Cartilage oligomeric matrix protein and its binding partners in the cartilage extracellular matrix: Interaction, regulation and role in chondrogenesis

Matrix Biology

Volumn 37, Issue , 2014, Pages 102-111

  Acharya, Chitrangada ^a   Yik, Jasper H N ^a   Kishore, Ashleen ^a   Van Dinh, Victoria ^a   Di Cesare, Paul E ^b   Haudenschild, Dominik R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NEW YORK HOSPITAL QUEENS   (United States)

Author keywords

Cartilage oligomeric matrix protein; Complement system; Extracellular matrix; Growth factors; Proteases; Receptors

Indexed keywords

CARTILAGE OLIGOMERIC MATRIX PROTEIN; CELL PROTEIN; GROWTH FACTOR; PROTEIN BINDING; SCLEROPROTEIN;

ACHONDROPLASIA; ARTICLE; BONE DISEASE; BONE DYSPLASIA; CELL FUNCTION; CHONDROGENESIS; EXTRACELLULAR MATRIX; HUMAN; HYDROPHOBICITY; PROTEIN BINDING; PROTEIN INTERACTION; REGULATORY MECHANISM; BIOLOGICAL MODEL; GENETICS; METABOLISM; MUSCULOSKELETAL SYSTEM MALFORMATION; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN TERTIARY STRUCTURE;

CARTILAGE OLIGOMERIC MATRIX PROTEIN; CHONDROGENESIS; EXTRACELLULAR MATRIX PROTEINS; HUMANS; MODELS, BIOLOGICAL; MUSCULOSKELETAL ABNORMALITIES; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY;

EID: 84908349797     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2014.06.001     Document Type: Review

References (97)

1. Adams J.C. Thrombospondins: multifunctional regulators of cell interactions. Annu. Rev. Cell Dev. Biol. 2001, 17:25-51.
2. Agah A., Kyriakides T.R., Lawler J., Bornstein P. The lack of thrombospondin-1 (TSP1) dictates the course of wound healing in double-TSP1/TSP2-null mice. Am. J. Pathol. 2002, 161:831-839.
3. Agarwal P., Zwolanek D., Keene D.R., Schulz J.N., Blumbach K., Heinegard D., Zaucke F., Paulsson M., Krieg T., Koch M., Eckes B. Collagen XII and XIV, new partners of cartilage oligomeric matrix protein in the skin extracellular matrix suprastructure. J. Biol. Chem. 2012, 287:22549-22559.
4. Apte S.S. A disintegrin-like and metalloprotease (reprolysin type) with thrombospondin type 1 motifs: the ADAMTS family. Int. J. Biochem. Cell Biol. 2004, 36:981-985.
5. Arber S., Caroni P. Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neurite outgrowth. J. Cell Biol. 1995, 131:1083-1094.
6. Asch A.S., Barnwell J., Silverstein R.L., Nachman R.L. Isolation of the thrombospondin membrane receptor. J. Clin. Invest. 1987, 79:1054-1061.
7. Briggs M.D., Chapman K.L. Pseudoachondroplasia and multiple epiphyseal dysplasia: mutation review, molecular interactions, and genotype to phenotype correlations. Hum. Mutat. 2002, 19:465-478.
8. Briggs M.D., Hoffman S.M.G., King L.M., Olsen A.S., Mohrenweiser H., Leroy J.G., Mortier G.R., Rimoin D.L., Lachman R.S., Gaines E.S., Cekleniak J.A., Knowlton R.G., Cohn D.H. Pseudoachondroplasia and multiple epiphyseal dysplasia due to mutations in the cartilage oligomeric matrix protein gene. Nat. Genet. 1995, 10:330-336.
9. Brown E.J., Frazier W.A. Integrin-associated protein (CD47) and its ligands. Trends Cell Biol. 2001, 11:130-135.
10. Budde B., Blumbach K., Ylostalo J., Zaucke F., Ehlen H.W.A., Wagener R., Ala-Kokko L., Paulsson M., Bruckner P., Grassel S. Altered integration of matrilin-3 into cartilage extracellular matrix in the absence of collagen IX. Mol. Cell. Biol. 2005, 25:10465-10478.
