Association between collagen cross-links and trabecular microarchitecture properties of human vertebral bone

Bone

Volumn 46, Issue 2, 2010, Pages 342-347

  Viguet Carrin, S ^a   Follet, H ^a   Gineyts, E ^a   Roux, J P ^a   Munoz, F ^a   Chapurlat, R ^a   Delmas, P D ^a   Bouxsein, M L ^b  

^a UNIVERSITÉ LYON 1   (France)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Collagen cross links; Microarchitecture; Pentosidine; Trabecular bone; Vertebrae

Indexed keywords

COLLAGEN;

ADULT; AGED; ARTICLE; BIOCHEMISTRY; BIOMECHANICS; BONE AGE; BONE FRAGILITY; BONE STRUCTURE; CONTROLLED STUDY; DONOR; FEMALE; GLYCATION; HUMAN; HUMAN TISSUE; MALE; MICRO-COMPUTED TOMOGRAPHY; OSTEOMETRY; PROTEIN CROSS LINKING; SEX DIFFERENCE; TRABECULAR BONE; VERTEBRA;

AGED; AGED, 80 AND OVER; AGING; BONE DENSITY; COLLAGEN; CROSS-LINKING REAGENTS; FEMALE; HUMANS; MALE; MIDDLE AGED; SEX CHARACTERISTICS; SPINE; SURFACE PROPERTIES;

EID: 74249107400     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2009.10.001     Document Type: Article

References (41)

