Lathyrism-induced alterations in collagen cross-links influence the mechanical properties of bone material without affecting the mineral

Bone

Volumn 49, Issue 6, 2011, Pages 1232-1241

  Paschalis, E P ^a   Tatakis, D N ^b,c   Robins, S ^d   Fratzl, P ^e   Manjubala, I ^e   Zoehrer, R ^a,i   Gamsjaeger, S ^a   Buchinger, B ^a   Roschger, A ^a   Phipps, R ^f   Boskey, A L ^g   Dall'Ara, E ^h   Varga, P ^h   Zysset, P ^h   Klaushofer, K ^a   Roschger, P ^a  

^a HANUSCH HOSPITAL   (Austria)

^b OHIO STATE UNIVERSITY   (United States)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

^d ROWETT RESEARCH INSTITUTE   (United Kingdom)

^e MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^f HUSSON UNIVERSITY   (United States)

^g HOSPITAL FOR SPECIAL SURGERY   (United States)

^h VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

ⁱ FLINDERS UNIVERSITY   (Australia)

Author keywords

aminopropionitrile; Bone formation; Bone quality; Bone strength; Collagen; Collagen cross links

Indexed keywords

3 AMINOPROPIONITRILE; COLLAGEN; PROTEIN LYSINE 6 OXIDASE;

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE CHARACTERISTICS AND FUNCTIONS; BONE DENSITY; BONE HARDNESS; BONE MASS; BONE MATRIX; BONE MINERAL; BONE STRENGTH; BONE STRUCTURE; BONE THICKNESS; COMPRESSION; CONTROLLED STUDY; CRYSTALLIZATION; ENZYME INHIBITION; FEMALE; LATHYRISM; MUTATION; NONHUMAN; OSSIFICATION; PROTEIN CROSS LINKING; RAT; RIGIDITY; STRUCTURE ANALYSIS; TRABECULAR BONE;

AMINOPROPIONITRILE; ANALYSIS OF VARIANCE; ANIMALS; BIOMECHANICS; BONE DENSITY; COLLAGEN; CROSS-LINKING REAGENTS; FEMALE; HUMANS; LATHYRISM; RATS; SPINE; X-RAY MICROTOMOGRAPHY;

EID: 81355146742     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2011.08.027     Document Type: Article

References (70)

