Defects in articular cartilage metabolism and early arthritis in fibroblast growth factor receptor 3 deficient mice

Human Molecular Genetics

Volumn 15, Issue 11, 2006, Pages 1783-1792

  Valverde Franco, G ^a   Binette, J S ^a   Li, W ^a   Wang, H ^a   Chai, S ^a   Laflamme, F ^b   Tran Khanh, N ^b   Quenneville, E ^b   Meijers, T ^c   Poole, A R ^a   Mort, J S ^a   Buschmann, M D ^a   Henderson, Janet E ^a  

^a MCGILL UNIVERSITY   (Canada)

^b ÉCOLE POLYTECHNIQUE DE MONTRÉAL   (Canada)

^c TNO   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; COLLAGEN TYPE 10; COLLAGEN TYPE 2; COLLAGENASE 3; CORE PROTEIN; EPITOPE; FIBROBLAST GROWTH FACTOR RECEPTOR 3; PROTEOGLYCAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE DEGENERATION; CARTILAGE MATRIX; CELL STRUCTURE; COMPRESSION; CONTROLLED STUDY; GENETIC PROCEDURES; HUMERUS HEAD; HYPERTROPHY; IMMUNOREACTIVITY; MOUSE; NONHUMAN; PHYSICAL RESISTANCE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN TARGETING; RIGIDITY; SIGNAL TRANSDUCTION; SYNOVIUM; TISSUE METABOLISM;

AGGRECANS; ANIMALS; ARTHRITIS; CARTILAGE; CARTILAGE DISEASES; CARTILAGE, ARTICULAR; CHONDROCYTES; COLLAGEN TYPE II; COLLAGEN TYPE X; COLLAGENASES; CROSSES, GENETIC; EPITOPES; EXTRACELLULAR MATRIX PROTEINS; LECTINS, C-TYPE; MATRIX METALLOPROTEINASE 13; MICE; MICE, TRANSGENIC; OSTEOBLASTS; PROTEOCHONDROITIN SULFATES; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; SIGNAL TRANSDUCTION;

EID: 33744763965     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddl100     Document Type: Article

References (57)

