Deformation and failure of protein materials in physiologically extreme conditions and disease

Nature Materials

Volumn 8, Issue 3, 2009, Pages 175-188

  Buehler, Markus J ^a,b   Yung, Yu Ching ^c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b USA   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEFORMATION; PHYSIOLOGY; PROTEINS;

BIOLOGICAL PROCESS; BIOLOGICAL PROTEINS; BIOLOGICAL STRUCTURES; DEFORMATION AND FAILURES; HIERARCHICAL STRUCTURES; MICROSCOPIC LEVELS; PHYSIOLOGICAL MATERIALS; THEORETICAL METHODS;

BIOLOGICAL MATERIALS;

PROTEIN;

BIOLOGICAL MODEL; BIOMECHANICS; CHEMISTRY; GENERAL ASPECTS OF DISEASE; GENETICS; MATERIALS; NANOTECHNOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; REVIEW;

BIOMECHANICS; DISEASE; MANUFACTURED MATERIALS; MODELS, BIOLOGICAL; NANOTECHNOLOGY; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 60949107887     PISSN: 14761122     EISSN: 14764660     Source Type: Journal    
DOI: 10.1038/nmat2387     Document Type: Review

References (143)

1. Alberts, B. et al. Molecular Biology of the Cell. (Taylor & Francis, 2002).
2. Wang, N. & Stamenovic, D. Mechanics of vimentin intermediate filaments. J. Muscle Res. Cell. Motil. 23, 535-540 (2002).
3. Ingber, D. E. et al. in International Review of Cytology: A Survey of Cell Biology Vol 150, 173-224 (Academic, 1994).
4. Fratzl, P. & Weinkamer, R. Nature's hierarchical materials. Prog. Mater. Sci. 52, 1263-1334 (2007).
5. Gelse, K., Poschl, E. & Aigner, T. Collagens - structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 55, 1531-1546 (2003).
6. Liu, W. et al. Fibrin fibers have extraordinary extensibility and elasticity. Science 313, 634-634 (2006).
7. Weisel, J. W. Biophysics: Enigmas of blood clot elasticity. Science 320, 456-457 (2008).
8. Brown, A. E. X., Litvinov, R. I., Discher, D. E. & Weisel, J. W. Forced unfolding of the coiled-coils of fibrinogen by single molecule AFM. Biophys. J. 92, 39-41 (2007).
9. Lim, B. B. C., Lee, E. H., Sotomayor, M. & Schulten, K. Molecular basis of fibrin clot elasticity. Structure 16, 449-459 (2008).
10. Ideker, T., Galitski, T. & Hood, L. A new approach to decoding life: Systems biology. Annu. Rev. Genom. Hum. Genet. 2, 343-372 (2001).
11. Kitano, H. Computational systems biology. Nature 420, 206-210 (2002).
12. Kim, S. & Coulombe, P. A. Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes Dev. 21, 1581-1597 (2007).
13. Kreplak, L. & Fudge, D. Biomechanical properties of intermediate filaments: from tissues to single filaments and back. BioEssays 29, 26-35 (2007).
14. Herrmann, H. & Aebi, U. Intermediate filaments: Molecular structure, assembly mechanism, and integration into functionally distinct intracellular scaffolds. Annu. Rev. Bioehem. 73, 749-789 (2004).
15. Strelkov, S. V., Herrmann, H. & Aebi, U. Molecular architecture of intermediate filaments. BioEssays 25, 243-251 (2003).
16. Aebi, U., Cohn, J., Buhle, L. & Gerace, L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature 323, 560-564 (1986).
17. Rowat, A. C., Lammerding, J., Herrmann, H. & Aebi, U. Towards an integrated understanding of the structure and mechanics of the cell nucleus. BioEssays 30, 226-236 (2008).
18. Vaziri, A. & Gopinath, A. Cell and biomolecular mechanics in silico. Nature Mater. (2007).
19. Vaziri, A. & Mofrad, M. R. K. Mechanics and deformation of the nucleus in micropipette aspiration experiment. J. Biomech. 40, 2053-2062 (2007).
20. Lim, C. T., Zhou, E. H., Li, A., Vedula, S. R. K. & Fu, H. X. Experimental techniques for single cell and single molecule biomechanics. Mater. Sci. Eng. C: Biomim. Supramol. Syst. 26, 1278-1288 (2006).
