The nanometre-scale physiology of bone: Steric modelling and scanning transmission electron microscopy of collagen-mineral structure

Journal of the Royal Society Interface

Volumn 9, Issue 73, 2012, Pages 1774-1786

  Alexander, Benjamin ^a   Daulton, Tyrone L ^b   Genin, Guy M ^a,b   Lipner, Justin ^a,c   Pasteris, Jill D ^b   Wopenka, Brigitte ^b   Thomopoulos, Stavros ^a,b,c  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bioapatite; Elemental mapping; Mineralized collagen fibril; Scanning transmission electron microscopy electron energy loss spectroscopy imaging; Scanning transmission electron microscopy high angle annular dark field imaging

Indexed keywords

BONE; ELECTRON ENERGY LOSS SPECTROSCOPY; ELECTRON SCATTERING; MOLECULES; PHOSPHATE MINERALS; TISSUE; TRANSMISSION ELECTRON MICROSCOPY;

BIO-APATITE; COLLAGEN FIBRILS; COLLAGEN MOLECULES; ELEMENTAL MAPPING; GAP CHANNELS; HIGH-ANGLE ANNULAR DARK-FIELD IMAGING; INTERMOLECULAR SPACE; MINERALIZED COLLAGEN; NANOSTRUCTURAL; NUCLEATION AND GROWTH; OVERLAP REGION; PACKING DENSITY; SCANNING TRANSMISSION ELECTRON MICROSCOPY; STRENGTH AND TOUGHNESS; TRANSMISSION ELECTRON;

COLLAGEN;

APATITE; COLLAGEN FIBRIL; HYDROXYAPATITE; MINERAL; NANOMATERIAL;

ANIMAL TISSUE; ARTICLE; BONE NANOMETER SCALE PHYSIOLOGY; CHEMICAL STRUCTURE; ELECTRON ENERGY LOSS SPECTROSCOPY; MODEL; MOUSE; MUSCULOSKELETAL FUNCTION; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; PROTEIN STRUCTURE; SCANNING TRANSMISSION ELECTRON MICROSCOPY;

EID: 84865089250     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2011.0880     Document Type: Article

References (64)