1. Albright F., Reifenstein E.C. The parathyroid glands and metabolic bone disease 1948, Williams and Wilkins, Baltimore, MD.
2. Fratzl P., Gupta H., Paschalis E., Roschger P. Structure and mechanical quality of the collagen-mineral nano-composite in bone. J. Mater. Chem. 2004, 14:2115-2123.
3. Yamauchi M. Collagen: the major matrix molecule in mineralized tissues. Calcium and phosphorus in health and disease 1996, 127-141. CRC Press, New York. J.J.B. Anderson, S.C. Garner (Eds.).
4. Hansen D.A., Eyre D.R. Molecular site specificity of pyridinoline and pyrrole cross-links in type I collagen of human bone. J Biol Chem 1996, 271:26508-26516.
5. Kuypers R., Tyler M., Kurth L.B., Jenkins I.D., Hogan 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 1992, 283:129-136.
6. Knott L., Tarlton J.F., Bailey A.J. Chemistry of collagen cross-linking: biochemical changes in collagen during the partial mineralization of turkey leg tendon. Biochem J 1997, 322:535-542.
7. Brady J.D., Robins S.P. Structural characterization of pyrrolic cross-links in collagen using a biotinylated Ehrlich's reagent. J Biol Chem 2001, 276:18812-18818.
8. Robins S.P. Biochemistry and functional significance of collagen cross-linking. Biochem Soc Trans 2007, 35:849-852.
9. Nyman J.S., Roy A., Acuna R.L., Gayle H.J., Reyes M.J., Tyler J.H., et al. Age-related effect on the concentration of collagen crosslinks in human osteonal and interstitial bone tissue. Bone 2006, 39:1210-1217.
10. 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, 21:195-214.
11. Tang S.Y., Zeenath U., Vashishth D. Effects of non-enzymatic glycation on cancellous bone fragility. Bone 2007, 40:1144-1151.
12. Gjesdal C.G., Vollset S.E., Ueland P.M., Refsum H., Meyer H.E., Tell G.S. Plasma homocysteine, folate, and vitamin B 12 and the risk of hip fracture: the hordaland homocysteine study. J Bone Miner Res 2007, 22:747-756.
13. McLean R.R., Hannan M.T. B vitamins, homocysteine, and bone disease: epidemiology and pathophysiology. Curr Osteoporos Rep 2007, 5:112-119.
14. McLean R.R., Jacques P.F., Selhub J., Fredman L., Tucker K.L., Samelson E.J., et al. Plasma B vitamins, homocysteine, and their relation with bone loss and hip fracture in elderly men and women. J Clin Endocrinol Metab 2008, 93:2206-2212.
15. McLean R.R., Jacques P.F., Selhub J., Tucker K.L., Samelson E.J., Broe K.E., et al. Homocysteine as a predictive factor for hip fracture in older persons. N Engl J Med 2004, 350:2042-2049.
16. Blouin S., Thaler H.W., Korninger C., Schmid R., Hofstaetter J.G., Zoehrer R., et al. Bone matrix quality and plasma homocysteine levels. Bone 2009, 44:959-964.
17. Paschalis E.P., Recker R., DiCarlo E., Doty S.B., Atti E., Boskey A.L. Distribution of collagen cross-links in normal human trabecular bone. J Bone Miner Res 2003, 18:1942-1946.
18. Paschalis E.P., Shane E., Lyritis G., Skarantavos G., Mendelsohn R., Boskey A.L. Bone fragility and collagen cross-links. J Bone Miner Res 2004, 19:2000-2004.
19. Gourion-Arsiquaud S., Faibish D., Myers E., Spevak L., Compston J., Hodsman A., et al. Use of FTIR spectroscopic imaging to identify parameters associated with fragility fracture. J Bone Miner Res 2009, 24:1565-1571.
20. Blank R.D., Baldini T.H., Kaufman M., Bailey S., Gupta R., Yershov Y., et al. Spectroscopically determined collagen Pyr/deH-DHLNL cross-link ratio and crystallinity indices differ markedly in recombinant congenic mice with divergent calculated bone tissue strength. Connect Tissue Res 2003, 44:134-142.
21. Paschalis E.P., Glass E.V., Donley D.W., Eriksen E.F. Bone mineral and collagen quality in iliac crest biopsies of patients given teriparatide: new results from the fracture prevention trial. J Clin Endocrinol Metab 2005, 90:4644-4649.
22. Oxlund H., Barckman M., Ortoft G., Andreassen T.T. Reduced concentrations of collagen cross-links are associated with reduced strength of bone. Bone 1995, 17:365S-371S.
23. Spengler D.M., Baylink D.J., Rosenquist J.B. Effect of beta-aminopropionitrile on bone mechanical properties. J Bone Joint Surg Am 1977, 59:670-672.
24. Wegedal J.E. Enzymes of protein and phosphate catabolism in rat bone. I. Enzyme properties in normal rats. Calcif Tissue Res 1969, 3:55-66.