21. Wilson, K. L., Zastrow, M. S. & Lee, K. K. Lamins and disease: Insights into nuclear infrastructure. Cell 104, 647-650 (2001).
22. Dahl, K. N. et al. Distinct structural and mechanical properties of the nuclear lamina in Hutchinson-Gilford progeria syndrome. Proc. Natl Acad. Sci. USA 103, 10271-10276 (2006).
23. Ingber, D. E. Cellular mechanotransduction: putting all the pieces together again. FASEBJ. 20, 811-827 (2006).
24. Omary, M. B., Coulombe, P. A. & McLean, W. H. I. Mechanisms of disease: Intermediate filament proteins and their associated diseases. N. Engl. J. Med. 351, 2087-2100 (2004).
25. Hulmes, D. J. S., Wess, T. J., Prockop, D. J. & Fratzl, P. Radial packing, order, and disorder in collagen fibrils. Biophys. J. 68, 1661-1670 (1995).
26. Sasaki, N. & Odajima, S. Elongation mechanism of collagen fibrils and forcestrain relations of tendon at each level of structural hierarchy. J. Biomech. 29, 1131-1136 (1996).
27. Orgel, J. P. R. O., Irving, T. C., Miller, A. & Wess, T. J. Microfibrillar structure of type I collagen in situ. Proc. Natl Acad. Sci. USA 103, 9001-9005 (1995).
28. Weiner, S. & Wagner, H. D. The material bone: Structure mechanical function relations. Annu. Rev. Mater. Sci. 28, 271-298 (1998).
29. Nalla, R. K., Kinney, J. H. & Ritchie, R. O. Mechanistic fracture criteria for the failure of human cortical bone. Nature Mater. 2, 164-168 (2003).
30. Ramachandran, G. N. & Kartha, G. Structure of collagen. Nature 176, 593-595 (1955).
31. Buehler, M. J. & Wong, S. Y. Entropie elasticity controls nanomechanics of single tropocollagen molecules. Biophys. J. 93, 37-43 (2007).
32. Gupta, H. S. et al. Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc. Natl Acad. Sci. USA 103, 17741-17746 (2006).
33. Gupta, H. S. et al. Evidence for an elementary process in bone plasticity with an activation enthalpy of 1 eV. J. R. Soc. Interf. 4, 277-282 (2007).
34. Buehler, M. J. Nature designs tough collagen: Explaining the nanostructure of collagen fibrils. Proc. Natl Acad. Sci. USA 103, 12285-12290 (2006).
35. Gao, H., Ji, B., Jäger, I. L., Arzt, E. & Fratzl, P. Materials become insensitive to flaws at nanoscale: Lessons from nature. Proc. Natl Acad. Sci. USA 100, 5597-5600 (2003).
36. Taylor, D., Hazenberg, J. G. & Lee, T. C. Living with cracks: Damage and repair in human bone. Nature Mater. 6, 263-266 (2007).
37. Janmey, P. A., Leterrier, J. F. & Herrmann, H. Assembly and structure of neurofilaments. Curr. Opin. Colloid Interf. Sci. 8, 40-47 (2003).
38. Bini, E., Knight, D. P. & Kaplan, D. L. Mapping domain structures in silks from insects and spiders related to protein assembly. J., Mol. Biol. 335, 27-40 (2004).
39. Rammensee, S., Slotta, U., Scheibel, T. & Bausch, A. R. Assembly mechanism of recombinant spider silk proteins. Proc. Natl Acad. Sci. USA 105, 6590-6595 (2008).
40. Petka, W. A., Harden, J. L., McGrath, K. P., Wirtz, D. & Tirrell, D. A. Reversible hydrogels from self-assembling artificial proteins. Science 281, 389-392 (1998).
41. Zhao, X. J. & Zhang, S. G. Molecular designer self-assembling peptides. Chem. Soc. Rev. 35, 1105-1110 (2006).
42. Langer, R. & Tirrell, D. A. Designing materials for biology and medicine. Nature 428, 487-492 (2004).
43. Smeenk, J. M. et al. Controlled assembly of macromolecular beta-sheet fibrils. Angew. Chem. Int. Edn 44, 1968-1971 (2005).
44. Mershin, A., Cook, B., Kaiser, L. & Zhang, S. G. A classic assembly of nanobiomaterials. Nature Bioteehnol. 23, 1379-1380 (2005).
45. van Hest, J. C. M. & Tirrell, D. A. Protein-based materials, toward a new level of structural control. Chem. Commun. 1897-1904 (2001).
