Differences in matrix composition between calvaria and long bone in mice suggest differences in biomechanical properties and resorption. Special emphasis on collagen

Bone

Volumn 43, Issue 3, 2008, Pages 459-468

  van den Bos, T ^a   Speijer, D ^b   Bank, R A ^a,c   Bromme D ^d   Everts, V ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Bone mineralization; Collagen bone composition; Matrix proteins; Rodent

Indexed keywords

C REACTIVE PROTEIN; CATHEPSIN B; CATHEPSIN K; COLLAGEN; CYSTATIN; EDETIC ACID; FETUIN; FETUIN A; GELATINASE A; GLYCOPROTEIN; OSTEONECTIN; OSTEOPONTIN; PIGMENT EPITHELIUM DERIVED FACTOR; PROTEIN CHONDROCALCIN; PROTEIN HSPG 2; PROTEIN LYSINE 6 OXIDASE; PROTEIN OSTEOGLYCIN; PROTEIN SERPIN F1; PYRIDINOLINE; SECRETED PHOSPHOPROTEIN 24; TETRANECTIN; THROMBIN; THROMBOSPONDIN 1; UNCLASSIFIED DRUG; VITRONECTIN;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE MATRIX; BONE MINERAL; CALVARIA; CONTROLLED STUDY; CROSS LINKING; ENZYME ACTIVITY; FEMALE; FEMUR; LONG BONE; MASS SPECTROMETRY; MOUSE; NONHUMAN; OSTEOLYSIS; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN MOTIF; RADIUS; SOLUBILITY; TIBIA; TWO DIMENSIONAL GEL ELECTROPHORESIS; ULNA;

ANIMALS; BIOMECHANICS; BONE AND BONES; BONE RESORPTION; CALCIUM-BINDING PROTEINS; COLLAGEN; COLLAGEN TYPE II; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EYE PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MASS SPECTROMETRY; MICE; MODELS, BIOLOGICAL; NERVE GROWTH FACTORS; SERPINS; SKULL; STRESS, MECHANICAL; THROMBOSPONDINS;

EID: 49149110090     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2008.05.009     Document Type: Article

References (92)

