The role of collagen in bone strength
Abstract
Bone is a complex tissue of which the principal function is to resist mechanical forces and fractures. Bone strength depends not only on the quantity of bone tissue but also on the quality, which is characterized by the geometry and the shape of bones, the microarchitecture of the trabecular bones, the turnover, the mineral, and the collagen. Different determinants of bone quality are interrelated, especially the mineral and collagen, and analysis of their specific roles in bone strength is difficult. This review describes the interactions of type I collagen with the mineral and the contribution of the orientations of the collagen fibers when the bone is submitted to mechanical forces. Different processes of maturation of collagen occur in bone, which can result either from enzymatic or nonenzymatic processes. The enzymatic process involves activation of lysyl oxidase, which leads to the formation of immature and mature crosslinks that stabilize the collagen fibrils. Two type of nonenzymatic process are described in type I collagen: the formation of advanced glycation end products due to the accumulation of reducible sugars in bone tissue, and the process of racemization and isomerization in the telopeptide of the collagen. These modifications of collagen are age-related and may impair the mechanical properties of bone. To illustrate the role of the crosslinking process of collagen in bone strength, clinical disorders associated with bone collagen abnormalities and bone fragility, such as osteogenesis imperfecta and osteoporosis, are described.
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Collagen plays a critical role in the structure and function of bone tissue.
“In fact, it is known that collagen plays a critical role in the structure and function of bone tissue [120].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [120]
Cites
Advanced Glycosylation End Products in Tissue and the Biochemical Basis of Diabetic Complications
Flier, J. S., Underhill, L. H., Brownlee, M., Cerami, A., & Vlassara, H. (1988) · New England Journal of Medicine · doi:10.1056/nejm198805193182007 · Cited by 2,512 · see citing works
Oxidative stress hypothesis in Alzheimer’s disease
Markesbery, W. R. (1997) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(96)00629-6 · Cited by 2,383 · see citing works
Basic biomechanical measurements of bone: A tutorial
Turner, C. H., & Burr, D. B. (1993) · Bone · doi:10.1016/8756-3282(93)90081-k · Cited by 1,666 · see citing works
Geiger, T. L., & Clarke, S. G. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)75855-4 · Cited by 1,312 · see citing works
REST, M. V. D., & Garrone, R. (1991) · The FASEB Journal · doi:10.1096/fasebj.5.13.1916105 · Cited by 1,278 · see citing works
Wolff, S. P., & Dean, R. T. (1987) · Biochemical Journal · doi:10.1042/bj2450243 · Cited by 1,277 · see citing works
Rauch, F., & Glorieux, F. H. (2004) · The Lancet · doi:10.1016/s0140-6736(04)16051-0 · Cited by 1,202 · see citing works
Collagens, modifying enzymes and their mutations in humans, flies and worms
Myllyharju, J. (2003) · Trends in Genetics · doi:10.1016/j.tig.2003.11.004 · Cited by 1,179 · see citing works
Cross-linking in collagen and elastin.
Eyre, D. R., Paz, M. A., & Gallop, P. (1984) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.53.070184.003441 · Cited by 1,133 · see citing works
Structure Elucidation of a Senescence Cross-Link from Human Extracellular Matrix
Sell, D. R., & Monnier, V. M. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)88225-8 · Cited by 1,082 · see citing works
Stability of proteins. Proteins which do not present a single cooperative system.