46. Zhang, S. G., Lockshin, C., Cook, R. & Rich, A. Unusually stable beta-sheet formation in an ionic self-complementary oligopeptide. Biopolymers 34, 663-672 (1994).
47. Kreplak, L., Aebi, U. & Herrmann, H. Molecular mechanisms underlying the assembly of intermediate filaments. Exp. Cell Res. 301, 77-83 (2004).
48. Strelkov, S. V., Schumacher, J., Burkhard, P., Aebi, U. & Herrmann, H. Crystal structure of the human lamin a coil 2B dimer: Implications for the head-to-tail association of nuclear lamins. J. Mol. Biol. 343, 1067-1080 (2004).
49. Schietke, R. et al. Mutations in vimentin disrupt the cytoskeleton in fibroblasts and delay execution of apoptosis. Eur. J. Cell Biol. 85, 1-10 (2006).
50. Sokolova, A. V. et al. Monitoring intermediate filament assembly by small-angle X-ray scattering reveals the molecular architecture of assembly intermediates. Proc. Natl Acad. Sci. USA 103, 16206-16211 (2006).
51. Alon, U. Simplicity in biology. Nature 446, 497 (2007).
52. Csete, M. E. & Doyle, J. C. Reverse engineering of biological complexity. Science 295, 1664-1669 (2002).
53. Ackbarow, T. & Buehler, M. J. Hierarchical coexistence of universality and diversity controls robustness and multi-functionality in protein materials Theor. Comput. Nanosci. 5, 1193-1204 (2008).
54. Ferrer, J. M. et al. Measuring molecular rupture forces between single actin filaments and actin-binding proteins. Proc. Natl Acad. Sci. USA 105, 9221-9226 (2008).
55. Ackbarow, T., Chen, X., Keten, S. & Buehler, M. J. Hierarchies, multiple energy barriers and robustness govern the fracture mechanics of alpha-helical and beta-sheet protein domains. Proc. Natl Acad. Sci. USA 104, 16410-16415 (2007).
56. Buehler, M. J., Keten, S. & Ackbarow, T. Theoretical and computational hierarchical nanomechanics of protein materials: Deformation and fracture. Prog. Mater. Sci. 53, 1101-1241 (2008).
57. Astbury, W. T. & Street, A. X-ray studies of the structures of hair, wool and related fibres. I. General. Phil. Trans. R. Soc. A 230, 75-101 (1931).
58. Mittermaier, A. & Kay, L. E. Review: New tools provide new insights in NMR studies of protein dynamics. Science 312, 224-228 (2006).
59. Gupta, H. S. et al. Synchrotron diffraction study of deformation mechanisms in mineralized tendon. Phys. Rev. Lett. 93 (2004).
60. Bernstein, F. C. et al. Protein Data Bank: Computer-based archival file for macromolecular structures. J. Mol. Biol. 112, 535-542 (1977).
61. Le Gros, M. A., McDermott, G. & Larabell, C. A. X-ray tomography of whole cells. Curr. Opin. Struct. Biol. 15, 593-600 (2005).
62. Jackson, M. & Mantsch, H. H. The use and misuse of FTIR spectroscopy in the determination of protein-structure. Crit. Rev. Biochem. Molec. Biol. 30, 95-120 (1995).
63. Haris, P. I. & Chapman, D. The conformational analysis of peptides using Fourier-transform IR spectroscopy. Biopolymers 37, 251-263 (1995).
64. Prater, C. B., Butt, H. J. & Hansma, P. K. Atomic force microscopy. Nature 345, 839-840 (1990).
65. Fisher, T. E., Oberhauser, A. F., Carrion-Vazquez, M., Marszalek, P. E. & Fernandez, J. M. The study of protein mechanics with the atomic force microscope. Trends Biochem. Sci. 24, 379-384 (1999).
66. Oberhauser, A. F., Badilla-Fernandez, C., Carrion-Vazquez, M. & Fernandez, J. M. The mechanical hierarchies of fibronectin observed with single-molecule AFM. J. Mol. Biol. 319, 433-447 (2002).
67. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J. M. & Gaub, H. E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276, 1109-1112 (1997).
68. Mostaert, A. S., Higgins, M. J., Fukuma, T., Rindi, F. & Jarvis, S. P. Nanoscale mechanical characterisation of amyloid fibrils discovered in a natural adhesive. J. Biol. Phys. 32, 393-401 (2006).
