Collagen cross-links in mineralizing tissues: A review of their chemistry, function, and clinical relevance

Bone

Volumn 22, Issue 3, 1998, Pages 181-187

  Knott, Lynda ^a   Bailey, A J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Bone collagen; Bone strength; Collagen cross links; Mineralization; Osteoporosis; Pyridinoline

Indexed keywords

COLLAGEN; HYDROXYLYSINE; LYSINE; PYRIDINOLINE; PYRROLE;

BIOCHEMISTRY; BONE MINERAL; BONE MINERALIZATION; BONE STRENGTH; CROSS LINKING; CRYSTAL STRUCTURE; HUMAN; OSTEOLYSIS; OSTEOPOROSIS; PROTEIN MODIFICATION; REVIEW;

EID: 0032032089     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/S8756-3282(97)00279-2     Document Type: Article

References (77)

1. 1. Bailey, A. J. Chemical cross-linking restrictions on models for the molecular organization of the collagen fibre. Nature 288:408-413; 1980.
2. 2. Bailey, A. J. and Shimokomaki, M. Age-related changes in the reducible cross-links of collagen. FEBS Lett 16:86; 1971.
3. 3. Bailey, A. J., Sims, T. J., Lous, M. L., and Bazin, S. Collagen polymorphism in experimental granulation tissue. Biochem Biophys Res Commun 66:1160-1165; 1975.
4. 4. Bailey, A. J., Wotton, S. F., Sims, T. J., and Thompson, P. W. Post-translational modifications in the collagen of human osteoporotic femoral head. Biochem Biophys Res Commun 185:801-805; 1992.
5. 5. Barber, M., Bordoli, R. S., Elliott, G. J., Fujimoto, D., and Scott, J. E. The structure(s) of pyridinoline(s). Biochem Biophys Res Commun 109:1041-1046; 1982.
6. 6. Batge, B., Diebold, J., Stein, H., Bodo, M., and Muller, P. K. Compositional analysis of the collagenous bone matrix - A study on adult normal and osteopenic bone tissue. Eur J Clin Invest 22:805-812; 1992.
7. 7. Bonde, M., Qvist, P., Fidelius, C., Riis, B. J., and Christiansen, C. Immunoassay for quantifying type-I collagen degradation products in urine evaluated. Clin Chem 40:21122-2025; 1994.
8. 8. Eyre, D. R. Crosslink maturation in bone collagen. In: Veiss, A., Ed. The Chemistry and Biology of Mineralized Connective Tissues. New York: Elsevier North-Holland; 1981; 51-55.
9. 9. Eyre, D. R. The specificity of collagen cross-links as markers of bone and connective tissue degradation. Acta Orthop Scand 66; 1995.
10. 10. Eyre, D. R. Biochemical basis of collagen metabolites as bone turnover markers. In: Bilezikian, J. P., Raisz, L. G., and Rodan, G. A., Eds. Principles of Bone Biology. San Diego: Academic: 1996; 143-154.
11. 11. Eyre, D. R., Dickson, R., and Ness, K. V. Collagen cross-linking in human bone and articular cartilage. Biochem J 252:495-500; 1988.
12. 12. Eyre, D. R., Paz, M. A., and Gallop, P. M. Cross-linking on collagen and elastin. Ann Rev Biochem 53:749-790; 1984.
13. 13. Fledelius, C., Johnsen, A. H., Cloos, P. A. C., Bonde, M., and Qvist, P. Characterization of urinary degradation products derived from type I collagen. J Biol Chem 272:9755-9763; 1997.
14. 14. Fujimoto, D., Akiba, K., and Nakamura, N. Isolation and characterization of a fluorescent material in bovine achilles tendon collagen. Biochem Biophys Res Commun 76:1124-1129; 1977.
15. 15. Fujimoto, D., Moriguchi, T., Ishida, T., and Hayashi, H. The structure of pyridinoline, a collagen crosslink. Biochem Biophys Res Commun 84:52-57; 1978.
16. 16. Garnero, P., Gineyts, E., Arbault, P., Christiansen, C., and Delmas, P. D. Different effects of bisphosphonate and estrogen therapy on free and peptide-bound cross-links excretion. J Bone Miner Res 10:641-649; 1995.
17. 17. Garnero, P., Shin, W. J., Gineyts, E., Karpf, D. B., and Delmas, P. D. Comparison of new biochemical markers of bone turnover in late menopausal osteoporotic women in response to aledronate treatment. J Clin Endocrinol Metab 79:1693-1700; 1994.