1. Poole, A.R. (1993) Cartilage in health and disease. In McCarty, D.J. and Koopman, W.J. (eds), Arthritis and Allied Conditions: A Textbook of Rheumatology. Lea & Febiger, Philadelphia, pp. 279-333.
2. Poole, A.R., Laverty, S. and Mwale, F. (2000) Endochondral bone formation and development in the axial and appendicular skeleton. In Henderson, J.E. and Goltzman, D. (eds), The Osteoporosis Primer. Cambridge University Press, Cambridge, UK, pp. 3-17.
3. Kronenberg, H. (2003) Developmental regulation of the growth plate. Nature, 423, 332-336.
4. Hunziker, E.B. (2002) Articular cartilage repair: Basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage, 10, 432-463.
5. Solchaga, L.A., Goldberg, V.M. and Caplan, A.I. (2001) Experimental models of cartilage repair: Cartilage regeneration using principles of tissue engineering. Clin. Orthop., 391S, S161-S170.
6. Korblin, M. and Estrov, Z. (2003) Adult stem cells for tissue repair: A new theraputic concept. N. Engl. J. Med., 349, 570-582.
7. Dowthwaite, G.P., Bishop, J.C., Redman, S.N., Khan, I.M., Rooney, P., Evans, D.J.R., Haughton, L., Bayram, Z., Boyer, S., Thomson, B., Wolfe, M.S. and Archer, C.W. (2003) The surface of articular cartilage contains a progenitor cell population. J. Cell. Sci., 117, 889-897.
8. Ochi, M., Adachi, N., Nobutu, H., Yanada, S., Ito, Y. and Agung, M. (2004) Articular cartilage repair using tissue engineering technique-novel approach with minimally invasive procedure. Artif. Organs, 28, 28-32.
9. Reddi, A.H. (2003) Cartilage morphogenetic proteins: Role in joint development, homoeostasis, and regeneration. Ann. Rheum. Dis., 62, 73-78.
10. Issack, P.S. and DiCesare, P.E. (2003) Recent advances toward the clinical application of bone morphogenetic proteins in bone and cartilage repair. Am. J. Orthop., 32, 429-436.
11. Li, W.J., Tuli, R., Okafor, C., Derfoul, A., Danielson, K.G., Hall, D.J. and Tuan, R.S. (2005) A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials, 26, 599-609.
12. Sekiya, I., Larson, B.L., Vuoristo, J.T., Reger, R.L. and Prockop, D.J. (2005) Comparison of effect of BMP-2, -4 and -6 on in vitro cartilage formation of human adult stem cells from bone marrow stroma. Cell Tissue Res., 320, 269-276.
13. Barbero, A., Grogan, S., Schafer, D., Heberer, M., Mainil-Varlet, P. and Martin, I. (2004) Age related changes in human articular chondrocyte yield, proliferation and post-expansion chondrogenic capacity. Osteoarthritis Cartilage, 12, 476-484.
14. Henson, F.M., Bowie, E.A. and Davies, M.E. (2005) Promotion of the intrinsic damage-repair response in articular cartilage by fibroblastic growth factor-2. Osteoarthritis Cartilage, 13, 537-544.
15. Madry, H., Emkey, G., Zurakowski, D. and Trippel, S.B. (2004) Overexpression of human fibroblast growth factor 2 stimulates cell proliferation in an ex vivo model of articular chondrocyte transplantation. J. Gene Med., 6, 238-245.
16. Stevens, M.M., Marini, R.P., Martin, I., Langer, R. and Prasad Shastri, V. (2004) FGF-2 enhances TGF-beta1-induced periosteal chondrogenesis. J. Orthop. Res., 22, 1114-1119.
17. Veilleux, N. and Spector, M. (2005) Effects of FGF-2 and IGF-1 on adult canine articular chondrocytes in type II collagen-glycosaminoglycan scaffolds in vitro. Osteoarthritis Cartilage, 13, 278-286.
18. Ornitz, D.M. and Marie, P.J. (2002) FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev., 16, 1446-1465.
19. Naski, M.C., Colvin, J., Coffin, J. and Ornitz, D.M. (1998) Repression of hedgehog signalling and BMP4 expression in growth plate cartilage by fibroblast growth factor receptor 3. Development, 125, 4977-4988.
20. Li, C., Chen, L., Iwata, T., Kitagawa, M., Fu, X.-Y. and Deng, C.-X. (1999) A Lys644Glu substitution in fibroblast growth factor receptor 3 (FGFR3) causes dwarfism in mice by activation of STATs and Ink4 cell cycle inhibitors. Hum. Mel. Genet., 8, 35-44.
21. Bellus, G.A., Bamshad, M.J., Przylepa, K.A., Dorst, J., Lee, R.R., Hurko, O., Jabs, E.W., Curry, C.J.R., Wilcox, W.R., Lachman, R.S., Rimoin, D.L. and Francomano, C.A. (1999) Severe achondroplasia with developmental delay and acanthosis nigricans (SADDAN). Am. J. Med. Genet., 85, 53-65.