Privalov, P. L. (1982) · PubMed · Cited by 1,035 · see citing works
Martin, R., Burr, D. B., & Sharkey, N. A. (1998) · Springer eBooks · doi:10.1007/978-1-4757-2968-9 · Cited by 980 · see citing works
Roher, A. E., Lowenson, J. D., Clarke, S., Wolkow, C., Wang, R., Cotter, R. J., Reardon, I. M., Zürcher-Neely, H. A., Heinrikson, R. L., & Ball, M. J. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53661-9 · Cited by 799 · see citing works
The effect of porosity and mineral content on the Young's modulus of elasticity of compact bone
Currey, J. D. (1988) · Journal of Biomechanics · doi:10.1016/0021-9290(88)90006-1 · Cited by 798 · see citing works
Older Women with Diabetes Have an Increased Risk of Fracture: A Prospective Study
Schwartz, A. V., Sellmeyer, D. E., Ensrud, K. E., Cauley, J. A., Tabor, H. K., Schreiner, P. J., Jamal, S. A., Black, D. M., & Cummings, S. R. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.1.7139 · Cited by 788 · see citing works
Age-related changes in the collagen network and toughness of bone
Wang, X., Shen, X., Li, X., & Agrawal, C. M. (2002) · Bone · doi:10.1016/s8756-3282(01)00697-4 · Cited by 769 · see citing works
Privalov, P. L. (1982) · Advances in protein chemistry · doi:10.1016/s0065-3233(08)60468-4 · Cited by 745 · see citing works
Mechanisms of maturation and ageing of collagen
Bailey, A. J., Paul, R. G., & Knott, L. (1998) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(98)00119-5 · Cited by 672 · see citing works
Knott, L., & Bailey, A. J. (1998) · Bone · doi:10.1016/s8756-3282(97)00279-2 · Cited by 647 · see citing works
Hydration structure of a collagen peptide
Bella, J., Brodsky, B., & Berman, H. M. (1995) · Structure · doi:10.1016/s0969-2126(01)00224-6 · Cited by 642 · see citing works
Glycation and Diabetic Complications
Brownlee, M. (1994) · Diabetes · doi:10.2337/diab.43.6.836 · Cited by 634 · see citing works
Grant, S. F. A., Reid, D. M., Blake, G., Herd, R., Fogelman, I., & Ralston, S. H. (1996) · Nature Genetics · doi:10.1038/ng1096-203 · Cited by 625 · see citing works
Saido, T. C., Iwatsubo, T., Mann, D. M. A., Shimada, H., Ihara, Y., & Kawashima, S. (1995) · Neuron · doi:10.1016/0896-6273(95)90301-1 · Cited by 587 · see citing works
Lysyl oxidase: Properties, regulation and multiple functions in biology
Smith‐Mungo, L. I., & Kagan, H. M. (1998) · Matrix Biology · doi:10.1016/s0945-053x(98)90012-9 · Cited by 581 · see citing works
Type 1 and Type 2 Diabetes and Incident Hip Fractures in Postmenopausal Women
Nicodemus, K. K., & Folsom, A. R. (2001) · Diabetes Care · doi:10.2337/diacare.24.7.1192 · Cited by 569 · see citing works
Influence of nonenzymatic glycation on biomechanical properties of cortical bone
Vashishth, D., Gibson, G. J., Khoury, J. I., Schaffler, M. B., Kimura, J., & Fyhrie, D. P. (2001) · Bone · doi:10.1016/s8756-3282(00)00434-8 · Cited by 525 · see citing works
Lysyl oxidases: A novel multifunctional amine oxidase family
Csiszar, K. (2001) · Progress in nucleic acid research and molecular biology · doi:10.1016/s0079-6603(01)70012-8 · Cited by 514 · see citing works
Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis
Myllyharju, J. (2003) · Matrix Biology · doi:10.1016/s0945-053x(03)00006-4 · Cited by 491 · see citing works
Bone indentation recovery time correlates with bond reforming time
Thompson, J. B., Kindt, J. H., Drake, B., Hansma, H. G., Morse, D. E., & Hansma, P. K. (2001) · Nature · doi:10.1038/414773a · Cited by 468 · see citing works
Mann, V., Hobson, E. E., Li, B., Stewart, T. L., Grant, S. F. A., Robins, S. P., Aspden, R. M., & Ralston, S. H. (2001) · Journal of Clinical Investigation · doi:10.1172/jci10347 · Cited by 462 · see citing works
Collagen structure and functional implications
Ottani, V., Raspanti, M., & Ruggeri, A. (2001) · Micron · doi:10.1016/s0968-4328(00)00042-1 · Cited by 425 · see citing works
Uitterlinden, A. G., Burger, H., Huang, Q., Yue, F., McGuigan, F. E., Grant, S. F. A., Albert Hofman, D., van Leeuwen, J. P. T. M., Pols, H. A. P., & Ralston, S. H. (1998) · New England Journal of Medicine · doi:10.1056/nejm199804093381502 · Cited by 419 · see citing works
Eyre, D. R., Dickson, I., & Ness, K. V. (1988) · Biochemical Journal · doi:10.1042/bj2520495 · Cited by 415 · see citing works