11. Carlsen S., Nandakumar K.S., Backlund J., Holmberg J., Hultqvist M., Vestberg M., Holmdahl R. Cartilage oligomeric matrix protein induction of chronic arthritis in mice. Arthritis Rheum. 2008, 58:2000-2011.
12. Carlson C.B., Bernstein D.A., Annis D.S., Misenheimer T.M., Hannah B.L., Mosher D.F., Keck J.L. Structure of the calcium-rich signature domain of human thrombospondin-2. Nat. Struct. Mol. Biol. 2005, 12:910-914.
13. Chandran P.L., Horkay F. Aggrecan, an unusual polyelectrolyte: review of solution behavior and physiological implications. Acta Biomater. 2012, 8:3-12.
14. Chen H., Herndon M.E., Lawler J. The cell biology of thrombospondin-1. Matrix Biol. 2000, 19:597-614.
15. Chen F.H., Thomas A.O., Hecht J.T., Goldring M.B., Lawler J. Cartilage oligomeric matrix protein/thrombospondin 5 supports chondrocyte attachment through interaction with integrins. J. Biol. Chem. 2005, 280:32655-32661.
16. Chen F.H., Herndon M.E., Patel N., Hecht J.T., Tuan R.S., Lawler J. Interaction of cartilage oligomeric matrix protein/thrombospondin 5 with aggrecan. J. Biol. Chem. 2007, 282:24591-24598.
17. Cohn D.H., Briggs M.D., King L.M., Rimoin D.L., Wilcox W.R., Lachman R.S., Knowlton R.G. Mutations in the cartilage oligomeric matrix protein (COMP) gene in pseudoachondroplasia and multiple epiphyseal dysplasia. Ann. N. Y. Acad. Sci. 1996, 785:188-194.
18. Conway A., Vazin T., Spelke D.P., Rode N.A., Healy K.E., Kane R.S., Schaffer D.V. Multivalent ligands control stem cell behaviour in vitro and in vivo. Nat. Nanotechnol. 2013, 8:831-838.
19. Corsetti J.P., Ryan D., Moss A.J., McCarthy J., Goldenberg I., Zareba W., Sparks C.E. Thrombospondin-4 polymorphism (A387P) predicts cardiovascular risk in postinfarction patients with high HDL cholesterol and C-reactive protein levels. Thromb. Haemost. 2011, 106:1170-1178.
20. DeLise A.M., Fischer L., Tuan R.S. Cellular interactions and signaling in cartilage development. Osteoarthr. Cartil. 2000, 8:309-334.
21. Délot E., Brodie S.G., King L.M., Wilcox W.R., Cohn D.H. Physiological and pathological secretion of cartilage oligomeric matrix protein by cells in culture. J. Biol. Chem. 1998, 273:26692-26697.
22. Di Cesare P.E., Carlson C.S., Stolerman E.S., Hauser N., Tulli H., Paulsson M. Increased degradation and altered tissue distribution of cartilage oligomeric matrix protein in human rheumatoid and osteoarthritic cartilage. J. Orthop. Res. 1996, 14:946-955.
23. Di Cesare P.E., Chen F.S., Moergelin M., Carlson C.S., Leslie M.P., Perris R., Fang C. Matrix-matrix interaction of cartilage oligomeric matrix protein and fibronectin. Matrix Biol. 2002, 21:461-470.
24. DiCesare P.E., Mörgelin M., Mann K., Paulsson M. Cartilage oligomeric matrix protein and thrombospondin 1. Purification from articular cartilage, electron microscopic structure, and chondrocyte binding. Eur. J. Biochem. 1994, 223:927-937.
25. DiCesare P.E., Mörgelin M., Carlson C.S., Pasumarti S., Paulsson M. Cartilage oligomeric matrix protein: isolation and characterization from human articular cartilage. J. Orthop. Res. 1995, 13:422-428.