18. 18. Gerriets, G. E., Curwin, S. L., and Last, J. A. Tendon hypertrophy is associated with increased hydroxylation of nonhelical lysine residues at two specific cross-linking sites in type I collagen. J Biol Chem 268:25553-25560; 1993.
19. 19. Glimcher, M. J., Shapiro, F., Ellis, R. D., and Eyre, D. R. Changes in tissue morphology and collagen composition during the repair of cortical bone in the adult chicken. J Bone Joint Surg 62A:964-973; 1980.
20. 20. Hanson, D. A. and Eyre, D. R. Molecular site specificity of pyridinoline and pyrrole cross-links in type I collagen of human bone. J Biol Chem 271; 1996.
21. 21. Hanson, D. A., Weis, M. E., Bollen, A., Maslan, S. L., Singer, F. S., and Eyre, D R. A specific immunoassay for monitoring human bone resorption: quantification of type-I collagen cross-linked N-telopeptides in urine. J Bone Miner Res 7:1251-1258; 1992.
22. 22. Henkel, W., Glanville, R. W., and Greifendorf, D. Characterisation of a type-I collagen trimeric cross-linked peptide from calf aorta and its cross-linked structure. Eur J Biochem 165:427-436; 1987.
23. 23. Horgan, D. J., King, N. L., Kurth, L. B., and Kuypers, R. Collagen cross-links and their relationship to the thermal properties of calf tendons. Arch Biochem Biophys 281:21-26; 1990.
24. 24. Hulmes, D. J. S. and Miller, A. A quasihexagonal model for the molecular packing of collagen. Nature 282:878-880; 1979.
25. 25. Ihme, A., Krieg, T., Nerlich, A., Feldmann, U., Rauterberg, J., Glanville, R. W., Edel, G., and Muller, P. K. Ehlers-Danlos syndrome type VI: Collagen type specificity of defective lysyl hydroxylation in various tissues. J Invest Dermatol 83:161-165; 1984.
26. 26. Kamel, S., Brazier, M., Rogez, J. C., Vincent, O., Maamer, M., Desmet, G., and Sebert, J. L. Different responses of free and peptide-bound cross-links to vitamin D and calcium supplementation in elderly women with vitamin D insufficiency. J Clin Endocrin Metab 81; 1996.
27. 27. Kang, A. H. Studies on the location of intermolecular cross-links in collagen. Isolation of a CNBr peptide containing hydroxylysinorleucine. Biochem 11: 1828-1835; 1972.
28. 28. Katz, I., Li, M., Joffe, I., Stein, B., Jacobs, T., Liang, X. G., Ke, H. Z., Jee, W., and Epstein, S. Influence of age on cyclosporin A-induced alterations in bone mineral metabolism in the rat in vivo. J Bone Miner Res 9; 1994.
29. 29. Kemp, P. D. and Scott, J. E. Ehrlich chromogens, probable cross-links in elastin and collagen. Biochem J 252:387-393; 1988.
30. 30. Kirsche, E., Krieg, T., Remberger, K., Fendel, M., Bruckner, P., and Muller, P. K. Disorder of collagen metabolism in a patient with osteogenesis imperfecta (lethal type)-increased degree of hydroxylation of lysine in collagen type I and type III. J Clin Invest 11:39-47; 1981.
31. 31. Kivirikko, K. I. Collagen glycosyltransferases. Int Rev Connect Tissue Res 8:23-72; 1979.
32. 32. Knott, L., Tarlton, J. F., and Bailey, A. J. Chemistry of collagen cross-linking: Biochemical changes in collagen during the partial mineralization of turkey leg tendon. Biochem J 322:535-542; 1997.
33. 33. Knott, L., Whitehead, C. C., Fleming, R. H., and Bailey, A. J. Biochemical changes in the collagenous matrix of osteoporotic avian bone. Biochem J 310:1045-1051; 1995.
34. 34. Kuboki, Y. and Mechanic, G. L. Comparitive molecular distribution of cross-links in bone and dentin collagen. Structure function relationships. Calcif Tissue Int 34:306-308; 1982.