1. Glimcher, M. J. 2006 Bone: nature of the calcium phosphate crystals and cellular, structural, and physical chemical mechanisms in their formation. Rev. Mineral. Geochem. 64, 223-282. (doi:10.2138/rmg.2006.64.8)
2. Hollister, D. W. 1987 Molecular basis of osteogenesis imperfecta. Curr. Probl. Dermatol. 17, 76-94.
3. Boskey, A. 2001 Bone mineralization. In Bone mechanics handbook, 2nd edn. (ed. S. C. Cowin), p. 5:1-33. Boca Raton, FL: CRC Press.
4. Hodge, A. J. & Petruska, J. A. 1963 In Aspects of protein structure (ed. G. N. Ramachandran), pp. 289-300. New York, NY: Academic Press.
5. Landis, W. J., Moradian-Oldak, J. & Weiner, S. 1991 Topographic imaging of mineral and collagen in the calcifying turkey tendon. Connect. Tissue Res. 25, 181-196. (doi:10.3109/03008209109029155)
6. Orgel, J. P. R. O., Miller, A., Irving, T. C., Fischetti, R. F., Hammersley, A. P. & Wess, T. J. 2001 The in situ supermolecular structure of type I collagen. Structure 9, 1061-1069. (doi:10.1016/S0969-2126(01)00669-4)
7. Orgel, J. P. R. O., Irving, T. C., Miller, A. & Wess, T. J. 2006 Microfibrillar structure of type I collagen in situ. Proc. Natl Acad. Sci. USA 103, 9001-9005. (doi:10.1073/pnas.0502718103)
8. Landis, W. J., Song, M. J., Leith, A., McEwen, L. & McEwen, B. F. 1993 Mineral and organic matrix interaction in normally calcifying tendon visualized in three dimensions by high-voltage electron microscopic tomography and graphic image reconstruction. J. Struct. Biol. 110, 39-54. (doi:10.1006/jsbi.1993.1003)
9. Hodge, A. J. 1967 Structure at the electron microscopic level. In Treatise on collagen (ed. G. Ramachandran), pp. 185-205. New York, NY: Academic Press.
10. Hodge, A. J. 1989 Molecular models illustrating the possible distributions of 'holes' in simple systematically staggered arrays of type I collagen molecules in nativetype fibrils. Connect. Tissue Res. 21, 137-147. (doi:10.3109/03008208909050004)
11. Katz, E. P. & Li, S. T. 1973 Structure and function of bone collagen fibrils. J. Mol. Biol. 80, 1-15. (doi:10.1016/0022-2836(73)90230-1)
12. Olszta, M. J., Cheng, X., Jee, S. S., Kumar, R., Kim, Y. Y., Kaufman, M. J., Douglas, E. P. & Gower, L. B. 2007 Bone structure and formation: a new perspective. Mater. Sci. Eng. R-Rep. 58, 77-116. (doi:10.1016/j.mser.2007.05. 001)
13. Landis, W. J., Hauschka, B. T., Rogerson, C. A. & Glimcher, M. J. 1977 Electron microscopic observations of bone tissue prepared by ultracryomicrotomy. J. Ultrastruct. Res. 59, 185-206. (doi:10.1016/S0022- 5320(77)80079-8)
14. Lee, D. D.&Glimcher, M. J. 1991 Three-dimensional spatial relationship between the collagen fibrils and the inorganic calcium phosphate crystals of pickerel (Americanus americanus) and herring (Clupea harengus) bone. J. Mol. Biol. 217, 487-501. (doi:10.1016/0022-2836 (91)90752-R)
15. Glimcher, M. J. 1959 Molecular biology of mineralized tissues with particular reference to bone. Rev. Mod. Phys. 31, 359-393. (doi:10.1103/ RevModPhys.31.359)
16. Glimcher, M. J. 1968 A basic architectural principle in the organization of mineralized tissues. In Proc 5th European Symp. Calcif Tiss (ed. G. Milhaud, M. Owen & H. J. J. Blackwood), pp. 3-26. Paris: Societe d'Edition d'Enseignement Superieur.
17. White, S. W., Hulmes, D. J. S., Miller, A. & Timmins, P. A. 1977 Collagen-mineral axial relationship in calcified turkey leg tendon by X-ray and neutron diffraction. Nature 266, 421-425. (doi:10.1038/266421a0)
18. Miller, A. 1984 Collagen: the organic matrix in bone. In Mineral phases in biology (ed. A. Miller, D. Phillips & R. J. P.Williams), pp. 45-68. London, UK: Royal Society.
19. Berthet-Colominas, C., Miller, A. & White, S. W. 1979 Structural study of the calcifying collagen in turkey leg tendons. J. Mol. Biol. 134, 431-445. (doi:10.1016/0022-2836(79)90362-0)
20. Bonar, L. C., Lees, S. & Mook, H. A. 1985 Neutron diffraction studies of collagen in fully mineralized bone. J. Mol. Biol. 181, 265-270. (doi:10.1016/0022-2836(85)90090-7)
21. Fraser, R. D. B., MacRae, T. P., Miller, A. & Suzuki, E. 1983 Molecular conformation and packing in collagen fibrils. J. Mol. Biol. 167, 497-521. (doi:10.1016/S0022-2836(83)80347-7)
22. Berthet-Colominas, C., Miller, A., Herbage, D., Ronziere, M. C. & Tocchetti, D. 1982 Structural studies of collagen fibers from intervertebral disk. Biochim. Biophys. Acta 706, 50-64. (doi:10.1016/0167-4838(82)90374-0)