The role of collagen in determining bone mechanical properties
Wang, X., Bank, R. A., TeKoppele, J. M., & Agrawal, C. M. (2001) · Journal of Orthopaedic Research® · doi:10.1016/s0736-0266(01)00047-x · Cited by 373 · see citing works
Paul, R. G., & Bailey, A. J. (1996) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(96)00079-9 · Cited by 359 · see citing works
A Crosslinked Cofactor in Lysyl Oxidase: Redox Function for Amino Acid Side Chains
Wang, S. X., Mure, M., Medzihradszky, K. F., Burlingame, A. L., Brown, D. E., Dooley, D. M., Smith, A. J., Kagan, H. M., & Klinman, J. P. (1996) · Science · doi:10.1126/science.273.5278.1078 · Cited by 338 · see citing works
Clarke, S. G. (1987) · International journal of peptide & protein research · doi:10.1111/j.1399-3011.1987.tb03390.x · Cited by 338 · see citing works
Engel, J. D., & Prockop, D. J. (1991) · Annual Review of Biophysics and Biophysical Chemistry · doi:10.1146/annurev.bb.20.060191.001033 · Cited by 322 · see citing works
Dougados, M., Nguyen, M., Berdah, L., Mazi�res, B., Vignon, E. P., Lequesne, M. G., & for the ECHODIAH Investigators Study Group (2001) · Arthritis & Rheumatism · doi:10.1002/1529-0131(200111)44:11 · Cited by 320 · see citing works
Reduced concentrations of collagen cross-links are associated with reduced strength of bone
Oxlund, H., Barckman, M., Ørtoft, G., & Andreassen, T. T. (1995) · Bone · doi:10.1016/8756-3282(95)00328-b · Cited by 318 · see citing works
The effects of ageing and changes in mineral content in degrading the toughness of human femora
Currey, J. D., Brear, K., & Zioupos, P. (1996) · Journal of Biomechanics · doi:10.1016/0021-9290(95)00048-8 · Cited by 318 · see citing works
[7] Collagen cross-linking amino acids
Eyre, D. R. (1987) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(87)44176-1 · Cited by 316 · see citing works
Effects of ionizing radiation on the mechanical properties of human bone
Currey, J. D., Foreman, J., Laketić, I., et al. (1997) · Journal of Orthopaedic Research® · doi:10.1002/jor.1100150116 · Cited by 309 · see citing works
Prolyl 4-hydroxylases and their protein disulfide isomerase subunit
Kivirikko, K. I., & Myllyharju, J. (1998) · Matrix Biology · doi:10.1016/s0945-053x(98)90009-9 · Cited by 285 · see citing works
Robins, S. P., Shimokomaki, M., & Bailey, A. J. (1973) · Biochemical Journal · doi:10.1042/bj1310771 · Cited by 281 · see citing works
Banse, X., Sims, T. J., & Bailey, A. J. (2002) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2002.17.9.1621 · Cited by 267 · see citing works
Bone Fragility and Collagen Cross-Links
Paschalis, E. P., Shane, E. J., Lyritis, G. P., et al. (2004) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.040820 · Cited by 266 · see citing works
Engel, J. (1991) · Annual Review of Biophysics and Biomolecular Structure · doi:10.1146/annurev.biophys.20.1.137 · Cited by 264 · see citing works
Martin, R. B., & Boardman, D. L. (1993) · Journal of Biomechanics · doi:10.1016/s0021-9290(05)80004-1 · Cited by 250 · see citing works
Koivu, J., Myllylä, R., Helaakoski, T., Pihlajaniemi, T. A., Tasanen, K., & Kivirikko, K. I. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)48259-2 · Cited by 240 · see citing works
Peptidylproline cis/trans isomerases
Gałat, A., & Metcalfe, S. M. (1995) · Progress in Biophysics and Molecular Biology · doi:10.1016/0079-6107(94)00009-x · Cited by 240 · see citing works
Importance of measuring products of non-enzymatic glycation of proteins
Lapolla, A., Traldi, P., & Fedele, D. (2005) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2004.09.007 · Cited by 236 · see citing works
Fratzl, P., Paris, O., Klaushofer, K., et al. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118428 · Cited by 229 · see citing works
Barnett, M. L., Kremer, J. M., Clair, E. W. S., Clegg, D. O., Furst, D. E., Weisman, M. H., Fletcher, M., Chasan-Taber, S., Finger, E., Morales, A., et al. (1998) · Arthritis & Rheumatism · doi:10.1002/1529-0131(199802)41:2 · Cited by 227 · see citing works
Role of collagen and other organics in the mechanical properties of bone
Currey, J. D. (2003) · Osteoporosis International · doi:10.1007/s00198-003-1470-8 · Cited by 220 · see citing works
Changes in the impact energy absorption of bone with age