25. Robins S.P., Milne G., Duncan A., Davies C., Butt R., Greiling D., et al. Increased skin collagen extractability and proportions of collagen type III are not normalized after 6months healing of human excisional wounds. J Invest Dermatol 2003, 121:267-272.
26. Roschger P., Paschalis E.P., Fratzl P., Klaushofer K. Bone mineralization density distribution in health and disease. Bone 2008, 42:456-466.
27. Fratzl-Zelman N., Roschger P., Gourrier A., Weber M., Misof B.M., Loveridge N., et al. Combination of nanoindentation and quantitative backscattered electron imaging revealed altered bone material properties associated with femoral neck fragility. Calcif Tissue Int 2009, 85:335-343.
28. Manjubala I., Liu Y., Epari D.R., Roschger P., Schell H., Fratzl P., et al. Spatial and temporal variations of mechanical properties and mineral content of the external callus during bone healing. Bone 2009, 45:185-192.
29. Oliver W., Pharr G. An improved technique for determining hardness and elastic-modulus using load and displacement sensing indentation experiments. J Mater Res 1992, 7:1564-1583.
30. Boskey A.L., Pleshko N., Doty S.B., Mendelsohn R. Applications of Fourier transform infrared (FT-IR) microscopy to the study of mineralization in bone and cartilage. Cells Mater 1992, 2:209-220.
31. Gadaleta S.J., Paschalis E.P., Betts F., Mendelsohn R., Boskey A.L. Fourier transform infrared spectroscopy of the solution-mediated conversion of amorphous calcium phosphate to hydroxyapatite: new correlations between X-ray diffraction and infrared data. Calcif Tissue Int 1996, 58:9-16.
32. Paschalis E.P., DiCarlo E., Betts F., Sherman P., Mendelsohn R., Boskey A.L. FTIR microspectroscopic analysis of human osteonal bone. Calcif Tissue Int 1996, 59:480-487.
33. Paschalis E.P., Verdelis K., Doty S.B., Boskey A.L., Mendelsohn R., Yamauchi M. Spectroscopic characterization of collagen cross-links in bone. J Bone Miner Res 2001, 16:1821-1828.
34. Bailey A.J., Wotton S.F., Sims T.J., Thompson P.W. Biochemical changes in the collagen of human osteoporotic bone matrix. Connect Tissue Res 1993, 29:119-132.
35. Banse X. When density fails to predict bone strength. Acta Orthop Scand Suppl 2002, 73:1-57.
36. Banse X., Sims T.J., Bailey A.J. Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links. J Bone Miner Res 2002, 17:1621-1628.
37. Knott L., Whitehead C.C., Fleming R.H., Bailey A.J. Biochemical changes in the collagenous matrix of osteoporotic avian bone. Biochem J 1995, 310:1045-1051.
38. Kowitz J., Knippel M., Schuhr T., Mach J. Alteration in the extent of collagen I hydroxylation, isolated from femoral heads of women with a femoral neck fracture caused by osteoporosis. Calcif Tissue Int 1997, 60:501-505.
39. Oxlund H., Mosekilde L., Ortoff G. Alterations in the stability of collagen from human trabecular bone with respect to age. Osteoporosis 1987 1987, 309-312. Osteopress APS, Copenhagen. C. Christiansen, J.S. Johansen, B.J. Riis (Eds.).
40. Banse X., Devogelaer J.P., Lafosse A., Sims T.J., Grynpas M., Bailey A.J. Cross-link profile of bone collagen correlates with structural organization of trabeculae. Bone 2002, 31:70-76.
41. Smith L.J., Schirer J.P., Fazzalari N.L. The role of mineral content in determining the micromechanical properties of discrete trabecular bone remodeling packets. J Biomech 2010, 43:3144-3149.
42. Zebaze R.M., Jones A.C., Pandy M.G., Knackstedt M.A., Seeman E. Differences in the degree of bone tissue mineralization account for little of the differences in tissue elastic properties. Bone 2011, 48(6):1246-1251.
43. Gao H., Ji B., Jager I.L., Arzt E., Fratzl P. Materials become insensitive to flaws at nanoscale: lessons from nature. Proc Natl Acad Sci USA 2003, 100:5597-5600.
44. Jager I., Fratzl P. Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles. Biophys J 2000, 79:1737-1746.
45. Bailey A.J., Knott L. Molecular changes in bone collagen in osteoporosis and osteoarthritis in the elderly. Exp Gerontol 1999, 34:337-351.
46. Bailey A.J., Wotton S.F., Sims T.J., Thompson P.W. Post-translational modifications in the collagen of human osteoporotic femoral head. Biochem Biophys Res Commun 1992, 185:801-805.
47. Knott L., Bailey A.J. Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 1998, 22:181-187.
