Understanding the influence of structural hierarchy and its coupling with chemical environment on the strength of idealized tropocollagen-hydroxyapatite biomaterials

Journal of the Mechanics and Physics of Solids

Volumn 57, Issue 10, 2009, Pages 1702-1717

  Dubey, Devendra K ^a   Tomar, Vikas ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Biological material; Chemo mechanical processes; Constitutive behavior; Molecular simulations; Strengthening and mechanisms

Indexed keywords

CALCIUM IONS; CHEMICAL ENVIRONMENT; CHEMO-MECHANICAL PROCESSES; COMPOSITE SYSTEMS; COMPUTATIONAL TIME; CONSTITUTIVE BEHAVIOR; CONTACT AREAS; FRACTURE STRENGTHS; HAP CRYSTAL; INTERFACIAL INTERACTION; INTERFACIAL STRENGTH; LENGTH SCALE; MATERIAL SYSTEMS; MECHANICAL STRENGTH; MINERAL PHASE; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR SIMULATIONS; MULTISCALING; ORGANIC PHASE; PEAK STRENGTH; PEAK STRESS; PRESENCE OF WATER; STAGGERED ARRANGEMENT; STRENGTHENING AND MECHANISMS; STRUCTURAL ARRANGEMENT; STRUCTURAL EFFECT; STRUCTURAL HIERARCHIES; TENSILE LOADING; WATER MOLECULE; YOUNG'S MODULUS;

APATITE; BIOMATERIALS; BOUNDARY LAYER FLOW; CALCIUM; CARBONATE MINERALS; CRYSTAL ORIENTATION; DEFORMATION; FRACTURE; HAZARDOUS MATERIALS; HYDRATES; HYDRATION; HYDROXYAPATITE; MECHANISMS; MINERALS; MINING; MOLECULAR DYNAMICS; MOLECULAR STRUCTURE; MOLECULES; SILICATE MINERALS; STRENGTHENING (METAL); STRESS ANALYSIS; THREE DIMENSIONAL;

BIOLOGICAL MATERIALS;

EID: 68949194432     PISSN: 00225096     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmps.2009.07.002     Document Type: Article

References (67)

