ADAMTS-7: A metalloproteinase that directly binds to and degrades cartilage oligomeric matrix protein

FASEB Journal

Volumn 20, Issue 7, 2006, Pages

  Liu, Chuan Ju ^a,b   Kong, Wei ^a   Ilalov, Kiril ^a   Yu, Shuang ^c   Xu, Ke ^a   Prazak, Lisa ^a   Fajardo, Marc ^a   Sehgal, Bantoo ^a   Di Cesare, Paul E ^a,b  

^a NYU HOSPITAL FOR JOINT DISEASES   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Arthritis; COMP; Degradation

Indexed keywords

CARTILAGE OLIGOMERIC MATRIX PROTEIN; EPIDERMAL GROWTH FACTOR; METALLOPROTEINASE; PROTEIN ADAMTS 7; ADAM PROTEIN; ADAMTS7 PROTEIN, HUMAN; ADAMTS7 PROTEIN, MOUSE; CARTILAGE MATRIX PROTEIN; GLYCOPROTEIN; MESSENGER RNA; SCLEROPROTEIN; ZINC;

ARTHRITIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CARTILAGE DEGENERATION; CONTROLLED STUDY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; ADULT; AGED; ANIMAL; BINDING SITE; CARTILAGE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; MOUSE; PH; RAT; RHEUMATOID ARTHRITIS; SYNOVIUM; TWO HYBRID SYSTEM; UPREGULATION;

ADAM PROTEINS; ADULT; AGED; ANIMALS; ARTHRITIS, RHEUMATOID; BINDING SITES; CARTILAGE; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOPROTEINS; HUMANS; HYDROGEN-ION CONCENTRATION; MICE; MIDDLE AGED; PROTEIN BINDING; RATS; RNA, MESSENGER; SYNOVIAL MEMBRANE; TWO-HYBRID SYSTEM TECHNIQUES; UP-REGULATION; ZINC;

EID: 33845702259     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.05-3877fje     Document Type: Article

References (65)