69. Marszalek, P. E. et al. Mechanical unfolding intermediates in titin modules. Nature 402, 100-103 (1999).
70. Sotomayor, M. & Schulten, K. Single-molecule experiments in vitro and in silico. Science 316, 1144-1148 (2007).
71. Lim, C. T., Dao, M., Suresh, S., Sow, C. H. & Chew, K. T. Large deformation of living cells using laser traps. Acta Mater. 52, 1837-1845 (2004).
72. Hassenkam, T. et al. High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35, 4-10 (2004).
73. Shao, Z. F., Mou, J., Czajkowsky, D. M., Yang, J. & Yuan, J. Y. Biological atomic force microscopy: What is achieved and what is needed. Adv. Phys. 45, 1-86 (1996).
74. Fisher, T. E., Marszalek, P. E. & Fernandez, J. M. Stretching single molecules into novel conformations using the atomic force microscope. Nature Struct. Biol. 7, 719-724 (2000).
75. Kadler, K. E., Holmes, D. F., Graham, H. & Starborg, T. Tip-mediated fusion involving unipolar collagen fibrils accounts for rapid fibril elongation, the occurrence of fibrillar branched networks in skin and the paucity of collagen fibril ends in vertebrates. Matrix Biol. 19, 359-365 (2000).
76. Rainey, J. K., Wen, C. K. & Goh, M. C. Hierarchical assembly and the onset of banding in fibrous long spacing collagen revealed by atomic force microscopy. Matrix Biol. 21, 647-660 (2002).
77. Fantner, G. E. et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nature Mater. 4, 612-616 (2005).
78. Johnson, C. P., Tang, H. Y., Carag, C., Speicher, D. W. & Discher, D. E. Forced unfolding of proteins within cells. Science 317, 663-666 (2007).
79. Oliver, W. C. & Pharr, G. M. Measurement of hardness and elastic modulus by instrumented indentation: Advances in understanding and refinements to methodology. J. Mater. Res. 19, 3-20 (2004).
80. Thompson, J. B. et al. Bone indentation recovery time correlates with bond reforming time. Nature 414, 773-776 (2001).
81. Tai, K., Dao, M., Suresh, S., Palazoglu, A. & Ortiz, C. Nanoscale heterogeneity promotes energy dissipation in bone. Nature Mater. 6, 454-462 (2007).
82. Eppell, S. J., Smith, B. N., Kahn, H. & Ballarini, R. Nano measurements with micro-devices: mechanical properties of hydrated collagen fibrils. J., R. Soc. Interf. 3, 117-121 (2006).
83. Karplus, M. & McCammon, J. A. Molecular dynamics simulations of biomolecules. Nature Struct. Biol. 9, 646-652 (2002).
84. Wang, W., Donini, O., Reyes, C. M. & Kollman, P. A. Biomolecular simulations: Recent developments in force fields, simulations of enzyme catalysis, protein-ligand, protein-protein, and protein-nucleic acid noncovalent interactions. Annu. Rev. Biophys. Biomol Struct. 30, 211-243 (2001).
85. Mackerell, A. D. Empirical force fields for biological macromolecules: Overview and issues. J. Comput. Chem. 25, 1584-1604 (2004).
86. Gautieri, A., Buehler, M. J. & Redaelli, A. Deformation rate controls elasticity and unfolding pathway of single tropocollagen molecules. J. Mech. Behavior Biomed. Mater. 2, 130-137 (2009).
87. Bell, G. I. Models for specific adhesion of cells to cells. Science 200, 618-627 (1978).
88. Kramers, H. A. Brownian motion in a field of force and the diffusion model of chemical reactions. Physica 7, 10 (1940).
89. Hanggi, P., Talkner, P. & Borkovec, M. Reaction-rate theory: fifty years after Kramers. Rev. Mod. Phys. 62, 251-341 (1990).
90. Zhurkov, S. N. Kinetic concept of the strength of solids. Int. J. Fracture Mech. 1, 311-323 (1965).
91. Evans, E. Probing the relation between force, lifetime, and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30, 105-128 (2001).
92. Merkel, R., Nassoy, P., Leung, A., Ritchie, K. & Evans, E. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 379, 50-53 (1999).
93. Evans, E. & Ritchie, K. Dynamic strength of molecular adhesion bonds. Biophys. J. 72, 1541-1555 (1997).
94. Dudko, O. K., Hummer, G. & Szabo, A. Intrinsic rates and activation free energies from single-molecule pulling experiments. Phys. Rev. Lett. 96 (2006).