1. Anderson, D., 2005. Collagen self-assembly: A complementary experimental and theoretical perspective, Ph.D. Dissertation, University of Toronto.
2. Bella J., Eaton M., Brodsky B., and Berman H.M. Crystal and molecular structure of a collagen-like peptide at 1.9 angstrom resolution. Science 266 (1994) 75-81
3. Bembey A.K., Bushby A.J., Boyde A., Ferguson V.L., and Oyen M.L. Hydration effects on the micro-mechanical properties of bone. Journal of Materials Research 21 8 (2006) 1962-1968
4. Berg R.A., and Prockop D.J. The thermal transition of a non-hydroxylated form of collagen. Evidence for a role for hydroxyproline in stabilizing the triple-helix of collagen. Biochemical and Biophysical Research Communications 52 1 (1973) 115-120
5. Berryman J.G. Bounds and self-consistent estimates for elastic constants of random polycrystals with hexagonal, trigonal, and tetragonal symmetries. Journal of the Mechanics and Physics of Solids 53 10 (2005) 2141-2173
6. Bhowmik R., Katti K.S., and Katti D. Molecular dynamics simulation of hydroxyapatite-polyacrylic acid interface. Polymer 48 (2007) 664-674
7. Bhowmik, R., Katti, K.S., Katti, D.R., 2007b. Investigating the interfacial interactions between organic and inorganic phases and their influence on the mechanics of organic phase in natural bone, Materials Research Society Symposia Proceedings 975, Paper # 0975-DD02-05.
8. Bhowmik R., Katti K.S., Verma D., and Katti D.R. Probing molecular interactions in bone biomaterials: through molecular dynamics and Fourier transform infrared spectroscopy. Materials Science and Engineering 27 (2007) 352-371
9. Broedling N.C., Hartmaier A., Buehler M., and Gao H. The strength limit in a bio-inspired metallic nanocomposite. Journal of the Mechanics and Physics of Solids 56 (2008) 1086-1104
10. Buehler M.J. Atomistic and continuum modeling of mechanical properties of collagen: Elasticity, fracture, and self-assembly. Journal of Materials Research 21 8 (2006) 1947-1962
11. 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 103 33 (2006) 12285-12290
12. Buehler M.J. Molecular nanomechanics of nascent bone: fibrillar toughening by mineralization. Nanotechnology 18 (2007) 295102-295110
13. Buehler M.J. Nanomechanics of collagen fibrils under varying cross-link densities: Atomistic and continuum studies. Journal of the Mechanical Behavior of Biomedical Materials 1 (2008) 59-67
14. Chen J., Li L., Yu T., Long H., Weidner D., Wang L., and Vaughan M. Do Reuss and Voigt bounds really bound in high-pressure rheology experiments. Journal of Physics C: Condensed Matter 18 (2006) S1049-S1059
15. Chen P.-Y., Lin A.Y.M., Lin Y.S., Seki Y., Stokes A.G., Peyras J., Olevsky E.A., Meyers M.A., and McKittrick J. Structure and mechanical properties of selected biological materials. Journal of the Mechanical Behavior of Biomedical Materials 1 (2008) 208-226
16. Cusack S., and Miller A. Determination of the elastic-constants of collagen by Brillouin light-scattering. Journal of Molecular Biology 135 1 (1979) 39-51
17. Elliott J.C., Mackie P.E., and Young R.A. Monoclinic hydroxyapatite. Science 180 (1973) 1055-1057
18. Eppell S.J., Smith B.N., Kahn H., and Ballarini R. Nano measurements with micro-devices: mechanical properties of hydrated collagen fibrils. Journal of the Royal Society Interface 3 (2005) 117-121
19. Fantner G.E., Hassenkam T., Kindt J.H., Weaver J.C., Birkedal H., Pechenik L., Cutroni J.A., Cidade G.A.G., Stucky G.D., Morse D.E., and Hansma P.K. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nature Materials 4 8 (2005) 612-616
20. Fratzl P., Fratzlzelman N., Klaushofer K., Vogl G., and Koller K. Nucleation and growth of mineral crystals in bone studied by small-angle X-ray scattering. Calcified Tissue International 48 6 (1991) 407-413
21. Fratzl P., and Weinkamer R. Nature's hierarchical materials. Progress in Materials Science 52 (2007) 1263-1334
22. Gao H. Application of fracture mechanics concepts to hierarchical biomechanics of bone and bone-like materials. International Journal of Fracture 138 (2006) 101-137
23. Ghosh P., Katti D.R., and Katti K.S. Mineral proximity influences mechanical response of proteins in biological mineral-protein hybrid systems. Biomacromolecules 8 3 (2007) 851-856