35. 35. Kuypers, R., Tyler, M., Kurth, L. B., Jenkins, I. D., and Horgan, D. J. Identification of the loci of the collagen-associated Ehrlich chromogen in type I collagen confirms its role as a trivalent cross-link. Biochem J 283:129-136; 1992.
36. 36. 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. Microsc Res Techn 33; 1996.
37. 37. Lees, S., Eyre, D. E., and Barnard, S. M. Bapn dose dependence of mature cross-linking in bone matrix collagen of rabbit compact bone: Corresponding sonic velocity and equatorial diffraction spacing. Connect Tissue Res 24:95-105; 1990.
38. 38. Lees, S. and Page, E. A. A study of some properties of mineralized turkey leg tendon. Connect Tissue Res 28:263-287; 1992.
39. 39. Mansell, J. P., Bailey, A. J., Ristelli, L., and Ristelli, J. Pyrrolic cross-links in mineralised tissues. In: FECTS XIVth Meeting. Lyon, France: 1994; N13.
40. 40. Mather, B. S. Variation with age and sex in strength of the femur. Med Biol Eng 6:129-132; 1968.
41. 41. McCalden, R. W., McGeough, J. A., Barker, M. B., and Court-Brown, C. M. Age-related changes in the tensile properties of cortical bone. J Bone Joint Surg 75A:1193-1205; 1993.
42. 42. Melick, R. A. and Miller, D. R. Variations of tensile strength of human cortical bone with age. Clin Sci 30:243-248; 1966.
43. 43. Miller, E. J. Collagen cross-links. Identification of two CNBr peptides containing sites of intermolecular cross-link formation in cartilage. Biochem Biophys Res Commun 43:444-451; 1971.
44. 44. Mosekilde, L., Danielsen, C. C., and Knudsen, U. B. The effect of aging and ovariectomy on the vertebral bone mass and biomechanical properties of mature rats. Bone 14:1-6; 1993.
45. 45. Nicholls, A. C. and Bailey, A. J. Identification of cyanogen bromide peptides involved in intermolecular cross-linking of bovine type III collagen. Biochem J 185:195-201; 1980.
46. 46. Ogawa, T., Ono, T., Tsuda, M., and Kawanishi, Y. A novel fluor in insoluble collagen: A cross-linking moiety in collagen molecules. Biochem Biophys Res Commun 107:1252-1257; 1982.
47. 47. Orth, M. W., Martinez, D. A., Cook, M. E., and Vailas, A. C. The presence of lysylpyridinoline in the hypertrophic cartilage of newly hatched chicks. Biochim Biophys Acta 1157:229-232; 1993.
48. 48. Otsubo, K., Katz, E. P., Mechanic, G. L., and Yamauchi, M. Cross-linking connectivity in bone collagen fibrils: The COOH-terminal locus of free aldehyde. Biochem 31:396-402; 1992.
49. 49. Oxlund, H., Barckman, M., Ortoft, G., and Andreassen, T. T. Reduced concentrations ot collagen cross-links are associated with reduced strength of bone. Bone 17; 1995.
50. 50. Paul, R. G. and Bailey, A. J. Glycation of collagen: The basis of its central role in the late complications of aging and diabetes. Int J Biochem Cell Biol 28:1297-1310; 1996.
51. 51. Reiser, K. M. and Last, J. A. Biosynthesis of collagen cross-links: In vivo labeling of neonatal skin, tendon, and bone in rats. Connect Tissue Res 14:293-306; 1986.
52. 52. Ricard-Blum, S. and Ville, G. Collagen cross-linking. Cell Molec Biol 34:581-590; 1988.
53. 53. Risteli, L., Risteli, J., and Moniz, C. Measuring collagen degredation. Eur J Clin Invest 23:339-340; 1993.
54. 54. Robins, S. P. An enzyme-linked immunoassay for the collagen cross-link, pyridinoline. Biochem J 207:617-620; 1982.
55. 55. Robins, S. P. Turnover and cross-linking of collagen. In: Weiss, J. B. and Jayson, M. I. V., Eds. Collagen in Health and Disease. Edinburgh: Churchill Livingstone; 1982; 160-178.
56. 56. Robins, S. P. Cross-linking of collagen. Isolation, structural characterization. and glycosylation of pyridinoline. Biochem J 215:167-173; 1983.
57. 57. Robins, S. P. Collagen cross-links in metabolic bone disease. Acta Orthop Scand 66; 1995.