Currey, J. D. (1979) · Journal of Biomechanics · doi:10.1016/0021-9290(79)90031-9 · Cited by 214 · see citing works
Oxlund, H., Sekilde, L., & Ørtoft, G. (1996) · Bone · doi:10.1016/s8756-3282(96)00283-9 · Cited by 210 · see citing works
Boskey, A. L., Wright, T. M., & Blank, R. D. (1999) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1999.14.3.330 · Cited by 207 · see citing works
Maroudas, A., Bayliss, M. T., Kaushansky, N., Schneiderman, R. S., & Gil‐Av, E. (1998) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1997.0492 · Cited by 207 · see citing works
Procollagen folding and assembly: The role of endoplasmic reticulum enzymes and molecular chaperones
Lamandé, S. R., & Bateman, J. F. (1999) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.1999.0317 · Cited by 207 · see citing works
Characterization of Urinary Degradation Products Derived from Type I Collagen
Fledelius, C., Johnsen, A. H., CLOOS, P. A. C., et al. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.15.9755 · Cited by 203 · see citing works
Molecular Site Specificity of Pyridinoline and Pyrrole Cross-links in Type I Collagen of Human Bone
Hanson, D. A., & Eyre, D. R. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.43.26508 · Cited by 202 · see citing works
Prolyl 3-Hydroxylase 1, Enzyme Characterization and Identification of a Novel Family of Enzymes
Vranka, J. A., Sakai, L. Y., & Bächinger, H. P. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m312807200 · Cited by 200 · see citing works
Role of nonenzymatic glycosylation of type I collagen in diabetic osteopenia
Katayama, Y., Akatsu, T., Yamamoto, M., Kugai, N., & Nagata, N. (1996) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650110709 · Cited by 200 · see citing works
Bank, R. A., Robins, S. P., Wijmenga, C., Breslau‐Siderius, L., Bardoel, A. F. J., van der Sluijs, H. A., Pruijs, H. E. H., & TeKoppele, J. M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.3.1054 · Cited by 200 · see citing works
Mann, V., & Ralston, S. H. (2003) · Bone · doi:10.1016/s8756-3282(03)00087-5 · Cited by 196 · see citing works
Nagata, K. (1998) · Matrix Biology · doi:10.1016/s0945-053x(98)90011-7 · Cited by 195 · see citing works
Saito, M., Marumo, K., Fujii, K., & Ishioka, N. (1997) · Analytical Biochemistry · doi:10.1006/abio.1997.2350 · Cited by 193 · see citing works
Opsahl, W., Zeronian, H., Ellison, M., Lewis, D., Rucker, R. B., & Riggins, R. S. (1982) · Journal of Nutrition · doi:10.1093/jn/112.4.708 · Cited by 187 · see citing works
Leuchter, R. H., Alanay, Y., Bank, R. A., Campos‐Xavier, B., Zankl, A., Superti‐Furga, A., & Bonafé, L. (2004) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.30231 · Cited by 185 · see citing works
Biochemical changes in the collagenous matrix of osteoporotic avian bone
Knott, L., Whitehead, C. C., Fleming, R. H., & Bailey, A. J. (1995) · Biochemical Journal · doi:10.1042/bj3101045 · Cited by 172 · see citing works
The influence of peptidyl-prolyl cis-trans isomerase on the in vitro folding of type III collagen.
Bächinger, H. P. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)45502-0 · Cited by 171 · see citing works
Eyre, D. R., & Oguchi, H. (1980) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(80)90347-2 · Cited by 167 · see citing works
Uzawa, K., Grzesik, W. J., Nishiura, T., Kuznetsov, S. A., Robey, P. G., Brenner, D. A., & Yamauchi, M. (1999) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1999.14.8.1272 · Cited by 167 · see citing works
Isolation and structural identification of a labile intermolecular crosslink in collagen
Bailey, A. J., & Peach, C. M. (1968) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(68)90233-7 · Cited by 156 · see citing works
Ageing Human Bone: Factors Affecting its Biomechanical Properties and the Role of Collagen
Zioupos, P. (2001) · Journal of Biomaterials Applications · doi:10.1106/5juj-tfj3-jvva-3rj0 · Cited by 156 · see citing works
Tomiyama, T., Asano, S., Furiya, Y., Shirasawa, T., Endo, N., & Mori, H. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)34045-0 · Cited by 154 · see citing works
Cloos, P. A., & Fledelius, C. (2000) · Biochemical Journal · doi:10.1042/bj3450473 · Cited by 150 · see citing works
Protein motifs. 8. The triple-helix motif in proteins.