1. Chung U.I., Kawaguchi H., Takato T., and Nakamura K. Distinct osteogenic mechanisms of bones of distinct origins. J Orthop Sci 9 (2004) 410-414
2. Sodek K.L., Tupy J.H., Sodek J., and Grynpas M.D. Relationships between bone protein and mineral in developing porcine long bone and calvaria. Bone 26 (2000) 189-198
3. Ninomiya J.T., Tracy R.P., Calore J.D., Gendreau M.A., Kelm R.J., and Mann K.G. Heterogeneity of human bone. J Bone Miner Res 5 (1990) 933-938
4. Finkelman R.D., Eason A.L., Rakijian D.R., Tutundzhyan Y., and Hardesty R.A. Elevated IGF-II and TGF-beta concentrations in human calvarial bone: potential mechanism for increased graft survival and resistance to osteoporosis. Plast Reconstr Surg 93 (1994) 732-738
5. Kasperk C., Wergedal J., Strong D., Farley J., Wangerin K., Gropp H., et al. Human bone cell phenotypes differ depending on their skeletal site of origin. J Clin Endocrinol Metab 80 (1995) 2511-2517
6. Malpe R., Baylink D.J., Linkhart T.A., Wergedal J.E., and Mohan S. Insulin-like growth factor (IGF)-I, -II, IGF binding proteins (IGFBP)-3, -4, and -5 levels in the conditioned media of normal human bone cells are skeletal site-dependent. J Bone Miner Res 12 (1997) 423-430
7. Fisher L.W., Termine J.D., Dejter Jr. S.W., Whitson S.W., Yanagishita M., Kimura J.H., et al. Proteoglycans of developing bone. J Biol Chem 258 (1983) 6588-6594
8. Chen J., Shapiro H.S., and Sodek J. Development expression of bone sialoprotein mRNA in rat mineralized connective tissues. J Bone Miner Res 7 (1992) 987-997
9. Mizoguchi I., Takahashi I., Sasano Y., Kagayama M., Kuboki Y., and Mitani H. Localization of types I, II and X collagen and osteocalcin in intramembranous, endochondral and chondroid bone of rats. Anat Embryol (Berl) 196 (1997) 291-297
10. Suttapreyasri S., Koontongkaew S., Phongdara A., and Leggat U. Expression of bone morphogenetic proteins in normal human intramembranous and endochondral bones. Int J Oral Maxillofac Surg 35 (2006) 444-452
11. Fujii T., Ueno T., Kagawa T., Sakata Y., and Sugahara T. Comparison of bone formation ingrafted periosteum harvested from tibia and calvaria. Microsc Res Tech 69 (2006) 580-584
12. Rabie A.B., Dan Z., and Samman N. Ultrastructural identification of cells involved in the healing of intramembranous and endochondral bones. Int J Oral Maxillofac Surg 25 (1996) 383-388
13. Scott C.K., and Hightower J.A. The matrix of endochondral bone differs from the matrix of intramembranous bone. Calcif Tissue Int 49 (1991) 349-354
14. Matsubara T., Suardita K., Ishii M., Sugiyama M., Igarashi A., Oda R., et al. Alveolar bone marrow as a cell source for regenerative medicine: differences between alveolar and iliac bone marrow stromal cells. J Bone Miner Res 20 (2005) 399-409
15. Akintoye S.O., Lam T., Shi S., Brahim J., Collins M.T., and Robey P.G. Skeletal site-specific characterization of orofacial and iliac crest human bone marrow stromal cells in same individuals. Bone 38 (2006) 758-768
16. Everts V., Korper W., Jansen D.C., Steinfort J., Lammerse I., Heera S., et al. Functional heterogeneity of osteoclasts: matrix metalloproteinases participate in osteoclastic resorption of calvarial bone but not in resorption of long bone. FASEB J 13 (1999) 1219-1230
17. Shorey S., Heersche J.N., and Manolson M.F. The relative contribution of cysteine proteinases and matrix metalloproteinases to the resorption process in osteoclasts derived from long bone and scapula. Bone 35 (2004) 909-917
18. Lecanda F., Warlow P.M., Sheikh S., Furlan F., Steinberg T.H., and Civitelli R. Connexin43 deficiency causes delayed ossification, craniofacial abnormalities, and osteoblast dysfunction. J Cell Biol 151 (2000) 931-944
19. Saftig P., Hunziker E., Wehmeyer O., Jones S., Boyde A., Rommerskirch W., et al. Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci U S A 95 (1998) 13453-13458
20. Gowen M., Lazner F., Dodds R., Kapadia R., Feild J., Tavaria M., et al. Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J Bone Miner Res 14 (1999) 1654-1663
21. Chen W., Yang S., Abe Y., Li M., Wang Y., Shao J., et al. Novel pycnodysostosis mouse model uncovers cathepsin K function as a potential regulator of osteoclast apoptosis and senescence. Hum Mol Genet 16 (2007) 410-423