58. 58. Robins, S. P. and Bailey, A. J. Isolation and characterisation of glycosyl derivatives of the reducible cross-links in collagen. FEBS Lett 38:334-336; 1974.
59. 59. Robins, S. P. and Bailey, A. J. The chemistry of the collagen cross-links. The mechanism of stabilisation of the reducible intermediate cross-links. Biochem J 149:381-385; 1975.
60. 60. Robins, S. P. and Duncan, A. Cross-linking of collagen. Location of pyridinoline in bovine articular cartilage at two sites of the molecule. Biochem J 215:175-182; 1983.
61. 61. Robins, S. P. and Duncan, A. Pyridinium cross-links of bone collagen and their location in peptides isolated from rat femur. Biochim Biophys Acta 914:233-239; 1987.
62. 62. Robins, S. P., Woitge, H., Hesley, R., Ju, J., Seyedin, S., and Seibel, M. J. A direct enzyme-linked immunoassay for urinary deoxypyridinoline as a specific marker for measuring bone resorption. J Bone Miner Res 9:1643-1649; 1994.
63. 63. Royce, P. M. and Barnes, M. J. Failure of highly purified lysyl hydroxlase to hydroxylate lysyl residues in the nonhelical regions of collagen. Biochem J 230:475-480; 1985.
64. 64. Russell, R. G. G. The assessment of bone metabolism in vivo using biochemical approaches. Horm Metab Res 29:138-144; 1997.
65. 65. Scott, J. E., Hughes, E. W., and Shuttleworth, A. A collagen-associated Ehrlich chromogen: A pyrrolic cross-link? Biosci Rep 1:611-618; 1981.
66. 66. Segrest, J. P. and Cunningham, L. W. Variation in human urinary O-hydrolysyl glycoside levels and their relationaship to collagen metabolism. J Clin Invest 49:1497-1509; 1970.
67. 67. Seigel, R. C. Lysyl oxidase. Int Rev Connect Tissue Res 8:73-118; 1979.
68. 68. Sell, D. R. and Monnier, V. M. Structure elucidation of a senescence cross-link from human extracellular matrix. Implication of pentoses in the aging process. J Biol Chem 264:21597-21602; 1989.
69. 69. Steinmann, B., Bruckner, P., and Superti-Furga, A. Cyclosporin A slows collagen triple-helix formation in vivo: Indirect evidence for a physiologic role of petidyl-prolyl cis-trans-isomerase. J Biol Chem 266:1299-1303; 1991.
70. 70. Steinmann, B., Royce, P. M., and Superti-Furga, A The Ehlers-Danlos syndrome. In: Royce, P. M. and Steimann, B., Eds. Connective Tissue and Its Heritable Disorders. New York: Wiley-Liss; 1993; 351-407.
71. 71. Tilson, M. D., Dreyer, R. N., Hudson, A., and Cotter, R. J. Partial charaeterization of an analog of pyridinoline isolated from human skin. Biochem Biophys Res Commun 126:1222-1227; 1985.
72. 72. Torre-Blanco, A., Adachi, E., Hojima, Y., Wootton, J A. M., Minor, R. R., and Prockop, D. J. Temperature-induced post-translational overmodification of type I collagen. J Biol Chem 267:2650-2655; 1992.
73. 73. Traub, W., Arad, T., and Weiner, S. Three-dimensional ordered distribution of crystals in turkey tendon collagen fibers. Proc Natl Acad Sci 86:9822-9826; 1989.
74. 74. Yamauchi, M. and Katz, E. P. The post-translational chemistry and molecular packing of mineralizing tendon collagens. Connect Tissue Res 29:81-98; 1993.
75. 75. Yamauchi, M. Katz, E. P., and Mechanic, G. L. Intermolecular cross-linking and stereospecific molecular packing in type I collagen fibrils of the periodontal ligament. Biochem 25:4907-4913; 1986.
76. 76. Yamauchi, M., Katz, E. P., Otsubo, K., Teraoka, K., and Mechanic, G. L. Cross-linking and stereospecific structure of collagen in mineralized and nonmineralized skeletal tissues. Connect Tissue Res 21:159-169; 1989.
77. 77. Yamauchi, M., Noyes, C., Kuboki, Y., and Mechanic, G. L. Collagen structural microheterogencity and a possible role for glycosylated hydroxylysine in type I collagen. Proc Natl Acad Sci USA 7:7684-7688; 1982.