95. Hummer, G. & Szabo, A. Kinetics from nonequilibrium single-molecule pulling experiments. Biophys. J. 85, 5-15 (2003).
96. Hummer, G. & Szabo, A. Free energy reconstruction from nonequilibrium single-molecule pulling experiments. Proc. Natl Acad. Sci. USA 98, 3658-3661 (2001).
97. Snow, C. D., Sorin, E. J., Rhee, Y. M. & Pande, V. S. How well can simulation predict protein folding kinetics and thermodynamics? Annu. Rev. Biophys. Biomol. Struct. 34, 43-69 (2005).
98. Dietz, H. & Rief, M. Elastic bond network model for protein unfolding mechanics. Phys. Rev. Lett. 100, 098101 (2008).
99. Seifert, U. Rupture of multiple parallel molecular bonds under dynamic loading. Phys. Rev. Lett. 84, 2750-2753 (2000).
100. Erdmann, T. & Schwarz, U. S. Stability of adhesion clusters under constant force. Phys. Rev. Lett. 92, 4 (2004).
101. Dietz, H., Berkemeier, F., Bertz, M. & Rief, M. Anisotropic deformation response of single protein molecules. Proc. Natl Acad. Sci. USA 103, 12724-12728 (2006).
102. Bustamante, C., Marko, J. F., Siggia, E. D. & Smith, S. Entropic elasticity of lambda-phage DNA. Science 265, 1599-1600 (1994).
103. Sun, Y. L., Luo, Z. P., Fertala, A. & An, K. N. Stretching type II collagen with optical tweezers. J. Biomech. 37, 1665-1669 (2004).
104. Rief, M., Fernandez, J. M. & Gaub, H. E. Elastically coupled two-level systems as a model for biopolymer extensibility. Phys. Rev. Lett. 81, 4764-4767 (1998).
105. Keten, S. & Buehler, M. J. Strength limit of entropic elasticity in beta-sheet protein domains. Phys. Rev. E 78, 061913 (2008).
106. Mesquida, P., Riener, C. K., MacPhee, C. E. & McKendry, R. A. Morphology and mechanical stability of amyloid-like peptide fibrils. J. Mater. Sci. Mater. Med. 18, 1325-1331 (2007).
107. Iconomidou, V. A. & Hamodrakas, S. J. Natural protective amyloids. Curr. Protein Pept. Sci. 9, 291-309 (2008).
108. Hardy, J. & Selkoe, D. J. Medicine: The amyloid hypothesis of Alzheimer's disease. Progress and problems on the road to therapeutics. Science 297, 353-356 (2002).
109. Selkoe, D. J. Alzheimer's disease: Genes, proteins, and therapy. Physiol. Rev. 81, 741-766 (2001).
110. Knowles, T. P. et al. Role of intermolecular forces in defining material properties of protein nanofibrils. Science 318, 1900-1903 (2007).
111. Smith, J. F., Knowles, T. P. J., Dobson, C. M., MacPhee, C. E. & Welland, M. E. Characterization of the nanoscale properties of individual amyloid fibrils. Proc. Natl Acad. Sci. USA 103, 15806-15811 (2006).
112. Dutt, A., Drew, M. G. B. & Pramanik, A. Beta-sheet mediated self-assembly of dipeptides of Omega-amino acids and remarkable fibrillation in the solid state. Org. Biomol. Chem. 3, 2250 (2005).
113. Burkoth, T. S. et al. Structure of the beta-amyloid((10-35)) fibril. J. Am. Chem. Soc. 122, 7883-7889 (2000).
114. Chiti, F. & Dobson, C. M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366 (2006).
115. Dobson, C. M. Protein folding and misfolding. Nature 426, 884-890 (2003).
116. Nguyen, H. D. & Hall, C. K. Molecular dynamics simulations of spontaneous fibril formation by random-coil peptides. Proc. Natl Acad. Sci. USA 101, 16180 (2004).
117. Hwang, W., Zhang, S. G., Kamm, R. D. & Karplus, M. Kinetic control of dimer structure formation in amyloid fibrillogenesis. Proc. Natl Acad. Sci. USA 101, 12916-12921 (2004).
118. Gruenbaum, Y., Margalit, A., Goldman, R. D., Shumaker, D. K. & Wilson, K. L. The nuclear lamina comes of age. Nature Rev. Mol. Cell Biol. 6, 21-31 (2005).