23. Landis, W. J., Hodgens, K. J., Song, M. J., Arena, J., Kiyonaga, S., Marko, M., Owen, C. & McEwen, B. F. 1996 Mineralization of collagen may occur on fibril surfaces: evidence from conventional and high-voltage electron microscopy and three-dimensional imaging. J. Struct. Biol. 117, 24-35. (doi:10.1006/jsbi.1996.0066)
24. Landis, W. J. & Song, M. J. 1991 Early mineral deposition in calcifying tendon characterized by high voltage electron microscopy and 3-dimensional graphic imaging. J. Struct. Biol. 107, 116-127. (doi:10.1016/1047-8477 (91)90015-O)
25. Jantou-Morris, V., Horton, M. A. & McComb, D. W. 2010 The nano-morphological relationships between apatite crystals and collagen fibrils in ivory dentine. Biomaterials 31, 5275-5286. (doi:10.1016/j.biomaterials.2010. 03.025)
26. Lees, S. & Prostak, K. 1988 The locus of mineral crystallites in bone. Connect. Tissue Res. 18, 41-54. (doi:10.3109/03008208809019071)
27. Lees, S., Prostak, K. S., Ingle, V. K. & Kjoller, K. 1994 The loci of mineral in turkey leg tendon as seen by atomic force microscope and electron microscopy. Calcif. Tissue Int. 55, 180-189. (doi:10.1007/BF00425873)
28. Hassenkam, T., Fantner, G. E., Cutroni, J. A., Weaver, J. C., Morse, D. E. & Hansma, P. K. 2004 High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35, 4-10. (doi:10.1016/j.bone.2004.02.024)
29. Sasaki, N., Tagami, A., Goto, T., Taniguchi, M., Nakata, M. & Hikichi, K. 2002 Atomic force microscopic studies on the structure of bovine femoral cortical bone at the collagen fibril-mineral level. J. Mater. Sci. Mater. Med. 13, 333-337. (doi:10.1023/A:1014079421895)
30. Pidaparti, R. M. V., Chandran, A., Takano, Y. & Turner, C. H. 1996 Bone mineral lies mainly outside collagen fibrils: predictions of a composite model for osteonal bone. J. Biomech. 29, 909-916. (doi:10.1016/0021-9290(95) 00147-6)
31. Alexander, B.E., Daulton, T.L., Genin, G.M., Pasteris, J.D., Wopenka, B. & Thomopoulos, S. 2009 The nano-physiology of mineralized tissues. In Proc. of the ASME 2009 Summer Bioengineering Conf. (SBC2009), p.175. New York, NY: American Society of Mechanical Engineer.
32. Egerton, R. F. 1996 Electron energy-loss spectroscopy in the electron microscope. New York, NY: Plenum.
33. 3X (X= F, OH, Cl) system. Am. Mineral. 75, 295-304.
34. McConnell, D. 1973 Apatite: its crystal chemistry, mineralogy, utilization, and geologic and biologic occurrences. New York, NY: Springer.
35. Nriagu, J. O. & Moore, P. B. 1984 Phosphate minerals. New York, NY: Springer.
36. 3(F, OH, Cl). In Phosphates: geochemical, geobiological and material importance reviews in mineralogy and geochemistry (eds M. J. Kohn, J. Rakovan & J. M. Hughes), pp. 1-12. Washington, DC: Mineralogical Society of America.
37. Pan, Y. & Fleet, M. E. 2002 Compositions of the apatite-group minerals: Substitution mechanisms and controlling factors. In Phosphates: geochemical, geobiological and material importance reviews in mineralogy and geochemistry (eds D. H. Kohn, J. Rakovan & J. M. Hughes), pp. 13-50. Washington, DC: Mineralogical Society of America.
38. Cazalbou, S., Combes, C., Eichert, D. & Rey, C. 2004 Adaptative physico-chemistry of bio-related calcium phosphates. J. Mater. Chem. 14, 2148-2153. (doi:0.1039/B401318b)
39. Eppell, S. J., Tong, W., Katz, J. L., Kuhn, L. & Glimcher, M. J. 2001 Shape and size of isolated bone mineralites measured using atomic force microscopy. J. Orthop. Res. 19, 1027-1034. (doi:10.1016/S0736-0266(01)00034-1)
40. Tong, W., Glimcher, M. J., Katz, J. L., Kuhn, L. & Eppell, S. J. 2003 Size and shape of mineralites in young bovine bone measured by atomic force microscopy. Calcif. Tissue Int. 72, 592-598. (doi:10.1007/s00223-002-1077-7)
41. Derwin, K. A. & Soslowsky, L. J. 1999 A quantitative investigation of structure-function relationships in a tendon fascicle model. J. Biomech. Eng. 121, 598-604. (doi:10.1115/1.2800859)
42. Fratzl, P., Fratzl-Zelman, N. & Klaushofer, K. 1993 Collagen packing and mineralization. An x-ray scattering investigation of turkey leg tendon. Biophys. J. 64, 260-266. (doi:10.1016/S0006-3495(93)81362-6)