Brodsky, B., & Shah, N. K. (1995) · The FASEB Journal · doi:10.1096/fasebj.9.15.8529832 · Cited by 145 · see citing works
Garnero, P., CLOOS, P. A. C., Sornay‐Rendu, E., et al. (2002) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2002.17.5.826 · Cited by 138 · see citing works
Self-citationOsteon orientation of the diaphysis of the long bones in man
Heřt, J., Fiala, P., & Petrtýl, M. (1994) · Bone · doi:10.1016/8756-3282(94)90288-7 · Cited by 136 · see citing works
Segrest, J. P., & Cunningham, L. W. (1970) · Journal of Clinical Investigation · doi:10.1172/jci106367 · Cited by 136 · see citing works
Biochemical changes in the collagen of human osteoporotic bone matrix
Bailey, A. J., Wotton, S. F., Sims, T. J., & Thompson, P. W. (1993) · Connective Tissue Research · doi:10.3109/03008209309014239 · Cited by 135 · see citing works
The biomechanical integrity of bone in experimental diabetes
Reddy, G. K., Stehno‐Bittel, L., Hamade, S., & Enwemeka, C. S. (2001) · Diabetes Research and Clinical Practice · doi:10.1016/s0168-8227(01)00273-x · Cited by 135 · see citing works
Grabner, B., Landis, W. J., Roschger, P., et al. (2001) · Bone · doi:10.1016/s8756-3282(01)00594-4 · Cited by 134 · see citing works
Folding of peptide models of collagen and misfolding in disease
Baum, J., & Brodsky, B. (1999) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(99)80016-5 · Cited by 131 · see citing works
Nagata, K. (2003) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2003.09.020 · Cited by 130 · see citing works
Martin, R. B., Burr, D. B., Sharkey, N. A., & Fyhrie, D. P. (2015) · doi:10.1007/978-1-4939-3002-9 · Cited by 129 · see citing works
Structural Characteristics of Cross‐Linking Sites in type V Collagen of Bone
Niyibizi, C., & Eyre, D. R. (1994) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1994.00943.x · Cited by 128 · see citing works
Shimizu, T., Fukuda, H., Murayama, S., Izumiyama, N., & Shirasawa, T. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10350 · Cited by 128 · see citing works
Valtavaara, M., Szpirer, C., Szpirer, J., & Myllylä, R. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.21.12881 · Cited by 128 · see citing works
Cross-linking of collagen. Isolation, structural characterization and glycosylation of pyridinoline
Robins, S. P. (1983) · Biochemical Journal · doi:10.1042/bj2150167 · Cited by 126 · see citing works
Chen, A. C., Temple, M. M., Ng, D. M., Verzijl, N., DeGroot, J., TeKoppele, J. M., & Sah, R. L. (2002) · Arthritis & Rheumatism · doi:10.1002/art.10627 · Cited by 126 · see citing works
Fantner, G. E., Birkedal, H., Kindt, J. H., Hassenkam, T., Weaver, J. C., Cutroni, J. A., Bosma, B. L., Bawazer, L. A., Finch, M. M., Cidade, G. A. G., et al. (2004) · Bone · doi:10.1016/j.bone.2004.05.027 · Cited by 124 · see citing works
Type I collagen mutation alters the strength and fatigue behavior of Mov13 cortical tissue
Jepsen, K. J., Schaffler, M. B., Kuhn, J. L., et al. (1997) · Journal of Biomechanics · doi:10.1016/s0021-9290(97)00088-2 · Cited by 119 · see citing works
Kuznetsova, N. V., & Leikin, S. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.51.36083 · Cited by 119 · see citing works
John, D. C. A., Grant, M. E., & Bulleid, N. J. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05803.x · Cited by 114 · see citing works
Garnero, P., Fledelius, C., Gineyts, É., Serre, C., Vignot, E., & Delmas, P. D. (1997) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1997.12.9.1407 · Cited by 111 · see citing works
Self-citationPost-translational modifications in the collagen of human osteoporotic femoral head
Bailey, A. J., Wotton, S., Sims, T. J., & Thompson, P. W. (1992) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(92)91697-o · Cited by 109 · see citing works
Cloning and characterization of a third human lysyl hydroxylase isoform
Passoja, K., Rautavuoma, K., Ala‐Kokko, L., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.18.10482 · Cited by 107 · see citing works