119. Burke, B. & Stewart, C. L. Life at the edge: The nuclear envelope and human disease. Nature Rev. Mol. Cell Biol. 3, 575-585 (2002).
120. Lammerding, J. et al. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Invest. 113, 370-378 (2004).
121. Prockop, D. J. & Kivirikko, K. I. Collagens: molecular biology, diseases, and potentials for therapy. Annu. Rev. Biochem. 64, 403-434 (1995).
122. Byers, P. H., Wallis, G. A. & Willing, M. C. Osteogenesis imperfecta: translation of mutation to phenotype. J. Med. Genet. 28, 433-442 (1991).
123. Gautieri, A., Vesentini, S., Redaelli, A. & Buehler, M. J. Single molecule effects of osteogenesis imperfecta mutations in tropocollagen protein domains. Protein Sci. 18, 161-168 (2009).
124. McBride, D. J., Choe, V., Shapiro, J. R. & Brodsky, B. Altered collagen structure in mouse tail tendon lacking the α2(I) chain. J. Mol. Biol. 270, 275-284 (1997).
125. Miller, A., Delos, D., Baldini, T., Wright, T. M. & Camacho, N. P. Abnormal mineral-matrix interactions are a significant contributor to fragility in oim/oim bone. Calcif. Tissue Int. 81, 206-214 (2007).
126. Sims, T. J., Miles, C. A., Bailey, A. J. & Camacho, N. P. Properties of collagen in OIM mouse tissues. Connect. Tissue Res. 44, 202-205 (2003).
127. Grabner, B. et al. Age- and genotype-dependence of bone material properties in the osteogenesis imperfecta murine model (oim). Bone 29, 453-457 (2001).
128. Camacho, N. P. et al. The material basis for reduced mechanical properties in oim bones. J. Bone Mineral. Res. 14, 264-272 (1999).
129. Fratzl, P., Paris, O., Klaushofer, K. & Landis, W. J. Bone mineralization in an osteogenesis imperfecta mouse model studied by small-angle X-ray scattering. J. Clin. Invest. 97, 396-402 (1996).
130. Rauch, F. & Glorieux, F. H. Osteogenesis imperfecta. Lancet 363, 1377-1385 (2004).
131. Miller, E., Delos, D., Baldini, T., Wright, T. M. & Camacho, N. P. Abnormal mineral-matrix interactions are a significant contributor to fragility in oim/oim bone. Calcif. Tissue Int. 81, 206-214 (2007).
132. Misof, K., Landis, W. J., Klaushofer, K. & Fratzl, P. Collagen from the osteogenesis imperfecta mouse model (oim) shows reduced resistance against tensile stress. J. Clin. Invest. 100, 40-45 (1997).
133. Chavassieux, P., Seeman, E. & Delmas, P. D. Insights into material and structural basis of bone fragility from diseases associated with fractures: How determinants of the biomechanical properties of bone are compromised by disease. Endocrine Rev. 28, 151-164 (2007).
134. Hudson, B. G., Tryggvason, K., Sundaramoorthy, M. & Neilson, E. G. Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N. Engl. J. Med. 348, 2543-2556 (2003).
135. Guck, J. et al. Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys. J. 88, 3689-3698 (2005).
136. Cross, S. E., Jin, Y.-S., Rao, J. & Gimzewski, J. K. Nanomechanical analysis of cells from cancer patients. Nature Nanotech. 2, 780-783 (2007).
137. Dao, M., Lim, C. T. & Suresh, S. Mechanics of the human red blood cell deformed by optical tweezers. J. Mech. Phys. Solids 51, 2259-2280 (2003).
138. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
139. Scheibel, T. et al. Conducting nanowires built by controlled self-assembly of amyloid fibers and selective metal deposition. Proc. Natl Acad. Sci. USA 100, 4527-4532 (2003).
140. Humphrey, W., Dalke, A. & Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graphics 14, 33 (1996).
141. Herrmann, H., Bar, H., Kreplak, L., Strelkov, S. V. & Aebi, U. Intermediate filaments: from cell architecture to nanomechanics. Nature Rev. Mol. Cell Biol. 8, 562-573 (2007).
142. Lantz, M. A. et al. Stretching the alpha-helix: a direct measure of the hydrogen-bond energy of a single-peptide molecule. Chem. Phys. Lett. 315, 61-68 (1999).
143. 143.www.nature.com/horizon/proteinfolding/highlights/figures/ s3-nonspecl-fl.html.