48. 6 deficiency experimentally-induced bone and joint disorder: microscopic, radiographic and biochemical evidence. Br J Nutr 1994, 71:919-932.
49. 6 deficient tarsometatarsal chick cartilage. Scanning Microsc 1990, 4:667-674.
50. Masse P.G., Rimnac C.M., Yamauchi M., Coburn P.S., Rucker B.R., Howell S.D., et al. Pyridoxine deficiency affects biomechanical properties of chick tibial bone. Bone 1996, 18:567-574.
51. Prockop D.J., Kivirikko K.I. Heritable diseases of collagen. N Engl J Med 1984, 311:376-396.
52. Golub L., Stern B., Glimcher M., Goldhaber P. The inhibition of the maturation of newly synthesized bone collagen by beta-aminopropionitrile in tissue culture. Proc Soc Exp Biol Med 1968, 129:465-469.
53. Golub L., Stern B., Glimcher M., Goldhaber P. The effect of a lathyrogenic agent on the synthesis and degradation of mouse bone collagen in tissue culture. Arch Oral Biol 1968, 13:1395-1398.
54. Golub L., Stern B., Glimcher M., Goldhaber P. The effect of lathyrism on bone collagen metabolism in tissue culture. J Periodontol 1968, 39:44-45.
55. Henneman D.H. Inhibition by estradiol-17 beta of the lathyritic effect of beta-aminopropionitrile (BAPN) on skin and bone collagen. Clin Orthop Relat Res 1972, 83:245-254.
56. Shimizu M., Golub L., Glimcher M. The effect of lathyrogens on the rate of collagen fibril formation and dissolution. Biochim Biophys Acta 1968, 168:356-358.
57. Paschalis E.P., Mendelsohn R., Boskey A.L. Infrared assessment of bone quality: a review. Clin Orthop Relat Res 2011, 469(8):2170-2178.
58. Bloebaum R., Skedros J., Vajda E., Bachus K., Constantz P. Determining mineral content variations in bone using backscattered electron imaging. Bone 1997, 20:485-490.
59. Donnelly E., Chen D.X., Boskey A.L., Baker S.P., van der Meulen M.C. Contribution of mineral to bone structural behavior and tissue mechanical properties. Calcif Tissue Int 2010, 87:450-460.
60. Camacho N.P., Rimnac C.M., Meyer R.A., Doty S., Boskey A.L. Effect of abnormal mineralization on the mechanical behavior of X-linked hypophosphatemic mice femora. Bone 1995, 17:271-278.
61. Courtland H.W., Nasser P., Goldstone A.B., Spevak L., Boskey A.L., Jepsen K.J. Fourier transform infrared imaging microspectroscopy and tissue-level mechanical testing reveal intraspecies variation in mouse bone mineral and matrix composition. Calcif Tissue Int 2008, 83:342-353.
62. Thaler R., Spitzer S., Rumpler M., Fratzl-Zelman N., Klaushofer K., Paschalis E.P., et al. Differential effects of homocysteine and beta aminopropionitrile on preosteoblastic MC3T3-E1 cells. Bone 2010, 46:703-709.
63. Turecek C., Fratzl-Zelman N., Rumpler M., Buchinger B., Spitzer S., Zoehrer R., et al. Collagen cross-linking influences osteoblastic differentiation. Calcif Tissue Int 2008, 82:392-400.
64. Chevalier Y., Pahr D., Zysset P.K. The role of cortical shell and trabecular fabric in finite element analysis of the human vertebral body. J Biomech Eng 2009, 131:111003.
65. Christiansen B.A., Kopperdahl D.L., Kiel D.P., Keaveny T.M., Bouxsein M.L. Mechanical contributions of the cortical and trabecular compartments contribute to differences in age-related changes in vertebral body strength in men and women assessed by QCT-based finite element analysis. J Bone Miner Res 2011, 26:974-983.
66. Melton L.J., Riggs B.L., Keaveny T.M., Achenbach S.J., Kopperdahl D., Camp J.J., et al. Relation of vertebral deformities to bone density, structure, and strength. J Bone Miner Res 2010, 25:1922-1930.
67. Szulc P., Boutroy S., Vilayphiou N., Chaitou A., Delmas P.D., Chapurlat R. Cross-sectional analysis of the association between fragility fractures and bone microarchitecture in older men: the STRAMBO study. J Bone Miner Res 2011, 26:1358-1367.
68. Vilayphiou N., Boutroy S., Szulc P., van Rietbergen B., Munoz F., Delmas P.D., et al. Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in men. J Bone Miner Res 2011, 26:965-973.
69. Wegrzyn J., Roux J.P., Arlot M.E., Boutroy S., Vilayphiou N., Guyen O., et al. Determinants of the mechanical behavior of human lumbar vertebrae after simulated mild fracture. J Bone Miner Res 2011, 26:739-746.
70. Cooper C., Melton L. Magnitude and impact of osteoporosis and fractures. Osteoporosis 1996, 425. Academic press Inc., London. R. Marcus, D. Feldman, J. Kelsey (Eds.).