22. Vu T.H., Shipley J.M., Bergers G., Berger J.E., Helms J.A., Hanahan D., et al. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93 (1998) 411-422
23. Segev O., Chumakov I., Nevo Z., Givol D., Madar-Shapiro L., Sheinin Y., et al. Restrained chondrocyte proliferation and maturation with abnormal growth plate vascularization and ossification in human FGFR-3(G380R) transgenic mice. Hum Mol Genet 9 (2000) 249-258
24. Takeuchi S., Takeda K., Oishi I., Nomi M., Ikeya M., Itoh K., et al. Mouse Ror2 receptor tyrosine kinase is required for the heart development and limb formation. Genes Cells 5 (2000) 71-78
25. Lomaga M.A., Yeh W.C., Sarosi I., Duncan G.S., Furlonger C., Ho A., et al. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev 13 (1999) 1015-1024
26. St Jacques B., Hammerschmidt M., and McMahon A.P. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13 (1999) 2072-2086
27. Wang Y., Wan C., Deng L., Liu X., Cao X., Gilbert S.R., et al. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest 117 (2007) 1616-1626
28. Tiziani V., Reichenberger E., Buzzo C.L., Niazi S., Fukai N., Stiller M., et al. The gene for cherubism maps to chromosome 4p16. Am J Hum Genet 65 (1999) 158-166
29. Stiller M., Urban M., Golder W., Tiziani V., Reichenberger E., Frege J., et al. Craniosynostosis in cherubism. Am J Med Genet 95 (2000) 325-331
30. Ueki Y., Tiziani V., Santanna C., Fukai N., Maulik C., Garfinkle J., et al. Mutations in the gene encoding c-Abl-binding protein SH3BP2 cause cherubism. Nat Genet 28 (2001) 125-126
31. Carpten J.D., Robbins C.M., Villablanca A., Forsberg L., Presciuttini S., Bailey-Wilson J., et al. HRPT2, encoding parafibromin, is mutated in hyperparathyroidism-jaw tumor syndrome. Nat Genet 32 (2002) 676-680
32. Alban A., David S.O., Bjorkesten L., Andersson C., Sloge E., Lewis S., et al. A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 3 (2003) 36-44
33. Marouga R., David S., and Hawkins E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bioanal Chem 382 (2005) 669-678
34. Mortz E., Krogh T.N., Vorum H., and Gorg A. Improved silver staining protocols for high sensitivity protein identification using matrix-assisted laser desorption/ionization-time of flight analysis. Proteomics 1 (2001) 1359-1363
35. Shevchenko A., Sunyaev S., Loboda A., Shevchenko A., Bork P., Ens W., et al. Charting the proteomes of organisms with unsequenced genomes by MALDI-quadrupole time-of-flight mass spectrometry and BLAST homology searching. Anal Chem 73 (2001) 1917-1926
36. Stegemann H., and Stalder K. Determination of hydroxyproline. Clin Chim Acta 18 (1967) 267-273
37. Bank R.A., Beekman B., Verzijl N., de Roos J.A., Sakkee A.N., and TeKoppele J.M. Sensitive fluorimetric quantitation of pyridinium and pentosidine crosslinks in biological samples in a single high-performance liquid chromatographic run. J Chromatogr B Biomed Sci Appl 703 (1997) 37-44
38. Hess H.H., and Derr J.E. Assay of inorganic and organic phosphorus in the 0.1-5 nanomole range. Anal Biochem 63 (1975) 607-613
39. Wassen M.H., Lammens J., TeKoppele J.M., Sakkers R.J., Liu Z., Verbout A.J., et al. Collagen structure regulates fibril mineralization in osteogenesis as revealed by cross-link patterns in calcifying callus. J Bone Miner Res 15 (2000) 1776-1785
40. Li Z., Yasuda Y., Li W., Bogyo M., Katz N., Gordon R.E., et al. Regulation of collagenase activities of human cathepsins by glycosaminoglycans. J Biol Chem 279 (2004) 5470-5479
41. Murray E.J., Simon R., Murray S.S., and Behnam K. Recombinant expression, isolation and proteolysis of extracellular matrix secreted phosphoprotein-24 kDa. Connect Tissue Res 48 (2007) 292-299
42. Delmas P.D., Tracy R.P., Riggs B.L., and Mann K.G. Identification of the noncollagenous proteins of bovine bone by two-dimensional gel electrophoresis. Calcif Tissue Int 36 (1984) 308-316
43. Funderburgh J.L., Corpuz L.M., Roth M.R., Funderburgh M.L., Tasheva E.S., and Conrad G.W. Mimecan, the 25-kDa corneal keratan sulfate proteoglycan, is a product of the gene producing osteoglycin. J Biol Chem 272 (1997) 28089-28095
44. Tasheva E.S., Koester A., Paulsen A.Q., Garrett A.S., Boyle D.L., Davidson H.J., et al. Mimecan/osteoglycin-deficient mice have collagen fibril abnormalities. Mol Vis 8 (2002) 407-415