26. Dickinson S.C., Vankemmelbeke M.N., Buttle D.J., Rosenberg K., Heinegård D., Hollander A.P. Cleavage of cartilage oligomeric matrix protein (thrombospondin-5) by matrix metalloproteinases and a disintegrin and metalloproteinase with thrombospondin motifs. Matrix Biol. 2003, 22:267-278.
27. DiPietro L.A., Nissen N.N., Gamelli R.L., Koch A.E., Pyle J.M., Polverini P.J. Thrombospondin 1 synthesis and function in wound repair. Am. J. Pathol. 1996, 148:1851-1860.
28. Du Y., Wang Y., Wang L., Liu B., Tian Q., Liu C.J., Zhang T., Xu Q., Zhu Y., Ake O., Qi Y., Tang C., Kong W., Wang X. Cartilage oligomeric matrix protein inhibits vascular smooth muscle calcification by interacting with bone morphogenetic protein-2. Circ. Res. 2011, 108:917-928.
29. Efimov V.P., Engel J., Malashkevich V.N. Crystallization and preliminary crystallographic study of the pentamerizing domain from cartilage oligomeric matrix protein: a five-stranded alpha-helical bundle. Proteins 1996, 24:259-262.
30. Fang C., Carlson C.S., Leslie M.P., Tulli H., Stolerman E., Perris R., Ni L., Di Cesare P.E. Molecular cloning, sequencing, and tissue and developmental expression of mouse cartilage oligomeric matrix protein (COMP). J. Orthop. Res. 2000, 18:593-603.
31. Franzen A., Heinegard D., Solursh M. Evidence for sequential appearance of cartilage matrix proteins in developing mouse limbs and in cultures of mouse mesenchymal cells. Differentiation 1987, 36:199-210.
32. Ganu V., Goldberg R., Peppard J., Rediske J., Melton R., Hu S.I., Wang W., Duvander C., Heinegard D. Inhibition of interleukin-1alpha-induced cartilage oligomeric matrix protein degradation in bovine articular cartilage by matrix metalloproteinase inhibitors: potential role for matrix metalloproteinases in the generation of cartilage oligomeric matrix protein fragments in arthritic synovial fluid. Arthritis Rheum. 1998, 41:2143-2151.
33. Geng H., Nandakumar K.S., Pramhed A., Aspberg A., Mattsson R., Holmdahl R. Cartilage oligomeric matrix protein specific antibodies are pathogenic. Arthritis Res. Ther. 2012, 14:R191.
34. Geng H., Nandakumar K.S., Xiong L., Jie R., Dong J., Holmdahl R. Incomplete B cell tolerance to cartilage oligomeric matrix protein in mice. Arthritis Rheum. 2013, 65:2301-2309.
35. Guo Y., Bozic D., Malashkevich V.N., Kammerer R.A., Schulthess T., Engel J. All-trans retinol, vitamin D and other hydrophobic compounds bind in the axial pore of the five-stranded coiled-coil domain of cartilage oligomeric matrix protein. EMBO J. 1998, 17:5265-5272.
36. Halász K., Kassner A., Mörgelin M., Heinegård D. COMP acts as a catalyst in collagen fibrillogenesis. J. Biol. Chem. 2007, 282:31166-31173.
37. Haleem-Smith H., Calderon R., Song Y., Tuan R.S., Chen F.H. Cartilage oligomeric matrix protein enhances matrix assembly during chondrogenesis of human mesenchymal stem cells. J. Cell. Biochem. 2012, 113:1245-1252.
38. Hansen U., Platz N., Becker A., Bruckner P., Paulsson M., Zaucke F. A secreted variant of cartilage oligomeric matrix protein carrying a chondrodysplasia-causing mutation (p.H587R) disrupts collagen fibrillogenesis. Arthritis Rheum. 2011, 63:159-167.