22. Iwata, T., Li, C.-L., Deng, C.-X. and Francomano, C. (2001) Highly activated FGFR3 with the K644M mutation causes prolonged survival in severe dwarf mice. Hum. Mol. Genet., 10, 1255-1264.
23. Colvin, J.S., Bohne, B.A., Harding, G.W., McEwen, D.G. and Ornitz, D.M. (1996) Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nat. Genet., 12, 390-397.
24. Valverde-Franco, G., Liu, H., Davidson, D., Chai, S., Carvajal, H.V., Goltzman, D., Ornitz, D.M. and Henderson, J.E. (2004) Defective bone mineralization and osteopenia in young adult FGFR3-/- mice. Hum. Mol. Genet., 13, 271-284.
25. Liu, Z., Xu, J., Colvin, J.S. and Ornitz, D.M. (2002) Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev., 16, 859-869.
26. Ohbayashi, N., Shibayama, M., Kurotaki, Y., Imanishi, M., Fujimori, T., Itoh, N. and Takada, S. (2002) FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev., 16, 870-879.
27. Davidson, D., Blanc, A., Filion, D., Wang, H., Plut, P., Pfeffer, G., Buschmann, M.D. and Henderson, J.E. (2005) FGF18 signals through FGFR3 to promote chondrogenesis. J. Biol. Chem., 280, 20509-20515.
28. Ellsworth, J.L., Berry, J., Bukowski, T., Claus, J., Feldhaus, A., Holderman, S., Holdren, M.S., Lum, K.D., Moore, E.E., Raymond, F. et al. (2002) Fibroblast growth factor-18 is a trophic factor for mature chondrocytes and their progenitors. Osteoarthritis Cartilage, 10, 308-320.
29. D'Angelo, M., Yan, Z., Nooreyazdan, M., Pacifici, M., Sarment, D.S., Billings, P.C. and Leboy, P.S. (2000) MMP-13 is induced during chondrcyte hypertrophy. J. Cell. Biochem., 77, 678-693.
30. Fortin, M., Soulhat, J., Sirazi-Adl, A., Hunziker, E.B. and Buschmann, M.D. (2000) Unconfined compression of articular cartilage: Nonlinear behaviour and comparison with a fibril-reinforced biphasic model. J. Biomech. Eng., 122, 189-195.
31. Hyttinen, M.M., Toyras, J., Lapvetelainen, T., Lindblom, J., Prockop, D.J., Li, S.W., Arita, M., Jurvelin, J.S. and Helminen, H.J. (2001) Inactivation of one allele of the type II collagen gene alters the collagen network in murine articular cartilage and makes cartilage softer. Ann. Rheum. Dis., 60, 262-268.
32. Hunter, D.J., Zhang, Y., Niu, J., Tu, X., Amin, S., Goggins, J., Lavalley, M., Guermazi, A., Gale, D. and Felson, D.T. (2005) Structural factors associated with malalignment in knee osteoarthritis: The Boston osteoarthritis knee study. J. Rheumatol., 32, 2192-2199.
33. Scharstuhl, A., Glansbeek, H.L., van Beuningen, H., Vitters, E.L., van der Kraan, P. and van der Berg, W. (2002) Inhibition of endogenous TGFb during experimental osteoarthritis prevents osteophyte formation and impairs cartilage repair. J. Immunol., 169, 507-514.
34. Zhang, Y.W., Su, Y., Lanning, N., Swiatek, P.J., Bronson, R.T., Sigler, R., Martin, R.W. and vandeWoude, G.F. (2005) Targeted disruption of Mig-6 in the mouse genome leads to early onset degenerative joint disease. Proc. Natl Acad. Sci. (USA), 102, 11740-11745.
35. Walsh, N.C. and Gravallese, E.M. (2004) Bone loss in inflammatory arthritis: Mechanisms and treatment strategies. Curr. Opin. Rheumatol., 16, 419-426.
36. Lajeunesse, D. and Reboul, P. (2003) Subchondral bone in osteoarthritis: a biologic link with articular cartilage leading to abnormal remodeling. Curr. Opin. Rheumatol., 15, 628-633.
37. Garnero, P. and Delmas, P.D. (2004) Noninvasive techniques for assessing skeletal changes in inflammatory arthritis: Bone biomarkers. Curr. Opin. Rheumatol., 16, 428-434.
38. Vortkamp, A., Lee, K., Lanske, B., Segre, G.V., Kronenberg, H.M. and Tabin, C.J. (1996) Regulation of the rate of cartilage differentiation by Indian Hedgehog and PTH-related protein. Science, 273, 613-622.
39. Kobayashi, T., Chung, U., Schipani, E., Starbuck, M., Karsenty, G., Katagiri, T., Goad, D., Lanske, B. and Kronenberg, H. (2002) PTHrP and Indian hedgehog control differentiation of growth plate chondrocytes at multiple steps. Development, 129, 2977-2986.