45. Wang X., Ford B.C., Praul C.A., and Leach Jr. R.M. Characterization of the non-collagenous proteins in avian cortical and medullary bone. Comp Biochem Physiol B Biochem Mol Biol 140 (2005) 665-672
46. Xing W., Baylink D., Kesavan C., Hu Y., Kapoor S., Chadwick R.B., et al. Global gene expression analysis in the bones reveals involvement of several novel genes and pathways in mediating an anabolic response of mechanical loading in mice. J Cell Biochem 96 (2005) 1049-1060
47. Duncan R.L., and Turner C.H. Mechanotransduction and the functional response of bone to mechanical strain. Calcif Tissue Int 57 (1995) 344-358
48. Becerra S.P. Structure-function studies on PEDF. A noninhibitory serpin with neurotrophic activity. Adv Exp Med Biol 425 (1997) 223-237
49. Tombran-Tink J., and Barnstable C.J. Osteoblasts and osteoclasts express PEDF, VEGF-A isoforms, and VEGF receptors: possible mediators of angiogenesis and matrix remodeling in the bone. Biochem Biophys Res Commun 316 (2004) 573-579
50. Doll J.A., Stellmach V.M., Bouck N.P., Bergh A.R., Lee C., Abramson L.P., et al. Pigment epithelium-derived factor regulates the vasculature and mass of the prostate and pancreas. Nat Med 9 (2003) 774-780
51. Quan G.M., Ojaimi J., Li Y., Kartsogiannis V., Zhou H., and Choong P.F. Localization of pigment epithelium-derived factor in growing mouse bone. Calcif Tissue Int 76 (2005) 146-153
52. Ek E.T., Dass C.R., Contreras K.G., and Choong P.F. Inhibition of orthotopic osteosarcoma growth and metastasis by multitargeted antitumor activities of pigment epithelium-derived factor. Clin Exp Metastasis 24 (2007) 93-106
53. Bornstein P., Agah A., and Kyriakides T.R. The role of thrombospondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury. Int J Biochem Cell Biol 36 (2004) 1115-1125
54. Grzesik W.J., and Robey P.G. Bone matrix RGD glycoproteins: immunolocalization and interaction with human primary osteoblastic bone cells in vitro. J Bone Miner Res 9 (1994) 487-496
55. Robey P.G., Young M.F., Fisher L.W., and McClain T.D. Thrombospondin is an osteoblast-derived component of mineralized extracellular matrix. J Cell Biol 108 (1989) 719-727
56. Schultz-Cherry S., and Murphy-Ullrich J.E. Thrombospondin causes activation of latent transforming growth factor-beta secreted by endothelial cells by a novel mechanism. J Cell Biol 122 (1993) 923-932
57. Adams J.C., and Lawler J. Diverse mechanisms for cell attachment to platelet thrombospondin. J Cell Sci 104 Pt 4 (1993) 1061-1071
58. Murphy-Ullrich J.E., Gurusiddappa S., Frazier W.A., and Hook M. Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity. J Biol Chem 268 (1993) 26784-26789
59. Crawford S.E., Stellmach V., Murphy-Ullrich J.E., Ribeiro S.M.F., Lawler J., Hynes R.O., et al. Thrombospondin-1 is a major activator of TGF-beta 1 in vivo. Cell 93 (1998) 1159-1170
60. Jimenez B., Volpert O.V., Crawford S.E., Febbraio M., Silverstein R.L., and Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6 (2000) 41-48
61. Choi H.U., Tang L.H., Johnson T.L., Pal S., Rosenberg L.C., Reiner A., et al. Isolation and characterization of a 35,000 molecular weight subunit fetal cartilage matrix protein. J Biol Chem 258 (1983) 655-661
62. Van der R.M., Rosenberg L.C., Olsen B.R., and Poole A.R. Chondrocalcin is identical with the C-propeptide of type II procollagen. Biochem J 237 (1986) 923-925
63. Poole A.R., Reiner A., Mort J.S., Tang L.H., Choi H.U., Rosenberg L.C., et al. Cartilage link proteins. Biochemical and immunochemical studies of isolation and heterogeneity. J Biol Chem 259 (1984) 14849-14856
64. Kujawa M.J., Weitzhandler M., Poole A.R., Rosenberg L., and Caplan A.I. Association of the C-propeptide of type II collagen with mineralization of embryonic chick long bone and sternal development. Connect Tissue Res 23 (1989) 179-199
65. Alberius P., and Johnell O. Immunohistochemical assessment of cranial suture development in rats. J Anat 173 (1990) 61-68
66. Nah H.D., Pacifici M., Gerstenfeld L.C., Adams S.L., and Kirsch T. Transient chondrogenic phase in the intramembranous pathway during normal skeletal development. J Bone Miner Res 15 (2000) 522-533
67. Hu B., Coulson L., Moyer B., and Price P.A. Isolation and molecular cloning of a novel bone phosphoprotein related in sequence to the cystatin family of thiol protease inhibitors. J Biol Chem 270 (1995) 431-436