Bulleid, N. J., Dalley, J. A., & Lees, J. F. (1997) · The EMBO Journal · doi:10.1093/emboj/16.22.6694 · Cited by 106 · see citing works
Changes in apatite crystal size in bones of patients with osteogenesis imperfecta
Vetter, U. K., Eanes, E. D., Kopp, J. B., et al. (1991) · Calcified Tissue International · doi:10.1007/bf02556213 · Cited by 104 · see citing works
Wang, C., Luosujärvi, H., Heikkinen, J., Risteli, M., Uitto, L., & Myllylä, R. (2002) · Matrix Biology · doi:10.1016/s0945-053x(02)00071-9 · Cited by 104 · see citing works
Lysyl Hydroxylase-2b Directs Collagen Cross-Linking Pathways in MC3T3-E1 Cells
Pornprasertsuk‐Damrongsri, S., Duarte, W. R., Mochida, Y., et al. (2004) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.040323 · Cited by 104 · see citing works
Gineyts, É., Cloos, P. A., Borel, O., Grimaud, L., Delmas, P. D., & Garnero, P. (2000) · Biochemical Journal · doi:10.1042/bj3450481 · Cited by 103 · see citing works
Self-citationMäki, J. M., Tikkanen, H., & Kivirikko, K. I. (2001) · Matrix Biology · doi:10.1016/s0945-053x(01)00157-3 · Cited by 101 · see citing works
Pyridoxine deficiency affects biomechanical properties of chick tibial bone
Masse, P. G., Rimnac, C. M., Yamauchi, M., Coburn, S. P., Rucker, R. B., Howell, D. S., & Boskey, A. L. (1996) · Bone · doi:10.1016/8756-3282(96)00072-5 · Cited by 100 · see citing works
Human collagens: Differences in glycosylated hydroxylysines in skin and bone
Pinnell, S. R., Fox, R., & Krane, S. M. (1971) · Biochimica et Biophysica Acta (BBA) - Protein Structure · doi:10.1016/0005-2795(71)90325-4 · Cited by 99 · see citing works
Feres‐Filho, E. J., Choi, Y. J., Han, X., et al. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.51.30797 · Cited by 98 · see citing works
Identification, expression, and tissue distribution of the three rat lysyl hydroxylase isoforms
Mercer, D. K., Nicol, P. F., Kimbembe, C. C., & Robins, S. P. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)01262-2 · Cited by 96 · see citing works
Ultrastructural studies of bones from patients with osteogenesis imperfecta
Traub, W., Arad, T., Vetter, U. K., & Weiner, S. (1994) · Matrix Biology · doi:10.1016/0945-053x(94)90200-3 · Cited by 92 · see citing works
Pornprasertsuk‐Damrongsri, S., Duarte, W. R., Mochida, Y., et al. (2005) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.041026 · Cited by 88 · see citing works
Robins, S. P., & Duncan, A. (1983) · Biochemical Journal · doi:10.1042/bj2150175 · Cited by 85 · see citing works
Eyre, D. R., & Glimcher, M. J. (1973) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(73)90764-x · Cited by 84 · see citing works
Kirsch, E., Krieg, T. M., REMBERGER, K., et al. (1981) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1981.tb01763.x · Cited by 82 · see citing works
Kuypers, R., Tyler, M., Kurth, L. B., et al. (1992) · Biochemical Journal · doi:10.1042/bj2830129 · Cited by 82 · see citing works
Molecular changes in bone collagen in osteoporosis and osteoarthritis in the elderly
Bailey, A. J., & Knott, L. (1999) · Experimental Gerontology · doi:10.1016/s0531-5565(99)00016-9 · Cited by 81 · see citing works
Torre-Blanco, A., Adachi, E., Hojima, Y., et al. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)45930-3 · Cited by 80 · see citing works
Verhaeghe, J., Suiker, A. M. H., Einhorn, T. A., Geusens, P., Visser, W. J., Herck, E. V., van Bree, R., Magitsky, S., & Bouillon, R. (1994) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650091021 · Cited by 77 · see citing works
DeFife, K. M., Colton, E., Nakayama, Y., Matsuda, T., & Anderson, J. M. (1999) · Journal of Biomedical Materials Research · doi:10.1002/(sici)1097-4636(199905)45:2 · Cited by 76 · see citing works
Harwood, R., Grant, M. E., & Jackson, D. S. (1974) · Biochemical Journal · doi:10.1042/bj1440123 · Cited by 71 · see citing works
Cross-link profile of bone collagen correlates with structural organization of trabeculae
Banse, X., Devogelaer, J. P., Lafosse, A., et al. (2002) · Bone · doi:10.1016/s8756-3282(02)00800-1 · Cited by 71 · see citing works