43. Arsenault, A. L. 1989 A comparative electron microscopic study of apatite crystals in collagen fibrils of rat bone, dentin and calcified turkey leg tendons. Bone Mineral 6, 165-177. (doi:10.1016/0169-6009(89)90048-2)
44. Maitland, M. E. & Arsenault, A. L. 1991 A correlation between the distribution of biological apatite and amino acid sequence of type I collagen. Calcif. Tissue Int. 48, 341-352. (doi:10.1007/BF02556154)
45. Ortolani, F. & Marchini, M. 1995 Cartilage type II collagen fibrils show distinctive negative-staining band patterns differences between type II and type I unfixed or glutaraldehyde-fixed collagen fibrils. J. Electron Microsc. 44, 365-375.
46. Schmitt, F. O. & Gross, J. 1948 Further progress in the electron microscopy of collagen. J. Am. Leather Chem. Assoc. 43, 658-675.
47. Shinagawa, Y. & Shinagawa, Y. 1974 Studies on collagen fibrils in amphibian skin by means of thin sectioning and densitometric method. J. ElectronMicrosc. 23, 161-165.
48. Kobayashi, K., Ito, T. & Hoshino, T. 1986 Correlation between negative staining pattern and hydrophobic residues of collagen. J. Electron Microsc. 35, 272-275.
49. Marchini, M., Morocutti, M., Castellani, P. P., Leonardi, L. & Ruggeri, A. 1983 The banding pattern of rat tail tendon freeze-etched collagen fibrils. Connect. Tissue Res. 11, 175-184. (doi:10.3109/03008208309004853)
50. Bairati, A., Petruccioli, M. G. & Tarelli, L. T. 1969 Studies on the ultrastructure of collagen fibrils. 1. Morphological evaluation of the periodic structure. J. Submicrosc. Cytol. 1, 113-141.
51. Raspanti, M., Alessandrini, A., Gobbi, P. & Ruggeri, A. 1996 Collagen fibril surface: TMAFM, FEG-SEM and freeze-etching observations. Microsc. Res. Tech. 35, 87-93. (doi:10.1002/(SICI)1097-0029(19960901)35:1 〈87::AID- JEMT8〉3.0.CO;2-P)
52. Baselt, D. R., Revel, J. P. & Baldeschwieler, J. D. 1993 Subfibrillar structure of type I collagen observed by atomic force microscopy. Biophys. J. 65, 2644-2655. (doi:10.1016/S0006-3495(93)81329-8)
53. Rosen, V. B., Hobbs, L. W. & Spector, M. 2002 The ultrastructure of anorganic bovine bone and selected synthetic hyroxyapatites used as bone graft substitute materials. Biomaterials 23, 921-928. (doi:10.1016/S0142-9612(01) 00204-6)
54. Chen, P. Y., Toroian, D., Price, P. A. & McKittrick, J. 2011 Minerals form a continuum phase in mature cancellous bone. Calcif. Tissue Int. 88, 351-361. (doi:10.1007/s00223-011-9462-8)
55. Boothroyd, B. 1964 The problem of demineralisation in thin sections of fully calcified bone. J. Cell Biol. 20, 165-173. (doi:10.1083/jcb.20.1.165)
56. Balooch, M., Balooch, G., Habelitz, S., Marshall, S. J. & Marshall, G. W. 2004 Intrafibrillar demineralization study of single human dentin collagen fibrils by AFM. Mat. Res. Soc. Symp. Proc. 823, W6.1. (doi:10.1557/PROC-823-W6. 1)
57. Balooch, M., Habelitz, S., Kinney, J. H., Marshall, S. J. & Marshall, G. W. 2008 Mechanical properties of mineralized collagen fibrils as influenced by demineralization. J. Struct. Biol. 162, 404-410. (doi:10.1016/j.jsb.2008.02. 010)
58. Buehler, M. J. 2007 Molecular nanomechanics of nascent bone: fibrillar toughening by mineralization. Nanotechnology 18, 295102. (doi:10.1088/0957-4484/ 18/29/295102)
59. Genin, G. M., Kent, A., Birman, V., Wopenka, B., Pasteris, J. D., Marquez, P. J. & Thomopoulos, S. 2009 Functional grading of mineral and collagen in the attachment of tendon to bone. Biophys. J. 97, 976-985. (doi:10.1016/j.bpj.2009.05.043)
60. Katz, E. P., Wachtel, E., Yamauchi, M. & Mechanic, G. L. 1989 The structure of mineralized collagen fibrils. Connect. Tissue Res. 21, 149-154 (discussion 55-58). (doi:10.3109/03008208909050005)
61. Fantner, G. E. et al. 2005 Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat. Mater. 4, 612-616. (doi:10.1038/nmat1428)
62. Jager, I. & Fratzl, P. 2000 Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles. Biophys. J. 79, 1737-1746. (doi:10.1016/S0006-3495(00)76426-5)
63. Genin, G. M. & Hutchinson, J. W. 1997 Composite laminates in plane stress: constitutive modeling, and stress redistribution due to matrix cracking. J. Am. Ceram. Soc. 80, 1245-1255. (doi:10.1111/j.1151-2916.1997.tb02971.x)
64. Budiansky, B., Hutchinson, J. W. & Evans, A. G. 1986 Matrix fracture in fiber-reinforced ceramics. J. Mech. Phys. Solids 34, 167-189. (doi:10.1016/0022-5096(86)90035-9)