24. Gupta H.S., Wagermaier W., Zickler G.A., Aroush D.R.-B., Funari S.r.S., Roschger P., Wagner H.D., and Fratzl P. Nanoscale deformation mechanisms in bone. Nano Letters 5 10 (2005) 2108-2111
25. Handgraaf J.W., and Zerbetto F. Molecular dynamics study of onset of water gelation around the collagen triple helix. Proteins: Structure, Function, and Bioinformatics 64 3 (2006) 711-718
26. Harley R., James D., Miller A., and White J.W. Phonons and elastic-moduli of collagen and muscle. Nature 267 5608 (1977) 285-287
27. Hauptmann S., Dufner H., Brickmann J., Kast S.M., and Berry R.S. Potential energy function for apatites. Physical Chemistry Chemical Physics 5 3 (2003) 635-639
28. Hein J., Reid F., Smith L., Bush I., Guest M., and Sherwood P. On the performance of molecular dynamics applications on current high-end systems. Philosophical Transactions of the Royal Society 363 (2005) 1987-1998
29. Hodge, A.J., Petruska, J.A., 1963. Recent studies with the electron microscope on ordered aggregates of the tropocollagen macromolecule. In: Ramachandran, G.N. (Ed.), Aspects of Protein Structure. Proceedings of a Symposium, pp. 289-300.
30. Hofmann H., Voss T., Kuhn K., and Engel J. Localization of flexible sites in thread-like molecules from electron-micrographs-comparison of interstitial, basement-membrane and intima collagens. Journal of Molecular Biology 172 3 (1984) 325-343
31. Holmgren S.K., Taylor K.M., Bretscher L.E., and Raines R.T. Code for collagen's stability deciphered. Nature 392 6677 (1998) 666-667
32. Huang, C.C., Couch, G.S., Pettersen, E.F., Ferrin, T.E., 1998. The object technology framework (OTF): an object-oriented interface to molecular data and its application to collagen. In: Pacific Symposium on Biocomputing, pp. 349-360.
33. Israelowitz M., Rizvi S.H.W., Kramer J., and Schroeder H.P.v. Computational modeling of type I collagen fibers to determine the extracellular matrix structure of connective tissues. Protein Engineering Design and Selection 18 7 (2005) 329-335
34. Jager I., and Fratzl P. Mineralized collagen fibrils: A mechanical model with a staggered arrangement of mineral particles. Biophysical Journal 79 4 (2000) 1737-1746
35. Jenkins C.L., Bretscher L.E., Guzei I.A., and Raines R.T. Effect of 3-hydroxyproline residues on collagen stability. Journal of the American Chemical Society 125 21 (2003) 6422-6427
36. Ji B., and Gao H. Mechanical properties of nanostructure of biological materials. Journal of the Mechanics and Physics of Solids 52 (2004) 1963-2000
37. Ji B.H. A study of the interface strength between protein and mineral in biological materials. Journal of Biomechanics 41 2 (2008) 259-266
38. Jorgensen W.L., Chandrasekhar J., Madura J.D., Impey R.W., and Klein M.L. Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics 79 2 (1983) 926-935
39. Keaveny T.M., Morgan E.F., Niebur G.L., and Yeh O.C. Biomechanics of Trabecular Bone. Annual Review of Biomedical Engineering 3 (2001) 307-333
40. Klein T.E., and Huang C.C. Computational investigations of structural changes resulting from point mutations in a collagen-like peptide. Biopolymers 49 2 (1999) 167-183
41. Kramer R.Z., Venugopal M.G., Bella J., Mayville P., Brodsky B., and Berman H.M. "Staggered molecular packing in crystals of a collagen-like peptide with a single charged pair. Journal of Molecular Biology 301 5 (2000) 1191-1205
42. Landis W.J., Hodgens K.J., Arena J., Song M.J., and McEwen B.F. Structural relations between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microscopy Research and Technique 33 2 (1996) 192-202
43. Landis W.J., Hodgens K.J., Song M.J., Arena J., Kiyonaga S., Marko M., Owen C., and Mcewen B.F. Mineralization of collagen may occur on fibril surfaces: evidence from conventional and high-voltage electron microscopy and three-dimensional imaging. Journal of Structural Biology 117 (1996) 24-35
44. Lorenzo A.C., and Caffarena E.R.l. Elastic properties, Young's modulus determination and structural stability of the tropocollagen molecule: a computational study by steered molecular dynamics. Journal of Biomechanics 38 (2005) 1527-1533
45. Lucksanasombool P., Higgs W.A.J., Higgs R., and Swain M.V. Fracture toughness of bovine bone: influence of orientation and storage media. Biomaterials 22 23 (2001) 3127-3132