1. Poole, R. A., Mort, J. S., and Roughley, P. J. (1993) Methods for evaluating mechanisms of cartilage breakdown. In: Joint cartilage degradation: Basic and clinical aspects, Marcel Dekker, Inc., New York, New York
2. Salzet, M. (2002) Leech thrombin inhibitors. Curr. Pharm. Des. 8, 493-503
3. Hedbom, E., Antonsson, P., Hjerpe, A., Aeschlimann, D., Paulsson, M., Rosa-Pimentel, E., Sommarin, Y., Wendel, M., Oldberg, A., and Heinegard, D. (1992) Cartilage matrix proteins. An acidic oligomeric protein (COMP) detected only in cartilage. J. Biol. Chem. 267, 6132-6136
4. Di Cesare, P. E., Fang, C., Leslie, M. P., Tulli, H., Perris, R., and Carlson, C. S. (2000) Expression of cartilage oligomeric matrix protein (COMP) by embryonic and adult osteoblasts. J. Orthop. Res. 18, 713-720
5. Di Cesare, P., Hauser, N., Lehman, D., Pasumarti, S., and Paulsson, M. (1994) Cartilage oligomeric matrix protein (COMP) is an abundant component of tendon. FEBS Lett. 354, 237-240
6. Di Cesare, P. E., Carlson, C. S., Stollerman, E. S., Chen, F. S., Leslie, M., and Perris, R. (1997) Expression of cartilage oligomeric matrix protein by human synovium. FEBS Lett. 412, 249-252
7. Morgelin, M., Engel, J., Heinegard, D., and Paulsson, M. (1992) Proteoglycans from the swarm rat chondrosarcoma. Structure of the aggregates extracted with associative and dissociative solvents as revealed by electron microscopy. J. Biol. Chem. 267, 14275-14284
8. Kraus, V. B., Huebner, J. L., Fink, C., King, J. B., Brown, S., Vail, T. P., and Guilak, F. (2002) Urea as a passive transport marker for arthritis biomarker studies. Arthritis Rheum. 46, 420-427
9. Misumi, K., Vilim, V., Hatazoe, T., Murata, T., Fujiki, M., Oka, T., Sakamoto, H., and Carter, S. D. (2002) Serum level of cartilage oligomeric matrix protein (COMP) in equine osteoarthritis. Equine Vet. J. 34, 602-608
10. Neidhart, M. (1996) Elevated serum prolactin or elevated prolactin/cortisol ratio are associated with autoimmune processes in systemic lupus erythematosus and other connective tissue diseases. J. Rheumatol. 23, 476-481
11. Mansson, B., Carey, D., Alini, M., Ionescu, M., Rosenberg, L. C., Poole, A. R., Heinegard, D., and Saxne, T. (1995) Cartilage and bone metabolism in rheumatoid arthritis. Differences between rapid and slow progression of disease identified by serum markers of cartilage metabolism. J. Clin. Invest. 95, 1071-1077
12. Lohmander, L. S., Ionescu, M., Jugessur, H., and Poole, A. R. (1999) Changes in joint cartilage aggrecan after knee injury and in osteoarthritis. Arthritis Rheum. 42, 534-544
13. Petersson, I. F., Boegard, T., Svensson, B., Heinegard, D., and Saxne, T. (1998) Changes in cartilage and bone metabolism identified by serum markers in early osteoarthritis of the knee joint. Br. J. Rheumatol. 37, 46-50
14. Briggs, M. D., Rasmussen, I. M., Weber, J. L., Yuen, J., Reinker, K., Garber, A. P., Rimoin, D. L., and Cohn, D. H. (1993) Genetic linkage of mild pseudoachondroplasia (PSACH) to markers in the pericentromeric region of chromosome 19. Genomics 18, 656-660
15. Briggs, M. D., Hoffman, S. M., King, L. M., Olsen, A. S., Mohrenweiser, H., Leroy, J. G., Mortier, G. R., Rimoin, D. L., Lachman, R. S., and Gaines, E. S. (1995) Pseudoachondroplasia and multiple epiphyseal dysplasia due to mutations in the cartilage oligomeric matrix protein gene. Nature 10, 330-336
16. Briggs, M. D., Mortier, G. R., Cole, W. G., King, L. M., Golik, S. S., Bonaventure, J., Nuytinck, L., De Paepe, A., Leroy, J. G., Biesecker, L., Lipson, M., Wilcox, W. R., Lachman, R. S., Rimoin, D. L., RG, K., and Cohn, D. H. (1998) Diverse mutations in the gene for cartilage oligomeric matrix protein in the pseudoachondroplasia-multiple epiphyseal dysplasia disease spectrum. Am. J. Hum. Genet. 62, 311-319