Diabetic and age-related enhancement of collagen-linked fluorescence in cortical bones of rats
Tomasek, J. J., Meyers, S. W., Basinger, J. B., et al. (1994) · Life Sciences · doi:10.1016/0024-3205(94)90041-8 · Cited by 71 · see citing works
Harwood, R., Grant, M. E., & Jackson, D. S. (1975) · Biochemical Journal · doi:10.1042/bj1520291 · Cited by 68 · see citing works
Bätge, B., Diebold, J., STEIN, H., et al. (1992) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1992.tb01450.x · Cited by 64 · see citing works
Puustjärvi, K., Nieminen, J., Räsänen, T., Hyttinen, M. M., Helminen, H. J., Kröger, H., Huuskonen, J., Alhava, E. M., & Kovanen, V. (1999) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1999.14.3.321 · Cited by 63 · see citing works
Detection of nonenzymatic browning products in the human lens
Monnier, V. M., & Cerami, A. (1983) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(83)90129-0 · Cited by 63 · see citing works
Changes in collagen cross-linking and lysyl oxidase by estrogen
Sanada, H., Shikata, J., Hamamoto, H., et al. (1978) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(78)90199-x · Cited by 63 · see citing works
Foot Problems as Risk Factors of Fractures
Keegan, T. H. M. (2002) · American Journal of Epidemiology · doi:10.1093/aje/155.10.926 · Cited by 62 · see citing works
Protein-specific chaperones: The role of hsp47 begins to gel
Hendershot, L. M., & Bulleid, N. J. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00850-2 · Cited by 60 · see citing works
Possible involvement of advanced glycation end-products in bone resorption
Miyata, T., Kawai, R., Taketomi, S., et al. (1996) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/11.supp5.54 · Cited by 59 · see citing works
Bone Type V Collagen: Chain Composition and Location of a Trypsin Cleavage Site
Niyibizi, C., & Eyre, D. R. (1989) · Connective Tissue Research · doi:10.3109/03008208909023894 · Cited by 58 · see citing works
Gineyts, É., Garnero, P., & Delmas, P. D. (2001) · Lara D. Veeken · doi:10.1093/rheumatology/40.3.315 · Cited by 57 · see citing works
Self-citationKöwitz, J., Knippel, M., Schuhr, T., & Mach, J. (1997) · Calcified Tissue International · doi:10.1007/s002239900271 · Cited by 52 · see citing works
Identification of a Second Functional Glutaredoxin Encoded by the Bacteriophage T4 Genome
Gvakharia, B. O., Hanson, E. S., Koonin, E. K., et al. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.26.15307 · Cited by 47 · see citing works
Collagen overglycosylation: A biochemical feature that may contribute to bone quality
Dominguez, L. J., Barbagallo, M., & Moro, L. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.02.050 · Cited by 47 · see citing works
Pereira, R. F., Hume, E. L., Halford, K. W., et al. (1995) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650101202 · Cited by 46 · see citing works
Isolation and characterization of glycosyl derivatives of the reducible cross‐links in collagens
Robins, S. P., & Bailey, A. J. (1974) · FEBS Letters · doi:10.1016/0014-5793(74)80085-2 · Cited by 39 · see citing works
Expression of lysyl oxidase isoforms in MC3T3-E1 osteoblastic cells
Atsawasuwan, P., Mochida, Y., Parisuthiman, D., & Yamauchi, M. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.12.119 · Cited by 39 · see citing works
Hydroxylysine in the N-terminal regions of the α1- and α2-chains of various collagens
Barnes, M. J., Constable, B. J., Morton, L. F., et al. (1971) · Biochemical Journal · doi:10.1042/bj1250433 · Cited by 38 · see citing works
Moro, L., Romanello, M., Favia, A., et al. (2000) · Calcified Tissue International · doi:10.1007/s002230010030 · Cited by 36 · see citing works
Lees, S. D., Hanson, D. B., Page, E. A., et al. (1994) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650090909 · Cited by 34 · see citing works
Colwell, A., Hamer, A. J., Blumsohn, A., et al. (1996) · European Journal of Clinical Investigation · doi:10.1046/j.1365-2362.1996.460602.x · Cited by 31 · see citing works
Structure and function of lamellar bone.