39. Happonen K.E., Saxne T., Aspberg A., Morgelin M., Heinegard D., Blom A.M. Regulation of complement by cartilage oligomeric matrix protein allows for a novel molecular diagnostic principle in rheumatoid arthritis. Arthritis Rheum. 2010, 62:3574-3583.
40. Happonen K.E., Heinegard D., Saxne T., Blom A.M. Interactions of the complement system with molecules of extracellular matrix: relevance for joint diseases. Immunobiology 2012, 217:1088-1096.
41. Happonen K.E., Saxne T., Geborek P., Andersson M., Bengtsson A.A., Hesselstrand R., Heinegard D., Blom A.M. Serum COMP-C3b complexes in rheumatic diseases and relation to anti-TNF-alpha treatment. Arthritis Res. Ther. 2012, 14:R15.
42. Hashimoto Y., Tomiyama T., Yamano Y., Mori H. Mutation (D472Y) in the type 3 repeat domain of cartilage oligomeric matrix protein affects its early vesicle trafficking in endoplasmic reticulum and induces apoptosis. Am. J. Pathol. 2003, 163:101-110.
43. Haudenschild D.R., Hong E., Yik J.H.N., Chromy B., Mörgelin M., Snow K.D., DiCesare P.E., Acharya C., Takada Y. Enhanced activity of TGF-ß1 bound to cartilage oligomeric matrix protein. J. Biol. Chem. 2011 Dec 16, 286(50):43250-43258.
44. Hecht J.T., Nelson L.D., Crowder D., Wang Y., Elder F.F.B., Harrison W.R., Francomano C.A., Prange C.K., Lennon G.K., Deere M., Lawler J. Mutations in exon 17B of cartilage oligomeric matrix protein (COMP) cause pseudoachondroplasia. Nat. Genet. 1995, 10:325-329.
45. Hecht J.T., Montufar-Solis D., Decker G., Lawler J., Daniels K., Duke P.J. Retention of cartilage oligomeric matrix protein (COMP) and cell death in redifferentiated pseudoachondroplasia chondrocytes. Matrix Biol. 1998, 17:625-633.
46. Hecht J.T., Hayes E., Haynes R., Cole W.G. COMP mutations, chondrocyte function and cartilage matrix. Matrix Biol. 2005, 23:525-533.
47. Hedbom E., Antonsson P., Hjerpe A., Aeschlimann D., Paulsson M., Rosa-Pimentel E., Sommarin Y., Wendel M., Oldberg A., Heinegård D. Cartilage matrix proteins. An acidic oligomeric protein (COMP) detected only in cartilage. J. Biol. Chem. 1992, 267:6132-6136.
48. Im G.I., Jung N.H., Tae S.K. Chondrogenic differentiation of mesenchymal stem cells isolated from patients in late adulthood: the optimal conditions of growth factors. Tissue Eng. 2006, 12:527-536.
49. Ishida K., Acharya C., Christiansen B.A., Yik J.H., DiCesare P.E., D.R.Haudenschild. Cartilage oligomeric matrix protein enhances osteogenesis by directly binding and activating bone morphogenetic protein-2. Bone 2013, 55:23-35.
50. Johnson A., Smith R., Saxne T., Hickery M., Heinegård D. Fibronectin fragments cause release and degradation of collagen-binding molecules from eqine explant cultures. Osteoarthr. Cartil. 2004, 12:149-159.
51. Kalchishkova N., Fürst C., Heinegård D., Blom A.M. The NC4 domain of the cartilage specific collagen IX inhibits complement directly due to attenuation of membrane attack formation and indirectly through binding and enhancing activity of complement inhibitors C4B-binding protein and factor H. J. Biol. Chem. 2011, 286:27915-27926.
52. Kawamura I., Maeda S., Imamura K., Setoguchi T., Yokouchi M., Ishidou Y., Komiya S. SnoN suppresses maturation of chondrocytes by mediating signal cross-talk between transforming growth factor-beta and bone morphogenetic protein pathways. J. Biol. Chem. 2012, 287:29101-29113.