40. Amizuka, N., Davidson, D., Liu, H., Valverde-Franco, G., Chai, S., Sasaki, T., Ozawa, H., Hammond, V., Ornitz, D.M., Goltzman, D. and Henderson, J.E. (2003) Signaling by fibroblast growth factor receptor 3 (FGFR3) and parathyroid hormone related protein (PTHrP) coordinate cartilage and bone development. Bone, 34, 13-25.
41. Poole, A.R., Kojima, T., Yasuda, T., Mwale, F., Kobayashi, M. and Laverty, S. (2001) Cartilage biology: Composition and structure of articular cartilage. Clin. Orthop., 391S, S26-S33.
42. Deng, C., Wynshaw-Boris, A., Zhou, F., Kuo, A. and Leder, P. (1996) Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell, 84, 911-921.
43. Billinhurst, R.C., Dahlberg, L., Ionescu, M., Reiner, A., Bourne, R., Rorabeck, C., Mitchell, P., Hambor, J., Diekmann, O., Tschesche, H. et al. (1997) Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J. Clin. Invest., 99, 1534-1545.
44. Hughes, C.E., Caterson, B., Fosang, A.J., Roughly, P.J. and Mort, J.S. (1995) Monoclonal antibodies that specifically recognize neoepitope sequences generated by 'aggrecanase' and matrix metalloproteinase cleavage of aggrecan: Application to catabolism in situ and in vitro. Biochem. J., 305, 799-804.
45. Neuhold, L.A., Killar, L., Zhao, W., Sung, M.L.A., Warner, L., Kulik, J., Turner, J., Wu, W., Billinghurst, C., Meijers, T. et al. (2001) Postnatal expression in hyaline cartilage of constitutively active human collagenase-3 (MMP-13) induces osteoarthritis in mice. J. Clin. Invest, 107, 35-44.
46. Ornitz, D.M. and Leder, P. (1992) Ligand specificity and heparin dependence of fibroblast growth factor receptors 1 and 3. J. Biol. Chem., 267, 16305-16311.
47. Shimoaka, T., Ogasawara, T., Yonamine, A., Chikazu, D., Kawano, H., Nakamura, K., Itoh, N. and Kawaguchi, H. (2002) Regulation of osteoblast, chondrocyte and osteoclast functions by fibroblast growth factor (FGF) 18 in comparison with FGF2 and FGF10. J. Biol. Chem., 277, 7493-7500.
48. Orito, K., Koshino, T. and Saito, T. (2003) Fibroblast growth factor 2 in synovial fluid from an osteoarthritic knee with cartilage regeneration. J. Orthop. Sci., 8, 294-300.
49. Wang, X., Manner, P.A., Horner, A., Shum, L., Tuan, R.S. and Nuckolls, G.H. (2004) Regulation of MMP-13 expression by RUNX2 and FGF2 in osteoarthritic cartilage. Osteoarthritis Cartilage, 12, 963-973.
50. Colnot, C., Thompson, X., Miclau, T., Werb, Z. and Helms, J.A. (2003) Altered fracture repair in the absence of MMP9. Development, 130, 4123-4133.
51. Vasara, A.L., Jurvelin, J.S., Peterson, L. and Kiviranta, I. (2005) Arthroscopic cartilage indentation and cartilage lesions of anterior cruciate ligament-deficient knees. Am. J. Sports Med., 33, 408-414.
52. Niederauer, G.G., Niederauer, G.M., Cullen, L.C., Athanasiou, K.A., Thomas, J.B. and Niederauer, M.Q. (2004) Correlation of cartilage stiffness to thickness and level of degeneration using a handheld indentation probe. Ann. Biomed. Eng., 32, 352-359.
53. Samosky, J.T., Burstein, D., Grimson, W.E., Howe, R., Martin, S. and Gray, M.L. (2005) Spatially-localized correlation of dGEMRIC-measured GAG distribution and mechanical stiffness in the human tibial plateau. J. Orthop. Res., 23, 93-101.
54. Jurvelin, J., Kiviranta, I., Tammi, M. and Helminen, J.H. (1986) Softening of canine articular cartilage after immobilization of the knee joint. Clin. Orthop., 207, 246-252.
55. Tran-Khan, N., Hoemann, C.D., McKee, M.D., Henderson, J.E. and Buschmann, M.D. (2005) Aged bovine chondrocytes display a diminshed capacity to produce a collagen-rich, mechanically functional cartilage extracellular matrix. J. Orthop. Res., 23, 1354-1362.
56. vanderKraan, P.M., Vitters, E.L., Meijers, T.H., Poole, A.R. and vandenBerg, W.B. (1998) Collagen type I antisense and collagen type IIA messenger RNA is expressed in adult murine articular cartilage. Osteoarthritis Cartilage, 6, 417-426.
57. Poole, A.R., Ionescu, M., Fitzcharles, M.A. and Billinghurst, R.C. (2004) The assessment of cartilage degradation in vivo: Development of an immunoassay for the measurement in body fluids of type II collagen cleaved by collagenases. J. Immunol. Methods, 294, 145-153.