior in nanocrystalline materials. Zeitschrift für Metallkunde, 2003. 94: 1052–1061.Google Scholar
  122. 122.
    Gruber, M. and A.N. Lupas, Historical review: Another 50th anniversary – new periodicities in coiled coils. Trends in Biochemical Sciences, 2003. 28(12): 679–685.CrossRefGoogle Scholar
  123. 123.
    Moir, R.D. and T.P. Spann, The structure and function of nuclear lamins: implications for disease. Cellular and Molecular Life Sciences, 2001. 58(12–13): 1748–1757.CrossRefGoogle Scholar
  124. 124.
    Wilson, K.L., M.S. Zastrow, and K.K. Lee, Lamins and disease: Insights into nuclear infrastructure. Cell, 2001. 104(5): 647–650.Google Scholar
  125. 125.
    Bryson, J.W., et al., Protein design – a hierarachical approach. Science, 1995. 270(5238): 935–941.CrossRefGoogle Scholar
  126. 126.
    Kirshenbaum, K., R.N. Zuckermann, and K.A. Dill, Designing polymers that mimic biomolecules. Current Opinion in Structural Biology, 1999. 9(4): 530–535.CrossRefGoogle Scholar
  127. 127.
    Kim, S. and P.A. Coulombe, Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes & Development, 2007. 21(13): 1581–1597.CrossRefGoogle Scholar
  128. 128.
    Herrmann, H., et al., Intermediate filaments: from cell architecture to nanomechanics. Nature Reviews Molecular Cell Biology, 2007. 8(7): 562–573.CrossRefGoogle Scholar
  129. 129.
    Ackbarow, T., S. Keten, and M.J. Buehler, A multi-timescale strength model of alpha-helical protein domains, Journal of Physics: Condensed Matter, 2009. 21: 035111.Google Scholar
  130. 130.
    Bell, G.I., Models for specific adhesion of cells to cells. Science, 1978. 200(4342): 618–627.CrossRefGoogle Scholar
  131. 131.
    Evans, E.A. and D.A. Calderwood, Forces and bond dynamics in cell adhesion. Science, 2007. 316(5828): 1148–1153.CrossRefGoogle Scholar
  132. 132.
    Evans, E., Probing the relation between force – lifetime – and chemistry in single molecular bonds. Annual Review of Biophysics and Biomolecular Structure, 2001. 30: 105–128.CrossRefGoogle Scholar
  133. 133.
    Evans, E.B., Looking inside molecular bonds at biological interfaces with dynamic force spectroscopy. Biophysical Chemistry, 1999. 82(2–3): 83–97.CrossRefGoogle Scholar
  134. 134.
    Merkel, R., et al., Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature (London), 1999. 379(6714): 50–53.Google Scholar
  135. 135.
    Dudko, O.K., G. Hummer, and A. Szabo, Intrinsic rates and activation free energies from single-molecule pulling experiments. Physical Review Letters, 2006. 96(10): 108101.CrossRefGoogle Scholar
  136. 136.
    Makarov, D.E., Unraveling individual molecules by mechanical forces: Theory meets experiment. Biophysical Journal, 2007. 92(12): 4135–4136.CrossRefGoogle Scholar
  137. 137.
    West, D.K., P.D. Olmsted, and E. Paci, Mechanical unfolding revisited through a simple but realistic model. Journal of Chemical Physics, 2006. 124(15): 154909.Google Scholar
  138. 138.
    Erdmann, T. and U.S. Schwarz, Stability of adhesion clusters under constant force. Physical Review Letters, 2004. 92(10): 108102.CrossRefGoogle Scholar
  139. 139.
    Lantz, M.A., et al., Stretching the alpha-helix: A direct measure of the hydrogen-bond energy of a single-peptide molecule. Chemical Physics Letters, 1999. 315(1–2): 61–68.CrossRefGoogle Scholar
  140. 140.
    Kageshima, M., et al., Insight into conformational changes of a single alpha-helix peptide molecule through stiffness measurements. Chemical Physics Letters, 2001. 343(1–2): 77–82.CrossRefGoogle Scholar
  141. 141.
    Dudko, O.K., et al., Extracting kinetics from single-molecule force spectroscopy: Nanopore unzipping of DNA hairpins. Biophysical Journal, 2007. 92(12): 4188–4195.CrossRefGoogle Scholar
  142. 142.