68. Bennett C.S., Khorram Khorshid H.R., Kitchen J.A., Arteta D., and Dalgleish R. Characterization of the human secreted phosphoprotein 24 gene (SPP2) and comparison of the protein sequence in nine species. Matrix Biol 22 (2004) 641-651
69. Ritonja A., Kopitar M., Jerala R., and Turk V. Primary structure of a new cysteine proteinase inhibitor from pig leucocytes. FEBS Lett 255 (1989) 211-214
70. Salvesen G., Parkes C., Abrahamson M., Grubb A., and Barrett A.J. Human low-Mr kininogen contains three copies of a cystatin sequence that are divergent in structure and in inhibitory activity for cysteine proteinases. Biochem J 234 (1986) 429-434
71. Verbanac D., Zanetti M., and Romeo D. Chemotactic and protease-inhibiting activities of antibiotic peptide precursors. FEBS Lett 317 (1993) 255-258
72. Brage M., Abrahamson M., Lindstrom V., Grubb A., and Lerner U.H. Different cysteine proteinases involved in bone resorption and osteoclast formation. Calcif Tissue Int 76 (2005) 439-447
73. Brand H.S., Lerner U.H., Grubb A., Beertsen W., Nieuw Amerongen A.V., and Everts V. Family 2 cystatins inhibit osteoclast-mediated bone resorption in calvarial bone explants. Bone 35 (2004) 689-696
74. Price P.A., Nguyen T.M., and Williamson M.K. Biochemical characterization of the serum fetuin-mineral complex. J Biol Chem 278 (2003) 22153-22160
75. Sintuu C., Murray S.S., Behnam K., Simon R., Jawien J., Silva J.D., Duarte M.E., and Brochmann E.J. Full-length bovine spp24 [spp24(24-203)] inhibits BMP-2 induced bone formation. J Orthop Res 26 (2008) 753-758
76. Schinke T., Amendt C., Trindl A., Poschke O., Muller-Esterl W., and Jahnen-Dechent W. The serum protein alpha2-HS glycoprotein/fetuin inhibits apatite formation in vitro and in mineralizing calvaria cells. A possible role in mineralization and calcium homeostasis. J Biol Chem 271 (1996) 20789-20796
77. Binkert C., Demetriou M., Sukhu B., Szweras M., Tenenbaum H.C., and Dennis J.W. Regulation of osteogenesis by fetuin. J Biol Chem 274 (1999) 28514-28520
78. Jahnen-Dechent W., Schinke T., Trindl A., Muller-Esterl W., Sablitzky F., Kaiser S., et al. Cloning and targeted deletion of the mouse fetuin gene. J Biol Chem 272 (1997) 31496-31503
79. Schafer C., Heiss A., Schwarz A., Westenfeld R., Ketteler M., Floege J., et al. The serum protein alpha 2-Heremans-Schmid glycoprotein/fetuin-A is a systemically acting inhibitor of ectopic calcification. J Clin Invest 112 (2003) 357-366
80. Elzanowski A., Barker W.C., Hunt L.T., and Seibel-Ross E. Cystatin domains in alpha-2-HS-glycoprotein and fetuin. FEBS Lett 227 (1988) 167-170
81. Sodek J., Ganss B., and McKee M.D. Osteopontin. Crit Rev Oral Biol Med 11 (2000) 279-303
82. Brekken R.A., and Sage E.H. SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol 19 (2001) 816-827
83. Lerner U.H., and Gustafson G.T. Blood coagulation and bone metabolism: some characteristics of the bone resorptive effect of thrombin in mouse calvarial bones in vitro. Biochim Biophys Acta 964 (1988) 309-318
84. Currey J.D., Brear K., and Zioupos P. The effects of ageing and changes in mineral content in degrading the toughness of human femora. J Biomech 29 (1996) 257-260
85. 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
86. Uchiyama A., Inoue T., and Fujimoto D. Synthesis of pyridinoline during in vitro aging of bone collagen. J Biochem (Tokyo) 90 (1981) 1795-1798
87. Vater C.A., Harris Jr. E.D., and Siegel R.C. Native cross-links in collagen fibrils induce resistance to human synovial collagenase. Biochem J 181 (1979) 639-645
88. Garnero P., Borel O., Byrjalsen I., Ferreras M., Drake F.H., McQueney M.S., et al. The collagenolytic activity of cathepsin K is unique among mammalian proteinases. J Biol Chem 273 (1998) 32347-32352
89. Everts V., Korper W., Hoeben K.A., Jansen I.D., Bromme D., Cleutjens K.B., et al. Osteoclastic bone degradation and the role of different cysteine proteinases and matrix metalloproteinases: differences between calvaria and long bone. J Bone Miner Res 21 (2006) 1399-1408
90. Viguet-Carrin S., Garnero P., and Delmas P.D. The role of collagen in bone strength. Osteoporos Int 17 (2006) 319-336
91. 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
92. Li X.Q., and Klein L. Decreasing rates of bone resorption in growing rats in vivo: comparison of different types of bones. Bone 11 (1990) 95-101