Bone fracture toughness and strength correlate with collagen cross-link maturity in a dose-controlled lathyrism mouse model

Journal of Bone and Mineral Research

Volumn 30, Issue 3, 2015, Pages 446-455

  McNerny, Erin M B ^a   Gong, Bo ^a   Morris, Michael D ^a   Kohn, David H ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

Author keywords

B aminopropionitrile (BAPN); Biomechanics; Collagen cross links; Fracture toughness; Raman spectroscopy

Indexed keywords

3 AMINOPROPIONITRILE; AMIDE; CALCEIN; COLLAGEN; PROTEIN LYSINE 6 OXIDASE; PYRIDINOLINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE STRENGTH; CELL CULTURE; CONTROLLED STUDY; CROSS LINKING; ENZYME INHIBITION; FRACTURE; LATHYRISM; MOUSE; NONHUMAN; OSSIFICATION; RAMAN SPECTROMETRY; 3T3 CELL LINE; ANIMAL; BIOMECHANICS; DISEASE MODEL; METABOLISM; PATHOPHYSIOLOGY;

3T3 CELLS; AMINOPROPIONITRILE; ANIMALS; BIOMECHANICAL PHENOMENA; COLLAGEN; DISEASE MODELS, ANIMAL; FRACTURES, BONE; LATHYRISM; MICE;

EID: 84922879229     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2356     Document Type: Article

References (59)

1. Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: A possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int. 2010;21(2): 195-214.
2. Donnelly E. Methods for assessing bone quality: A review. Clin Orthop Relat Res. 2010;469(8): 2128-38.
3. Viguet-Carrin S, Garnero P, Delmas PD. The role of collagen in bone strength. Osteoporos Int. 2006;17(3): 319-36.
4. Burr DB, Turner CH. Biomechanics of bone. In: Favus M, editor. Primer on the metabolic bone diseases and disorders of mineral metabolism. 5th ed. Washington DC: American Society for Bone and Mineral Research; p. 58-64. 2003.
5. Reilly DT, Burstein AH. Review article. The mechanical properties of cortical bone. J Bone Joint Surg Am. 1974;56(5): 1001-22.
6. Currey JD. Role of collagen and other organics in the mechanical properties of bone. Osteoporos Int. 2003;14(Suppl 5): S29-36.
7. Zioupos P. Ageing human bone: Factors affecting its biomechanical properties and the role of collagen. J Biomater Appl. 2001;15(3): 187-229.
8. Wang X, Shen X, Li X, Agrawal CM. Age-related changes in the collagen network and toughness of bone. Bone. 2002;31(1): 1-7.
9. Uzel SGM, Buehler MJ. Molecular structure, mechanical behavior and failure mechanism of the C-terminal cross-link domain in type I collagen. J Mech Behav Biomed Mater. 2011;4: 153-61.
10. Robins S. Fibrillogenesis and maturation of collagens. In: Seibel MJ, Robins SP, Bilezikian JP, editors. Dynamics of bone and cartilage metabolism. 2nd ed. Burlington, MA: Academic Press; 2006. p.41-53.
11. Robins SP, Brady JD. Collagen cross-linking and metabolism. In: Bilezikian JP, Raisz LG, Martin TJ, editors. Principles of bone biology. 3rd ed. San Diego: Academic Press; 2008. p.319-4.
12. Eyre DR, Wu J-J. Collagen cross-links. Top Curr Chem. 2005;247: 207-29.
13. Hanson DA, Eyre DR. Molecular site specificity of pyridinoline and pyrrole cross-links in type I collagen of human bone. J Biol Chem. 1996;271(43): 26508-16.
14. Eyre DR, Weis MA, Wu J-J. Advances in collagen cross-link analysis. Methods. 2008;45(1): 65-74.
15. Knott L, Bailey AJ. Collagen cross-links in mineralizing tissues: A review of their chemistry, function, and clinical relevance. Bone. 1998;22(3): 181-7.
16. Robins SP. The separation of cross-linking components from collagen. In: Hall DA, editor. The methodology of connective tissue research. Oxford: Joynson-Bruvvers; 1976. p.37-52.
17. Bailey AJ, Sims TJ, Avery NC, Halligan EP. Non-enzymic glycation of fibrous collagen: Reaction products of glucose and ribose. Biochem J. 1995;305(Pt 2): 385-90.
18. Smith-Mungo LI, Kagan HM. Lysyl oxidase: Properties, regulation and multiple functions in biology. Matrix Biol. 1998;16(7): 387-98.
19. Paschalis EP, Shane E, Lyritis G, Skarantavos G, Mendelsohn R, Boskey AL. Bone fragility and collagen cross-links. J Bone Miner Res. 2004; 19(12): 2000-4.
20. Knott L, Whitehead CC, Fleming RH, Bailey AJ. Biochemical changes in the collagenous matrix of osteoporotic avian bone. Biochem J. 1995;310(Pt 3): 1045-51.
21. Saito M, Fujii K, Mori Y, Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int. 2006;17(10): 1514-23.
22. Burr DB. Bone material properties and mineral matrix contributions to fracture risk or age in women and men. J Musculoskelet Neuronal Interact. 2002;2(3): 201-4.
23. Viguet-Carrin S, Roux JP, Arlot ME, 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. 2006;39(5): 1073-9.
24. Garnero P, Borel O, Gineyts E, et al. Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone. 2006;38(3): 300-9.
25. Mccallum HM. Experimental lathyrism in mice. J Pathol Bacteriol. 1965;89: 625-36.
26. Chvapil M, Misiorowski R, Eskelson C. On the mechanisms of betaaminopropionitrile toxicity. J Surg Res. 1981;31(2): 151-5.
27. Paschalis EP, Tatakis DN, Robins S, et al. Lathyrism-induced alterations in collagen cross-links influence the mechanical properties of bone material without affecting the mineral. Bone. 2011;49(6): 1232-41.
28. Lees S, Eyre DR, Barnard SM. BAPN dose dependence of mature crosslinking in bone matrix collagen of rabbit compact bone: Corresponding variation of sonic velocity and equatorial diffraction spacing. Connect Tissue Res. 1990;24(2): 95-105.
29. Kohn RR, Leash AM. Long-term lathyrogen administration to rats, with special reference to aging. Exp Mol Pathol. 1967;7(3): 354-61.
30. Di Cesare PE, Nimni ME, Yazdi M, Cheung DT. Effects of lathyritic drugs and lathyritic demineralized bone matrix on induced and sustained osteogenesis. J Orthop Res. 1994;12(3): 395-402.
31. Lees S, Hanson D, Page E, Mook H. Comparison of dosage-dependent effects of beta-aminopropionitrile, sodium fluoride, and hydrocortisone on selected physical properties of cortical bone. J Bone Miner Res. 1994;9(9): 1377-89.
32. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010; 25(7): 1468-86.
33. Wallace JM, Golcuk K, Morris MD, Kohn DH. Inbred strain-specific response to biglycan deficiency in the cortical bone of C57BL6/129 and C3H/He mice. J Bone Miner Res. 2009;24(6): 1002-12.