    Keten, S. and M.J. Buehler. Strength limit of entropic elasticity in beta-sheet protein domains. Physical Review E (Statistical, Nonlinear, and Soft Matter Physics), 2008. 78(6): 061913.Google Scholar
  143. 143.
    Griffith, A.A., The phenomenon of rupture and flows in solids. Philosophical Transactions of the Royal Society of London A, 1920. 221: 163–198.Google Scholar
  144. 144.
    Sheu, S.-Y., et al., Energetics of hydrogen bonds in peptides. PNAS, 2003. 100(22): 12683–12687.CrossRefGoogle Scholar
  145. 145.
    Rief, M., et al., Single molecule force spectroscopy of spectrin repeats: Low unfolding forces in helix bundles. Journal of Molecular Biology, 1999. 286(2): 553–561.CrossRefGoogle Scholar
  146. 146.
    Law, R., et al., Influence of lateral association on forced unfolding of antiparallel spectrin heterodimers. Journal of Biological Chemistry, 2004. 279(16): 16410–16416.CrossRefGoogle Scholar
  147. 147.
    Lenne, P.F., et al., Stales and transitions during forced unfolding of a single spectrin repeat. FEBS Letters, 2000. 476(3): 124–128.CrossRefGoogle Scholar
  148. 148.
    Law, R., et al., Cooperativity in forced unfolding of tandem spectrin repeats. Biophysical Journal, 2003. 84(1): 533–544.CrossRefGoogle Scholar
  149. 149.
    Law, R., et al., Pathway shifts and thermal softening in temperature-coupled forced unfolding of spectrin domains. Biophysical Journal, 2003. 85(5): 3286–3293.CrossRefGoogle Scholar
  150. 150.
    Bernstein, F.C., et al., Protein data bank – computer-based archival file for macromolecular structures. Journal of Molecular Biology, 1977. 112(3): 535–542.CrossRefGoogle Scholar
  151. 151.
    Kolano, C., et al., Watching hydrogen-bond dynamics in a beta-turn by transient two-dimensional infrared spectroscopy. Nature, 2006. 444(7118): 469–472.CrossRefGoogle Scholar
  152. 152.
    Grandbois, M., et al., How strong is a covalent bond? Science, 1999. 283(5408): 1727–1730.CrossRefGoogle Scholar
  153. 153.
    Bustamante, C., et al., Entropic elasticity of lambda-phage DNA. Science, 1994. 265(5178): 1599–1600.CrossRefGoogle Scholar
  154. 154.
    Marko, J.F. and E.D. Siggia, Stretching DNA. Macromolecules, 1995. 28(26): 8759–8770.CrossRefGoogle Scholar
  155. 155.
    Zhuang, X., Molecular biology: Unraveling DNA condensation with optical tweezers. Science, 2004. 305(5681): 188–190.CrossRefGoogle Scholar
  156. 156.
    Lang, M., Lighting up the mechanome, in Frontiers of Engineering: Reports on Leading-Edge Engineering from the 2007 Symposium. 2008, National Academy of Engineering of the National Academies.Google Scholar
  157. 157.
    Ebenstein, D.M. and L.A. Pruitt, Nanoindentation of biological materials. Nano Today, 2006. 1(3): 26–33.CrossRefGoogle Scholar
  158. 158.
    Bozec, L., et al., Atomic force microscopy of collagen structure in bone and dentine revealed by osteoclastic resorption. Ultramicroscopy, 2005. 105(1–4): 79–89.CrossRefGoogle Scholar
  159. 159.
    Guzman, C., et al., Exploring the mechanical properties of single vimentin intermediate filaments by atomic force microscopy. Journal of Molecular Biology, 2006. 360(3): 623–630.CrossRefGoogle Scholar
  160. 160.
    Yuan, C.B., et al., Energy landscape of streptavidin-biotin complexes measured by atomic force microscopy. Biochemistry, 2000. 39(33): 10219–10223.CrossRefGoogle Scholar
  161. 161.
    Sun, Y.L., Z.P. Luo, and K.N. An, Stretching short biopolymers using optical tweezers. Biochemical and Biophysical Research Communications, 2001. 286(4): 826–830.CrossRefGoogle Scholar
  162. 162.
    Sazonova, V., et al., A tunable carbon nanotube electromechanical oscillator. Nature, 2004. 431(7006): 284–287.CrossRefGoogle Scholar
  163. 163.