53. Kinne R.W. (Auto)immunity to cartilage matrix proteins - a time bomb?. Arthritis Res. Ther. 2013, 15:101.
54. Kipnes J., Carlberg A.L., Loredo G.A., Lawler J., Tuan R.S., Hall D.J. Effect of cartilage oligomeric matrix protein on mesenchymal chondrogenesis in vitro. Osteoarthr. Cartil. 2003, 11:442-454.
55. Koelling S., Clauditz T.S., Kaste M., Miosge N. Cartilage oligomeric matrix protein is involved in human limb development and in the pathogenesis of osteoarthritis. Arthritis Res. Ther. 2006, 8.
56. Kvansakul M., Adams J.C., Hohenester E. Structure of a thrombospondin C-terminal fragment reveals a novel calcium core in the type 3 repeats. EMBO J. 2004, 23:1223-1233.
57. Kyriakides T.R., Zhu Y.H., Smith L.T., Bain S.D., Yang Z., Lin M.T., Danielson K.G., Iozzo R.V., LaMarca M., McKinney C.E., Ginns E.I., Bornstein P. Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J. Cell Biol. 1998, 140:419-430.
58. Li H., Haudenschild D.R., Posey K.L., Hecht J.T., DiCesare P.E., Yik J.H. Comparative analysis with collagen type II distinguishes cartilage oligomeric matrix protein as a primary TGFb-responsive gene. Osteoarthr. Cartil. 2011, 10:1246-1253.
59. Liu C.J., Kong W., Ilalov K., Yu S., Xu K., Prazak L., Fajardo M., Sehgal B., Di Cesare P.E. ADAMTS-7: a metalloproteinase that directly binds to and degrades cartilage oligomeric matrix protein. FASEB J. 2006, 20:988-+.
60. Liu C.J., Kong W., Xu K., Luan Y., Ilalov K., Sehgal B., Yu S., Howell R.D., Di Cesare P.E. ADAMTS-12 associates with and degrades cartilage oligomeric matrix protein. J. Biol. Chem. 2006, 281:15800-15808.
61. Maddox B.K., Keene D.R., Sakai L.Y., Charbonneau N.L., Morris N.P., Ridgway C.C., Boswell B.A., Sussman M.D., Horton W.A., Bachinger H.P., Hecht J.T. The fate of cartilage oligomeric matrix protein is determined by the cell type in the case of a novel mutation in pseudoachondroplasia. J. Biol. Chem. 1997, 272:30993-30997.
62. Malashkevich V.N., Kammerer R.A., Efimov V.P., Schulthess T., Engel J. The crystal structure of a five-stranded coiled coil in COMP: a prototype ion channel?. Science 1996, 274:761-765.
63. Malfait A.M., Liu R.Q., Ijiri K., Komiya S., Tortorella M.D. Inhibition of ADAM-TS4 and ADAM-TS5 prevents aggrecan degradation in osteoarthritic cartilage. J. Biol. Chem. 2002, 277:22201-22208.
64. Mann H.H., Özbek S., Engel J., Paulsson P., Wagener R. Interactions between cartilage oligomeric matrix protein and matrilins. Implications for matrix assembly and the pathogenesis of chondrodysplasias. J. Biol. Chem. 2004, 279:25294-25298.
65. Mörgelin M., Heinegård D., Engel J., Paulsson M. Electron microscopy of native cartilage oligomeric matrix protein purified from the Swarm rat chondrosarcoma reveals a five-armed structure. J. Biol. Chem. 1992, 267:6137-6141.
66. Müller G., Michel A., Altenburg E. COMP (cartilage oligomeric matrix protein) is synthesized in ligament, tendon, meniscus, and articular cartilage. Connect. Tissue Res. 1998, 39:233-244.
67. Murphy-Ullrich J.E., Iozzo R.V. Thrombospondins in physiology and disease: new tricks for old dogs. Matrix Biol. 2012, 31:152-154.