17. Cohn, D. H., Briggs, M. D., King, L. M., Rimoin, D. L., Wilcox, W. R., Lachman, R. S., and Knowlton, R. G. (1996) Mutations in the cartilage oligomeric matrix protein (COMP) gene in pseudoachondroplasia and multiple epiphyseal dysplasia. Ann. N. Y. Acad. Sci. 785, 188-194
18. Hecht, J. T., Francomano, C. A., Briggs, M. D., Deere, M., Conner, B., Horton, W. A., Warman, M., Cohn, D. H., and Blanton, S. H. (1993) Linkage of typical pseudoachondroplasia to chromosome 19. Genomics 18, 661-666
19. Hecht, J. T., Nelson, L. D., Crowder, E., Wang, Y., Elder, F. F., Harrison, W. R., Francomano, C. A., Prange, C. K., Lennon, G. G., and Deere, M. (1995) Mutations in exon 17B of cartilage oligomeric matrix protein (COMP) cause pseudoachondroplasia. Nat. Genet. 10, 325-329
20. Susic, S., McGrory, J., Ahier, J., and Cole, W. G. (1997) Multiple epiphyseal dysplasia and pseudoachondroplasia due to novel mutations in the calmodulin-like repeats of cartilage oligomeric matrix protein. Clin. Genet. 51, 219-224
21. Di Cesare, P. E., Carlson, C. S., Stolerman, E. S., Hauser, N., Tulli, H., and Paulsson, M. (1996) Increased degradation and altered tissue distribution of cartilage oligomeric matrix protein in human rheumatoid and osteoarthritic cartilage. J. Orthop. Res. 14, 946-955
22. Neidhart, M., Hauser, N., Paulsson, M., DiCesare, P. E., Michel, B. A., and Hauselmann, H. J. (1997) Small fragments of cartilage oligomeric matrix protein in synovial fluid and serum as markers for cartilage degradation. Br. J. Rheumatol. 36, 1151-1160
23. Saxne, T., and Heinegard, D. (1992) Cartilage oligomeric matrix protein: a novel marker of cartilage turnover detectable in synovial fluid and blood. Br. J. Rheumatol. 31, 583-591
24. Hollenberg, S. M., Sternglanz, R., Cheng, P. F., and Weintraub, H. (1995) Identification of a new family of tissue-specific basic helix-loop- helix proteins with a two-hybrid system. Mol. Cell. Biol. 15, 3813-3822
25. Liu, C., Dib-Hajj, S. D., and Waxman, S. G. (2001) Fibroblast growth factor homologous factor 1B binds to the C terminus of the tetrodotoxin- resistant sodium channel rNav1.9a (NaN). J. Biol. Chem. 276, 18925-18933
26. Vojtek, A. B., Hollenberg, S. M., and Cooper, J. A. (1993) Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74, 205-214
27. Cal, S., Obaya, A. J., Llamazares, M., Garabaya, C., Quesada, V., and Lopez-Otin, C. (2002) Cloning, expression analysis, and structural characterization of seven novel human ADAMTSs, a family of metalloproteinases with disintegrin and thrombospondin-1 domains. Gene 283, 49-62
28. Tortorella, M. D., Burn, T. C., Pratta, M. A., Abbaszade, I., Hollis, J. M., Liu, R., Rosenfeld, S. A., Copeland, R. A., Decicco, C. P., Wynn, R., Rockwell, A., Yang, F., Duke, J. L., Solomon, K., George, H., Bruckner, R., Nagase, H., Itoh, Y., Ellis, D. M., Ross, H., Wiswall, B. H., Murphy, K., Hillman, M. C., Jr., Hollis, G. F., Arner, E. C., et al. (1999) Purification and cloning of aggrecanase-1: a member of the ADAMTS family of proteins. Science 284, 1664-1666
29. Hurskainen, T. L., Hirohata, S., Seldin, M. F., and Apte, S. S. (1999) ADAM-TS5, ADAM-TS6, and ADAM-TS7, novel members of a new family of zinc metalloproteases. General features and genomic distribution of the ADAM- TS family. J. Biol. Chem. 274, 25555-25563
30. Collins-Racie, L. A., Flannery, C. R., Zeng, W., Corcoran, C., Annis-Freeman, B., Agostino, M. J., Arai, M., DiBlasio-Smith, E., Dorner, A. J., Georgiadis, K. E., Jin, M., Tan, X. Y., Morris, E. A., and LaVallie, E. R. (2004) ADAMTS-8 exhibits aggrecanase activity and is expressed in human articular cartilage. Matrix Biol. 23, 219-230