1. Seeman E., and Delmas P.D. Bone quality - the material and structural basis of bone strength and fragility. N. Engl. J. Med. 354 (2006) 2250-2261
2. Kleerekoper M., Villanueva A.R., Stanciu J., Rao D.S., and Parfitt A.M. The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif. Tissue Int. 37 (1985) 594-597
3. Bouxsein M.L., Melton III L.J., Riggs B.L., Muller J., Atkinson E.J., Oberg A.L., et al. Age- and sex-specific differences in the factor of risk for vertebral fracture: a population-based study using QCT. J. Bone Miner. Res. 21 (2006) 1475-1482
4. Chen H., Shoumura S., Emura S., and Bunai Y. Regional variations of vertebral trabecular bone microstructure with age and gender. Osteoporos. Int. 19 (2008) 1473-1483
5. Lochmuller E.M., Matsuura M., Bauer J., Hitzl W., Link T.M., Muller R., et al. Site-specific deterioration of trabecular bone architecture in men and women with advancing age. J. Bone Miner. Res. 23 (2008) 1964-1973
6. Gordon C.L., Lang T.F., Augat P., and Genant H.K. Image-based assessment of spinal trabecular bone structure from high-resolution CT images. Osteoporos. Int. 8 (1998) 317-325
7. Eyre D. Collagen cross-linking amino acids. Methods Enzymol. 144 (1987) 115-139
8. Knott L., and Bailey A.J. Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 22 (1998) 181-187
9. Viguet-Carrin S., Garnero P., and Delmas P.D. The role of collagen in bone strength. Osteoporos. Int. 17 (2006) 319-336
10. Grandhee S.K., and Monnier V.M. Mechanism of formation of the Maillard protein cross-link pentosidine. Glucose, fructose, and ascorbate as pentosidine precursors. J. Biol. Chem. 266 (1991) 11649-11653
11. Sell D.R., and Monnier V.M. Isolation, purification and partial characterization of novel fluorophores from aging human insoluble collagen-rich tissue. Connect. Tissue Res. 19 (1989) 77-92
12. 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 (1989) 21597-21602
13. Bailey A.J., Paul R.G., and Knott L. Mechanisms of maturation and ageing of collagen. Mech. Ageing Dev. 106 (1998) 1-56
14. Verzijl N., DeGroot J., Thorpe S.R., Bank R.A., Shaw J.N., Lyons T.J., et al. Effect of collagen turnover on the accumulation of advanced glycation end products. J. Biol. Chem. 275 (2000) 39027-39031
15. Avery N.C., and Bailey A.J. Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: relevance to aging and exercise. Scand. J. Med. Sci. Sports 15 (2005) 231-240
16. Vashishth D., Gibson G.J., Khoury J.I., Schaffler M.B., Kimura J., and Fyhrie D.P. Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone 28 (2001) 195-201
17. Viguet-Carrin S., Roux J.P., Arlot M.E., Merabet Z., Leeming D.J., Byrjalsen I., et al. Contribution of the advanced glycation end product pentosidine and of maturation of type I collagen to compressive biomechanical properties of human lumbar vertebrae. Bone 39 (2006) 1073-1079
18. Wang X., Shen X., Li X., and Agrawal C.M. Age-related changes in the collagen network and toughness of bone. Bone 31 (2002) 1-7
19. Hernandez C.J., Tang S.Y., Baumbach B.M., Hwu P.B., Sakkee A.N., van der H.F., et al. Trabecular microfracture and the influence of pyridinium and non-enzymatic glycation-mediated collagen cross-links. Bone 37 (2005) 825-832
20. Banse X., Devogelaer J.P., Lafosse A., Sims T.J., Grynpas M., and Bailey A.J. Cross-link profile of bone collagen correlates with structural organization of trabeculae. Bone 31 (2002) 70-76
21. Arlot M.E., Burt-Pichat B., Roux J.P., Vashishth D., Bouxsein M.L., and Delmas P.D. Microarchitecture influences microdamage accumulation in human vertebral trabecular bone. J. Bone Miner. Res. 23 (2008) 1613-1618
22. Chavassieux P.M., Arlot M.E., Reda C., Wei L., Yates A.J., and Meunier P.J. Histomorphometric assessment of the long-term effects of alendronate on bone quality and remodeling in patients with osteoporosis. J. Clin. Invest. 100 (1997) 1475-1480
23. Viguet-Carrin S., Gineyts E., Bertholon C., and Delmas P.D. Simple and sensitive method for quantification of fluorescent enzymatic mature and senescent crosslinks of collagen in bone hydrolysate using single-column high performance liquid chromatography. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 877 (2009) 1-7
24. Saito M., Marumo K., Fujii K., and Ishioka N. Single-column high-performance liquid chromatographic-fluorescence detection of immature, mature, and senescent cross-links of collagen. Anal. Biochem. 253 (1997) 26-32
25. Tang S.Y., Allen M.R., Phipps R., Burr D.B., and Vashishth D. Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos. Int. 20 (2009) 887-894
26. DeGroot J., Verzijl N., Wenting-Van Wijk M.J., Bank R.A., Lafeber F.P., Bijlsma J.W., et al. Age-related decrease in susceptibility of human articular cartilage to matrix metalloproteinase-mediated degradation: the role of advanced glycation end products. Arthritis Rheum. 44 (2001) 2562-2571
27. Sanguineti R., Storace D., Monacelli F., Federici A., and Odetti P. Pentosidine effects on human osteoblasts in vitro. Ann. N.Y. Acad. Sci. 1126 (2008) 166-172
28. Mercer N., Ahmed H., Etcheverry S.B., Vasta G.R., and Cortizo A.M. Regulation of advanced glycation end product (AGE) receptors and apoptosis by AGEs in osteoblast-like cells. Mol. Cell Biochem. 306 (2007) 87-94
29. McCarthy A.D., Etcheverry S.B., Bruzzone L., and Cortizo A.M. Effects of advanced glycation end-products on the proliferation and differentiation of osteoblast-like cells. Mol. Cell Biochem. 170 (1997) 43-51
30. Valcourt U., Merle B., Gineyts E., Viguet-Carrin S., Delmas P.D., and Garnero P. Non-enzymatic glycation of bone collagen modifies osteoclastic activity and differentiation. J. Biol. Chem. 282 (2007) 5691-5703
31. Paul R.G., and Bailey A.J. The effect of advanced glycation end-product formation upon cell-matrix interactions. Int. J. Biochem. Cell Biol. 31 (1999) 653-660
32. Allen M.R., Gineyts E., Leeming D.J., Burr D.B., and Delmas P.D. Bisphosphonates alter trabecular bone collagen cross-linking and isomerization in beagle dog vertebra. Osteoporos. Int. 19 (2008) 329-337
33. Saito M., Mori S., Mashiba T., Komatsubara S., and Marumo K. Collagen maturity, glycation induced-pentosidine, and mineralization are increased following 3-year treatment with incadronate in dogs. Osteoporos. Int. 19 (2008) 1343-1354
34. Saito M., Fujii K., Soshi S., and Tanaka T. Reductions in degree of mineralization and enzymatic collagen cross-links and increases in glycation-induced pentosidine in the femoral neck cortex in cases of femoral neck fracture. Osteoporos. Int. 17 (2006) 986-995
35. Eyre D.R., Dickson I.R., and Van N.K. Collagen cross-linking in human bone and articular cartilage. Age-related changes in the content of mature hydroxypyridinium residues. Biochem. J. 252 (1988) 495-500
36. Bailey A.J., Sims T.J., Ebbesen E.N., Mansell J.P., Thomsen J.S., and Mosekilde L. Age-related changes in the biochemical properties of human cancellous bone collagen: relationship to bone strength. Calcif. Tissue Int. 65 (1999) 203-210
37. Hein G., Weiss C., Lehmann G., Niwa T., Stein G., and Franke S. Advanced glycation end product modification of bone proteins and bone remodelling: hypothesis and preliminary immunohistochemical findings. Ann. Rheum. Dis. 65 (2006) 101-104
38. Monnier V.M., Mustata G.T., Biemel K.L., Reihl O., Lederer M.O., Zhenyu D., et al. Cross-linking of the extracellular matrix by the maillard reaction in aging and diabetes: an update on "a puzzle nearing resolution". Ann. N. Y. Acad. Sci. 1043 (2005) 533-544
39. Sell D.R., Biemel K.M., Reihl O., Lederer M.O., Strauch C.M., and Monnier V.M. Glucosepane is a major protein cross-link of the senescent human extracellular matrix. Relationship with diabetes. J. Biol. Chem. 280 (2005) 12310-12315
40. Biemel K.M., Friedl D.A., and Lederer M.O. Identification and quantification of major maillard cross-links in human serum albumin and lens protein. Evidence for glucosepane as the dominant compound. J. Biol. Chem. 277 (2002) 24907-24915
41. Saito M., Fujii K., and Marumo K. Degree of mineralization-related collagen crosslinking in the femoral neck cancellous bone in cases of hip fracture and controls. Calcif Tissue Int 79 (2006) 160-168