68. Murphy-Ullrich J.E., Mosher D.F. Interactions of thrombospondin with endothelial cells: receptor-mediated binding and degradation. J. Cell Biol. 1987, 105:1603-1611.
69. Neidhart M., Hauser N., Paulsson M., DiCesare P.E., Michel B.A., Häuselmann H.J. Small fragments of cartilage oligomeric matrix protein in synovial fluid and serum as markers for cartilage degradation. Br. J. Rheumatol. 1997, 36:1151-1160.
70. Newton G., Weremowicz S., Morton C.C., Copeland N.G., Gilbert D.J., Jenkins N.A., Lawler J. Characterization of human and mouse cartilage oligomeric matrix protein. Genomics 1994, 24:435-439.
71. Özbek S., Engel J., Stetefeld J. Storage function of cartilage oligomeric matrix protein: the crystal structure of the coiled-coil domain in complex with vitamin D3. EMBO J. 2002, 21:5960-5968.
72. Patt L.M., Houck J.C. Role of polypeptide growth factors in normal and abnormal growth. Kidney Int. 1983, 23:603-610.
73. Petersson I.F., Boegård T., Dahlström J., Svensson B., Heinegård D., Saxne T. Bone scan and serum markers of bone and cartilage in patients with knee pain and osteoarthritis. Osteoarthr. Cartil. 1998, 6:33-39.
74. Piecha D., Wiberg C., Mörgelin M., Reinhardt D.P., Deak F., Maurer P., Paulsson M. Matrilin-2 interacts with itself and with other extracellular matrix proteins. Biochem. J. 2002, 367:715-721.
75. Porter S., Clark I.M., Kevorkian L., Edwards D.R. The ADAMTS metalloproteinases. Biochem. J. 2005, 386:15-27.
76. Posey K.L., Hankenson K., Veerisetty A.C., Bornstein P., Lawler J., Hecht J.T. Skeletal abnormalities in mice lacking extracellular matrix proteins, thrombospondin-1, thrombospondin-3, thrombospondin-5, and type IX collagen. Am. J. Pathol. 2008, 172:1664-1674.
77. Posey K.L., Coustry F., Veerisetty A.C., Liu P., Alcorn J.L., Hecht J.T. Chop (Ddit3) is essential for D469del-COMP retention and cell death in chondrocytes in an inducible transgenic mouse model of pseudoachondroplasia. Am. J. Pathol. 2012, 180:727-737.
78. Rock M.J., Holden P., Horton W.A., Cohn D.H. Cartilage oligomeric matrix protein promotes cell attachment via two independent mechanisms involving CD47 and alphaVbeta3 integrin. Mol. Cell. Biochem. 2010, 338:215-224.
79. Rosenberg K., Olsson H., Mörgelin M., Heinegård D. Cartilage oligomeric matrix protein shows high affinity zinc-dependent interaction with triple helical collagen. J. Biol. Chem. 1998, 273:20397-20403.
80. Schmitz M., Becker A., Schmitz A., Weirich C., Paulsson M., Zaucke F., Dinser R. Disruption of extracellular matrix structure may cause pseudoachondroplasia phenotypes in the absence of impaired cartilage oligomeric matrix protein secretion. J. Biol. Chem. 2006, 281:32587-32595.
81. Solorio L.D., Dhami C.D., Dang P.N., Vieregge E.L., Alsberg E. Spatiotemporal regulation of chondrogenic differentiation with controlled delivery of transforming growth factor-beta 1 from gelatin microspheres in mesenchymal stem cell aggregates. Stem Cell Transl. Med. 2012, 1:632-639.
82. Stracke J.O., Fosang A.J., Last K., Mercuri F.A., Pendas A.M., Llano E., Perris R., Di Cesare P.E., Murphy G., Knauper V. Matrix metalloproteinases 19 and 20 cleave aggrecan and cartilage oligomeric matrix protein (COMP). FEBS Lett. 2000, 478:52-56.