    Thorsen, T., S.J. Maerkl, and S.R. Quake, Microfluidic large-scale integration. Science, 2002. 298(5593): 580–584.CrossRefGoogle Scholar
  164. 164.
    Whitesides, G.M. and B. Grzybowski, Self-assembly at all scales. Science, 2002. 295(5564): 2418–2421.CrossRefGoogle Scholar
  165. 165.
    Yan, H., et al., DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science, 2003. 301(5641): 1882–1884.CrossRefGoogle Scholar
  166. 166.
    Rho, J.Y., L. Kuhn-Spearing, and P. Zioupos, Mechanical properties and the hierarchical structure of bone. Medical Engineering and Physics, 1998. 20(2): 92–102.CrossRefGoogle Scholar
  167. 167.
    Currey, J.D., Mechanical properties of mother of pearl in tension. Proceedings of the Royal Society of London. Series B, Biological Sciences, 1977. 196(1125): 443–463.CrossRefGoogle Scholar
  168. 168.
    Menig, R., et al., Quasi-static and dynamic mechanical response of Strombus gigas (conch) shells. Materials Science & Engineering A, 2001. 297(1–2): 203–211.CrossRefGoogle Scholar
  169. 169.
    Tesch, W., et al., Graded microstructure and mechanical properties of human crown dentin. Calcified Tissue International, 2001. 69(3): 147–157.CrossRefGoogle Scholar
  170. 170.
    Ritchie, R., M.J. Buehler, P. Hansma. The strength and toughness of bone, Physics Today, 2009. 62(6): 41-47.Google Scholar
  171. 171.
    Taylor, D., J.G. Hazenberg, and T.C. Lee, Living with cracks: Damage and repair in human bone. Nature Materials, 2007. 6(4): 263–266.CrossRefGoogle Scholar
  172. 172.
    Nalla, R.K., J.J. Kruzic, and R.O. Ritchie, On the origin of the toughness of mineralized tissue: Microcracking or crack bridging? Bone, 2004. 34(5): 790–798.CrossRefGoogle Scholar
  173. 173.
    Gao, H., et al., From the cover: Materials become insensitive to flaws at nanoscale: Lessons from nature. Proceedings of the National Academy of Sciences of the United States of America, 2003. 100(10): 5597.CrossRefGoogle Scholar
  174. 174.
    Mann, S., et al., Crystallization at Inorganic-organic Interfaces: Biominerals and biomimetic synthesis. Science, 1993. 261(5126): 1286–1292.CrossRefGoogle Scholar
  175. 175.
    Gilbert, P., M. Abrecht, and B.H. Frazer, The organic-mineral interface in biominerals. Reviews in Mineralogy and Geochemistry, 2005. 59(1): 157–185.CrossRefGoogle Scholar
  176. 176.
    Smith, B.L., et al., Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature, 1999. 399(6738): 761–763.CrossRefGoogle Scholar
  177. 177.
    Broedling, N.C., et al., The strength limit in a bio-inspired metallic nanocomposite. Journal of Mechanics and Physics of Solids, 2008. 56(3): 1086–1104.CrossRefGoogle Scholar
  178. 178.
    Sen, D. and M.J. Buehler, Crystal size controlled deformation mechanism: Breakdown of dislocation mediated plasticity in single nanocrystals under geometric confinement. Physical Review B, 2008. 77(19): 195439.CrossRefGoogle Scholar
  179. 179.
    Sen, D. and M.J. Buehler, Shock loading of bone-inspired metallic nanocomposites. Solid State Phenomena, 2008. 139: 11–22.Google Scholar
  180. 180.
    Whitesides, G.M., J.P. Mathias, and C.T. Seto, Molecular self-assembly and nanochemistry: A chemical strategy for the synthesis of nanostructures. Science, 1991. 254(5036): 1312–1319.CrossRefGoogle Scholar
  181. 181.
    Whitesides, G.M. and B. Grzybowski, Self-assembly at all scales. Science, 2002. 295: 2418–2421.CrossRefGoogle Scholar
  182. 182.
    Bejan, A., Constructal theory: From thermodynamic and geometric optimization to predicting shape in nature. Energy Conversion and Management, 1998. 39(16–18): 1705–1718.CrossRefGoogle Scholar
  183. 183.
    Kim, P., et al., Thermal Transport Measurements of Individual Multiwalled Nanotubes. Physical Review Letters, 2001. 87(21): 215502.CrossRefGoogle Scholar
  184. 184.