46. MacKerell A.D., Bashford D., Bellott M., Dunbrack R.L., Evanseck J.D., Field M.J., Fischer S., Gao J., Guo H., Ha S., Joseph-McCarthy D., Kuchnir L., Kuczera K., Lau F.T.K., Mattos C., Michnick S., Ngo T., Nguyen D.T., Prodhom B., Reiher W.E., Roux B., Schlenkrich M., Smith J.C., Stote R., Straub J., Watanabe M., Wiorkiewicz-Kuczera J., Yin D., and Karplus M. All-atom empirical potential for molecular modeling and dynamics studies of proteins. Journal of Physical Chemistry B 102 18 (1998) 3586-3616
47. Makarov V., Pettitt B.M., and Feig M. Solvation and hydration of proteins and nucleic acids: a theoretical view of simulations and experiment. Accounts of Chemical Research 35 (2002) 376-384
48. Meyers M.A., Chen P.-Y., Lin A.Y., and Seki Y. Biological materials: structure and mechanical properties. Progress in Materials Science 53 (2008) 1-206
49. Orgel J., Irving T.C., Miller A., and Wess T.J. Microfibrillar structure of type I collagen in situ. Proceedings of the National Academy of Sciences of the United States of America 103 24 (2006) 9001-9005
50. Park S., Radmer R.J., Klein T.E., and Pande V.S. A new set of molecular mechanics parameters for hydroxyproline and its use in molecular dynamics simulations of collagen-like peptides. Journal of Computational Chemistry 26 15 (2005) 1612-1616
51. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., Chipot C., and Skeel R.D. Scalable molecular dynamics with NAMD. Journal of Computational Chemistry 26 (2005) 1781-1802
52. Ponder J.W., and Case D.A. Force fields for protein simulations. Protein Simulations vol. 66 (2003), Academic Press Inc., San Diego 27-+
53. Posner A.S., and Beebe R.A. The surface chemistry of bone mineral and related calcium phosphates. Seminars in Arthritis and Rheumatism 4 3 (1975) 267-291
54. Radmer R.J., and Klein T.E. Triple helical structure and stabilization of collagen-like molecules with 4(R)-hydroxyproline in the Xaa position. Biophysical Journal 90 (2006) 578-588
55. Rubin M.A., Jasiuk L., Taylor J., Rubin J., Ganey T., and Apkarian R.P. TEM analysis of the nanostructure of normal and osteoporotic human trabecular bone. Bone 33 3 (2003) 270-282
56. Sasaki N., and Odajima S. Elongation mechanism of collagen fibrils and force-strain relations of tendon at each level of structural hierarchy. Journal of Biomechanics 29 9 (1996) 1131-1136
57. Sasaki N., and Odajima S. Stress-strain curve and Young's modulus of a collagen molecule as determined by the X-ray diffraction technique. Journal of Biomechanics 29 5 (1996) 655-658
58. Simone A.D., Vitaglaino L., and Berisio R. Role of hydration in collagen triple helix stabilization. Biochemical and Biophysical Research Communications 372 (2008) 121-125
59. Sun Y.L., Luo Z.P., Fertala A., and An K.N. Stretching type II collagen with optical tweezers. Journal of Biomechanics 37 11 (2004) 1665-1669
60. Thompson J.B., Kindt J.H., Drake B., Hansma H.G., Morse D.E., and Hansma P.K. Bone indentation recovery time correlates with bond reforming time. Nature 414 6865 (2001) 773-776
61. Thurner P.J., Erickson B., Jungmann R., Schriock Z., Weaver J.C., Fantner G.E., Schitter G., Morse D.E., and Hansma P.K. High-speed photography of compressed human trabecular bone correlates whitening to microscopic damage. Engineering Fracture Mechanics 74 12 (2007) 1928-1941
62. Tomar V., and Zhou M. Analyses of tensile deformation of nanocrystalline α-Fe2O3+fcc-Al composites using classical molecular dynamics. Journal of the Mechanics and Physics of Solids 55 (2007) 1053-1085
63. Vesentini S., Fitie C.F.C., Montevecchi F.M., and Redaelli A. Molecular assessment of the elastic properties of collagen-like homotrimer sequences. Biomechanics and Modeling in Mechanobiology 3 4 (2005) 224-234
64. Voth G.A. Computer simulation of proton solvation and transport in aqueous and biomolecular systems. Accounts of Chemical Research 39 2 (2006) 143-150
65. Weiner S., Talmon Y., and Traub W. Electron diffraction of mollusc shell organic matrices and their relationship to the mineral phase. International Journal of Biological Macromolecules 5 6 (1983) 325-328
66. Weiner S., and Wagner H.D. The material bone: structure mechanical function relations. Annual Review of Materials Science 28 (1998) 271-298
67. Zhang D., Chippada U., and Jordan K. Effect of the structural water on the mechanical properties of collagen-like microfibrils: a molecular dynamics study. Annals of Biomedical Engineering 35 (2007) 1216-1230