83. Svensson L., Aszodi A., Heinegård D., Hunziker E.B., Reinholt F.P., Fassler R., Oldberg A. Cartilage oligomeric matrix protein-deficient mice have normal skeletal development. Mol. Cell. Biol. 2002, 22:4366-4371.
84. Sweetwyne M.T., Murphy-Ullrich J.E. Thrombospondin1 in tissue repair and fibrosis: TGF-beta-dependent and independent mechanisms. Matrix Biol. 2012, 31:178-186.
85. Tan K., Lawler J. The interaction of thrombospondins with extracellular matrix proteins. J. Cell Commun. Signal. 2009, 3:177-187.
86. Tan K., Duquette M., Joachimiak A., Lawler J. The crystal structure of the signature domain of cartilage oligomeric matrix protein: implications for collagen, glycosaminoglycan and integrin binding. FASEB J. 2009, 23:2490-2501.
87. Thur J., Rosenberg K., Nitsche D.P., Pihlajamaa T., Ala-Kokko L., Heinegard D., Paulsson M., Maurer P. Mutations in cartilage oligomeric matrix protein causing pseudoachondroplasia and multiple epiphyseal dysplasia affect binding of calcium and collagen I, II, and IX. J. Biol. Chem. 2001, 276:6083-6092.
88. van der Kraan P.M., Goumans M.J., Blaney Davidson E., ten Dijke P. Age-dependent alteration of TGF-beta signalling in osteoarthritis. Cell Tissue Res. 2012, 347:257-265.
89. Vankemmelbeke M.N., Jones G.C., Fowles C., Ilic M.Z., Handley C.J., Day A.J., Knight C.G., Mort J.S., Buttle D.J. Selective inhibition of ADAMTS-1, -4 and -5 by catechin gallate esters. Eur. J. Biochem. 2003, 270:2394-2403.
90. Vertel B.M.V., LaFrance S., Walters L., Kaczman-Daniel K. Precursors of chondroitin sulfate proteoglycan are segregated within a sub-compartment of the chondrocyte endoplasmic reticulum. J. Cell Biol. 1989, 109:1827-1836.
91. Vranka J., Mokashi A., Keene D.R., Tufa S., Corson G., Sussman M., Horton W.A., Maddox K., Sakai L., Bächinger H.P. Selective intracellular retention of extracellular matrix proteins and chaperones associated with pseudoachondroplasia. Matrix Biol. 2001, 20:439-450.
92. Wakitani S., Nawata M., Kawaguchi A., Okabe T., Takaoka K., Tsuchiya T., Nakaoka R., Masuda H., Miyazaki K. Serum keratan sulfate is a promising marker of early articular cartilage breakdown. Rheumatology 2007, 46:1652-1656.
93. Wang L., Zheng J., Du Y., Huang Y., Li J., Liu B., Liu C.J., Zhu Y., Gao Y., Xu Q., Kong W., Wang X. Cartilage oligomeric matrix protein maintains the contractile phenotype of vascular smooth muscle cells by interacting with alpha(7)beta(1) integrin. Circ. Res. 2010, 106:514-525.
94. Woods V.L., Schreck P.J., Gesink D.S., Pacheco H.O., Amiel D., Akeson W.H., Lotz M. Integrin expression by human articular chondrocytes. Arthritis Rheum. 1994, 37:537-544.
95. Zaucke F., Grässel S. Genetic mouse models for the functional analysis of the perifibrillar components collagen IX, COMP and matrilin-3: implications for growth cartilage differentiation and endochondral ossification. Histol. Histopathol. 2009, 24:1067-1079.
96. Zemmyo M., Meharra E.J., Kuhn K., Creighton-Achermann L., Lotz M. Accelerated, aging-dependent development of osteoarthritis in alpha1 integrin-deficient mice. Arthritis Rheum. 2003, 48:2873-2880.
97. Zhen E.Y., Brittain I.J., Laska D.A., Mitchell P.G., Sumer E.U., Karsdal M.A., Duffin K.L. Characterization of metalloprotease cleavage products of human articular cartilage. Arthritis Rheum. 2008, 58:2420-2431.