Marotti, G., Muglia, M. A., & Palumbo, C. (1994) · PubMed · Cited by 28 · see citing works
Identification of disulfide bonds in carboxy‐terminal propeptides of human type I procollagen
Koivu, J. (1987) · FEBS Letters · doi:10.1016/0014-5793(87)81350-9 · Cited by 24 · see citing works
Collagen fractions in lathyritic rats
Mikkonen, L., Tuominen, T., & Kulonen, E. (1960) · Biochemical Pharmacology · doi:10.1016/0006-2952(60)90105-2 · Cited by 24 · see citing works
Seitzer, U., Bätge, B., Açil, Y., et al. (1995) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1995.tb01974.x · Cited by 18 · see citing works
Neutron studies of collagen in lathyritic bone
Lee, S.-H., Barnard, S. M., & Mook, H. A. (1987) · International Journal of Biological Macromolecules · doi:10.1016/0141-8130(87)90022-5 · Cited by 14 · see citing works
Fujimori, E. (1985) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/0167-4838(85)90015-9 · Cited by 10 · see citing works
Mitochondrial hyperpolarization and ATP depletion in patients with systemic lupus erythematosus
Gergely, P., Grossman, C., Niland, B., Puskas, F., Neupane, H., Allam, F., Banki, K., Phillips, P. E., & Perl, A. (2002) · Arthritis & Rheumatism · doi:10.1002/1529-0131(200201)46:1 · Cited by 5 · see citing works
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Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells
Florencio-Silva, R., Sasso, G. R. D. S., Sasso-Cerri, E., Simões, M. J., & Cerri, P. S. (2015) · BioMed Research International · doi:10.1155/2015/421746 · Cited by 2,044 · see citing works
Bone mechanical properties and changes with osteoporosis
Osterhoff, G., Morgan, E. F., Shefelbine, S. J., Karim, L., McNamara, L. M., & Augat, P. (2016) · Injury · doi:10.1016/s0020-1383(16)47003-8 · Cited by 557 · see citing works
Manolagas, S. C., & Parfitt, A. M. (2010) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2010.01.010 · Cited by 404 · see citing works
Exercise and Bone Mass in Adults
Guadalupe-Grau, A., Fuentes, T., Guerra, B., & Calbet, J. A. L. (2009) · Sports Medicine · doi:10.2165/00007256-200939060-00002 · Cited by 397 · see citing works
Lin, W., Li, Y., Qiu, C., Zou, B., Gong, Y., Zhang, X., Tian, D., Sherman, W., Sanchez, F., Wu, D., et al. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkae1298 · Cited by 46 · see citing works
Johnston, E., & Buckley, M. (2023) · Molecules · doi:10.3390/molecules28134899 · Cited by 10 · see citing works
- Authors
- Viguet-Carrin, S., Garnero, P., & Delmas, P. D.
- Affiliations
- Lyon 1 Université (FR)
- Corresponding author
- Delmas, P. D.
- ORCID
- Garnero, P.
- Venue
- Osteoporosis International
- Published
- 2005-12-09
- Volume
- 17
- Issue
- 3
- Pages
- 319-336
- ISSN
- 0937-941X (ISSN-L)
- 1433-2965
- OpenAlex
- W2132551393
- Cited by
- 1,047
- References
- 150
- Citations by year
- 2026: 28 · 2025: 55 · 2024: 54 · 2023: 62 · 2022: 61 · 2021: 64 · 2020: 75 · 2019: 65 · 2018: 105 · 2017: 45 · 2016: 44 · 2015: 64 · 2014: 52 · 2013: 46 · 2012: 48
- FWCI
- 22.16
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Osteoporosis International (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Connective tissue disorders research
- Physical Sciences › Materials Science › Biomaterials › Collagen: Extraction and Characterization
- Keywords
- type I collagen, bone strength, bone quality, collagen mineralization, collagen cross-linking, lysyl oxidase, advanced glycation end products, collagen telopeptides, collagen maturation, bone fragility, osteogenesis imperfecta, osteoporosis, bone mechanical properties
- MeSH terms
- Animals, Biomechanical Phenomena, Bone Development, Bone Matrix, Collagen, Humans, Osteoporosis, Bone Density, Bone Remodeling, Fractures, Bone
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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