31. Abbaszade, I., Liu, R. Q., Yang, F., Rosenfeld, S. A., Ross, O. H., Link, J. R., Ellis, D. M., Tortorella, M. D., Pratta, M. A., Hollis, J. M., Wynn, R., Duke, J. L., George, H. J., Hillman, M. C., Jr., Murphy, K., Wiswall, B. H., Copeland, R. A., Decicco, C. P., Bruckner, R., Nagase, H., Itoh, Y., Newton, R. C., Magolda, R. L., Trzaskos, J. M., Burn, T. C., et al. (1999) Cloning and characterization of ADAMTS11, an aggrecanase from the ADAMTS family. J. Biol. Chem. 274, 23443-23450
32. Kuno, K., Okada, Y., Kawashima, H., Nakamura, H., Miyasaka, M., Ohno, H., and Matsushima, K. (2000) ADAMTS-1 cleaves a cartilage proteoglycan, aggrecan. FEBS Lett. 478, 241-245
33. Tortorella, M. D., Pratta, M., Liu, R. Q., Austin, J., Ross, O. H., Abbaszade, I., Burn, T., and Arner, E. (2000) Sites of aggrecan cleavage by recombinant human aggrecanase-1 (ADAMTS-4). J. Biol. Chem. 275, 18566-18573
34. Sandy, J. D., Westling, J., Kenagy, R. D., Iruela-Arispe, M. L., Verscharen, C., Rodriguez-Mazaneque, J. C., Zimmermann, D. R., Lemire, J. M., Fischer, J. W., Wight, T. N., and Clowes, A. W. (2001) Versican V1 proteolysis in human aorta in vivo occurs at the Glu441- Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS- 4. J. Biol. Chem. 276, 13372-13378
35. Matthews, R. T., Gary, S. C., Zerillo, C., Pratta, M., Solomon, K., Arner, E. C., and Hockfield, S. (2000) Brain-enriched hyaluronan binding (BEHAB)/brevican cleavage in a glioma cell line is mediated by a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) family member. J. Biol. Chem. 275, 22695-22703
36. Vazquez, F., Hastings, G., Ortega, M. A., Lane, T. F., Oikemus, S., Lombardo, M., and Iruela-Arispe, M. L. (1999) METH-1, a human ortholog of ADAMTS-1, and METH-2 are members of a new family of proteins with angio-inhibitory activity. J. Biol. Chem. 274, 23349-23357
37. Mittaz, L., Russell, D. L., Wilson, T., Brasted, M., Tkalcevic, J., Salamonsen, L. A., Hertzog, P. J., and Pritchard, M. A. (2004) Adamts-1 is essential for the development and function of the urogenital system. Biol. Reprod. 70, 1096-1105
38. Colige, A., Vandenberghe, I., Thiry, M., Lambert, C. A., Van Beeumen, J., Li, S. W., Prockop, D. J., Lapiere, C. M., and Nusgens, B. V. (2002) Cloning and characterization of ADAMTS-14, a novel ADAMTS displaying high homology with ADAMTS-2 and ADAMTS-3. J. Biol. Chem. 277, 5756-5766
39. Fernandes, R. J., Hirohata, S., Engle, J. M., Colige, A., Cohn, D. H., Eyre, D. R., and Apte, S. S. (2001) Procollagen II amino propeptide processing by ADAMTS-3. Insights on dermatosparaxis. J. Biol. Chem. 276, 31502-31509
40. Colige, A., Sieron, A. L., Li, S. W., Schwarze, U., Petty, E., Wertelecki, W., Wilcox, W., Krakow, D., Cohn, D. H., Reardon, W., Byers, P. H., Lapiere, C. M., Prockop, D. J., and Nusgens, B. V. (1999) Human Ehlers-Danlos syndrome type VII C and bovine dermatosparaxis are caused by mutations in the procollagen I N-proteinase gene. Am. J. Hum. Genet. 65, 308-317
41. Levy, G. G., Nichols, W. C., Lian, E. C., Foroud, T., McClintick, J. N., McGee, B. M., Yang, A. Y., Siemieniak, D. R., Stark, K. R., Gruppo, R., Sarode, R., Shurin, S. B., Chandrasekaran, V., Stabler, S. P., Sabio, H., Bouhassira, E. E., Upshaw, J. D., Jr., Ginsburg, D., and Tsai, H. M. (2001) Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature 413, 488-494
42. Liu, C. J., Wang, H., and Lengyel, P. (1999) The interferon-inducible nucleolar p204 protein binds the ribosomal RNA-specific UBF1 transcription factor and inhibits ribosomal RNA transcription. EMBO J. 18, 2845-2854
43. Liu, C., Wang, H., Zhao, Z., Yu, S., Lu, Y. B., Meyer, J., Chatterjee, G., Deschamps, S., Roe, B. A., and Lengyel, P. (2000) MyoD-dependent induction during myoblast differentiation of p204, a protein also inducible by interferon. Mol. Cell. Biol. 20, 7024-7036