34. Ritchie RO, Koester KJ, Ionova S, Yao W, Lane NE, Ager JW. Measurement of the toughness of bone: A tutorial with special reference to small animal studies. Bone. 2008;43(5): 798-812.
35. Roberts HC, Knott L, Avery NC, Cox TM, Evans MJ, Hayman AR. Altered collagen in tartrate-resistant acid phosphatase (TRAP)-deficient mice: A role for TRAP in bone collagen metabolism. Calcif Tissue Int. 2007; 80(6): 400-10.
36. Brown S, Worsfold M, Sharp C. Microplate assay for the measurement of hydroxyproline in acid-hydrolyzed tissue samples. Biotechniques. 2001;30(1): 38-40 42.
37. Gineyts E, Borel O, Chapurlat R, Garnero P. Quantification of immature and mature collagen crosslinks by liquid chromatographyelectrospray ionization mass spectrometry in connective tissues. J Chromatogr B Analyt Technol Biomed Life Sci. 2010;878(19): 1449-54.
38. Spacek P, Adam M. HPLC method for pentosidine determination in urine, serum, and tissues as a marker of glycation and oxidation loading of the organism. J Liq Chromatogr Relat Technol. 2002; 25(12): 1807-20.
39. Slowik-Zylka D, Safranow K, Dziedziejko V, Bukowska H, Ciechanowski K, Chlubek D. A sensitive and specific HPLC method for the determination of total pentosidine concentration in plasma. J Biochem Biophys Methods. 2004;61(3): 313-29.
40. Henle T, Schwarzenbolz U, Klostermeyer H. Detection and quantification of pentosidine in foods. Zeitschrift für Leb und -forsch A. 1997;204(2): 95-8.
41. Gong B, Oest ME, Mann KA, Damron TA, Morris MD. Raman spectroscopy demonstrates prolonged alteration of bone chemical composition following extremity localized irradiation. Bone. 2013; 57(1): 252-8.
42. Fernandes H, Dechering K, Van Someren E, et al. The role of collagen crosslinking in differentiation of human mesenchymal stem cells and MC3T3-E1 cells. Tissue Eng Part A. 2009;15(12): 3857-67.
43. Oxlund H, Barckman M, Ørtoft G, Andreassen T, Ortoft G. Reduced concentrations of collagen cross-links are associated with reduced strength of bone. Bone. 1995;17(4 Suppl): 365S-71S.
44. Li J, Li H, Wang L, Zhang L, Jing Z. Comparison of betaaminopropionitrile-induced aortic dissection model in rats by different administration and dosage. Vascular. 2013;21(5): 287-92.
45. El Rouby DH, Bashir MH, Korany NS. Ultrastructural and histomorphometric alterations of rat jaw bones after experimental induction of lathyrism. Arch Oral Biol. 2008;53(10): 916-23.
46. Farlay D, Duclos M-E, Gineyts E, et al. The ratio 1660/1690 cm(-1) measured by infrared microspectroscopy is not specific of enzymatic collagen cross-links in bone tissue. PLoS One. 2011;6(12): E28736.
47. Paschalis EP, Verdelis K, Doty SB, Boskey AL, Mendelsohn R, Yamauchi M. Spectroscopic characterization of collagen cross-links in bone. J Bone Miner Res. 2001;16(10): 1821-8.
48. Carden A, Rajachar RM, Morris MD, Kohn DH. Ultrastructural changes accompanying the mechanical deformation of bone tissue: A Raman imaging study. Calcif Tissue Int. 2003;72(2): 166-75.
49. Barth HD, Zimmermann EA, Schaible E, Tang SY, Alliston T, Ritchie RO. Characterization of the effects of x-ray irradiation on the hierarchical structure and mechanical properties of human cortical bone. Biomaterials. 2011;32(34): 8892-904.
50. Kohn DH, Sahar ND, Wallace JM, Golcuk K, Morris MD. Exercise alters mineral and matrix composition in the absence of adding new bone. Cells Tissues Organs. 2009;189(1-4): 33-7.
51. Zhu P, Xu J, Sahar N, Morris MD, Kohn DH, Ramamoorthy A. Timeresolved dehydration-induced structural changes in an intact bovine cortical bone revealed by solid-state NMR spectroscopy. J Am Chem Soc. 2009;131(47): 17064-5.
52. Turecek C, Fratzl-Zelman N, Rumpler M, et al. Collagen cross-linking influences osteoblastic differentiation. Calcif Tissue Int. 2008;82(5): 392-400.
53. Valcourt U, Merle B, Gineyts E, Viguet-Carrin S, Delmas PD, Garnero P. Non-enzymatic glycation of bone collagen modifies osteoclastic activity and differentiation. J Biol Chem. 2007;282(8): 5691-703.
54. Rosenquist J, Baylink D, Spengler D. The effect of beta-aminopropionitrile (BAPN) on bone mineralization. Proc Soc Exp Biol Med. 1977;154(2): 310-3.
55. Martin RB, Ishida J. The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. J Biomech. 1989;22(5): 419-26.
56. Ramasamy JG, Akkus O. Local variations in the micromechanical properties of mouse femur: The involvement of collagen fiber orientation and mineralization. J Biomech. 2007;40(4): 910-8.
57. Hong H-H, Pischon N, Santana RB, et al. A role for lysyl oxidase regulation in the control of normal collagen deposition in differentiating osteoblast cultures. J Cell Physiol. 2004;200(1): 53-62.
58. Gerstenfeld LC, Riva A, Hodgens K, Eyre DR, Landis WJ. Posttranslational control of collagen fibrillogenesis in mineralizing cultures of chick osteoblasts. J Bone Miner Res. 1993;8(9): 1031-43.
59. Banse X, Sims TJ, Bailey AJ. Mechanical properties of adult vertebral cancellous bone: Correlation with collagen intermolecular cross-links. J Bone Miner Res. 2002;17(9): 1621-8.