    Balandin, A.A., et al., Superior thermal conductivity of single-layer graphene. Nano Letters, 2008. 8(3): 902–907.CrossRefGoogle Scholar
  185. 185.
    Meng, G., et al., Controlled fabrication of hierarchically branched nanopores, nanotubes, and nanowires. Proceedings of the National Academy of Sciences of the United States of America, 2005. 102(20): 7074–7078.CrossRefGoogle Scholar
  186. 186.
    Shinde, S.L. and J.S. Goela, eds. High Thermal Conductivity Materials. 2004, New York: Springer, p. 271.Google Scholar
  187. 187.
    Langer, R. and D.A. Tirrell, Designing materials for biology and medicine. Nature, 2004. 428(6982): 487–492.CrossRefGoogle Scholar
  188. 188.
    Zhao, X.J. and S.G. Zhang, Designer self-assembling peptide materials. Macromolecular Bioscience, 2007. 7(1): 13–22.CrossRefGoogle Scholar
  189. 189.
    Holland, J.H., Hidden Order – How Adaptation Builds Complexity. 1995, Reading, MA: Helix Books.Google Scholar
  190. 190.
    Ackbarow, T. and M.J. Buehler, Hierarchical coexistence of universality and diversity controls robustness and multi-functionality in protein materials. Journal of Computational and Theoretical Nanoscience, 2008. 5(7): 1193–1204.Google Scholar
  191. 191.
    Cui, X.Q., et al., Biocatalytic generation of ppy-enzyme-CNT nanocomposite: From network assembly to film growth. Journal of Physical Chemistry C, 2007. 111(5): 2025–2031.CrossRefGoogle Scholar
  192. 192.
    Hule, R., D. Pochan, Polymer nanocomposites for biomedical application. MRS Bulletin, 2007. 32(4): 5.Google Scholar
  193. 193.
    Winey, K.I., Vaia R.A., Polymer nanocomposites. MRS Bulletin, 2007. 32(4): 5.Google Scholar
  194. 194.
    Petka, W.A., et al., Reversible hydrogels from self-assembling artificial proteins. Science, 1998. 281(5375): 389–392.CrossRefGoogle Scholar
  195. 195.
    Smeenk, J.M., et al., Controlled assembly of macromolecular beta-sheet fibrils. Angewandte Chemie-International Edition, 2005. 44(13): 1968–1971.CrossRefGoogle Scholar
  196. 196.
    Zhao, X.J. and S.G. Zhang, Molecular designer self-assembling peptides. Chemical Society Reviews, 2006. 35(11): 1105–1110.CrossRefGoogle Scholar
  197. 197.
    Mershin, A., et al., A classic assembly of nanobiomaterials. Nature Biotechnology, 2005. 23(11): 1379–1380.CrossRefGoogle Scholar
  198. 198.
    Aebi, U., et al., The nuclear lamina is a meshwork of intermediate-type filaments. Nature, 1986. 323(6088): 560–564.CrossRefGoogle Scholar
  199. 199.
    Buehler, M.J., Hierarchical chemo-nanomechanics of proteins: Entropic elasticity, protein unfolding and molecular fracture. Journal of Mechanics of Materials and Structures, 2007. 2(6): 1019–1057.CrossRefGoogle Scholar
  200. 200.
    Ashby, M.F., et al., The mechanical properties of natural materials. I. Material property charts. Proceedings of the Mathematical and Physical Sciences, 1995. 450(1938): 123–140.CrossRefGoogle Scholar
  201. 201.
    Fratzl, P., et al., Structure and mechanical quality of the collagen–mineral nano-composite in bone. Journal of Materials Chemistry, 2004. 14(14): 2115–2123.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Sinan Keten
    • 1
  • Jeremie Bertaud
    • 1
  • Dipanjan Sen
    • 1
    • 2
  • Zhiping Xu
    • 1
  • Theodor Ackbarow
    • 1
  • Markus J. Buehler
    • 1
    Email author
  1. 1.Laboratory for Atomistic and Molecular Mechanics, Department of Civil and Environmental EngineeringMassachusetts Institute of TechnologyCambridgeUSA
  2. 2.Department of Materials Science and EngineeringMassachusetts Institute of TechnologyCambridgeUSA

Personalised recommendations

Cite chapter

Buy options