44. Chen, A. L., Fang, C., Liu, C., Leslie, M. P., Chang, E., and Di Cesare, P. E. (2004) Expression of bone morphogenetic proteins, receptors, and tissue inhibitors in human fetal, adult, and osteoarthritic articular cartilage. J. Orthop. Res. 22, 1188-1192
45. Di Cesare, P. E., Fang, C., Leslie, M. P., Della Valle, C. J., Gold, J. M., Tulli, H., Perris, R., and Carlson, C. S. (1999) Localization and expression of cartilage oligomeric matrix protein by human rheumatoid and osteoarthritic synovium and cartilage. J. Orthop. Res. 17, 437-445
46. Liu, C. J., Ding, B., Wang, H., and Lengyel, P. (2002) The MyoD-inducible p204 protein overcomes the inhibition of myoblast differentiation by Id proteins. Mol. Cell. Biol. 22, 2893-2905
47. Kellgren, J. H., and Lawrence, J. S. (1957) Radiological assessment of osteo-arthrosis. Ann. Rheum. Dis. 16, 494-502
48. Arnett, F. C., Edworthy, S. M., Bloch, D. A., McShane, D. J., Fries, J. F., Cooper, N. S., Healey, L. A., Kaplan, S. R., Liang, M. H., and Luthra, H. S. (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 31, 315-324
49. DiCesare, P., Hauser, N., Lehman, D., Pasumarti, S., and Paulsson, M. (1994b) Cartilage oligomeric matrix protein (COMP) is an abundant component of tendon. FEBS Lett. 354, 237-240
50. Somerville, R. P., Longpre, J. M., Apel, E. D., Lewis, R. M., Wang, L. W., Sanes, J. R., Leduc, R., and Apte, S. S. (2004) ADAMTS7B, the full-length product of the ADAMTS7 gene, is a chondroitin sulfate proteoglycan containing a mucin domain. J. Biol. Chem. 279, 35159-35175
51. Llamazares, M., Cal, S., Quesada, V., and Lopez-Otin, C. (2003) Identification and characterization of ADAMTS-20 defines a novel subfamily of metalloproteinases-disintegrins with multiple thrombospondin-1 repeats and a unique GON-domain. J. Biol. Chem. 31, 31
52. Chen, F. H. Thomas, A. O., Zhang, F, Hecht, J. T., and Lawler, J. (2004) Cartilage oligomeric matrix protein interaction with aggrecan. 50th Annual meeting of Orthopaedic Research Society, March 7-10, San Francisco, California
53. Di Cesare, P. E., Chen, F. S., Moergelin, M., Carlson, C. S., Leslie, M. P., Perris, R., and Fang, C. (2002) Matrix-matrix interaction of cartilage oligomeric matrix protein and fibronectin. Matrix Biol. 21, 461-470
54. Rosenberg, K., Olsson, H., Morgelin, M., and Heinegard, D. (1998) Cartilage oligomeric matrix protein shows high affinity zinc-dependent interaction with triple helical collagen. J. Biol. Chem. 273, 20397-20403
55. Mann, H. H., Ozbek, S., Engel, J., Paulsson, M., and Wagener, R. (2004) Interactions between the cartilage oligomeric matrix protein and matrilins. Implications for matrix assembly and the pathogenesis of chondrodysplasias. J. Biol. Chem. 279, 25294-25298
56. Hecht, J. T., Hayes, E., Snuggs, M., Decker, G., Montufar-Solis, D., Doege, K., Mwalle, F., Poole, R., Stevens, J., and Duke, P. J. (2001) Calreticulin, PDI, Grp94 and BiP chaperone proteins are associated with retained COMP in pseudoachondroplasia chondrocytes. Matrix Biol. 20, 251-262
57. Duke, J., Montufar-Solis, D., Underwood, S., Lalani, Z., and Hecht, J. T. (2003) Apoptosis staining in cultured pseudoachondroplasia chondrocytes. Apoptosis 8, 191-197
58. Vranka, J., Mokashi, A., Keene, D. R., Tufa, S., Corson, G., Sussman, M., Horton, W. A., Maddox, K., Sakai, L., and Bachinger, H. P. (2001) Selective intracellular retention of ECM proteins and chaperones associated with pseudoachondroplasia. Matrix Biol. 20, 439-450
59. Ozbek, S., Engel, J., and Stetefeld, J. (2002) Storage function of cartilage oligomeric matrix protein: the crystal structure of the coiled-coil domain in complex with vitamin D(3). EMBO J. 21, 5960-5968
60. Stracke, J. O., Fosang, A. J., Last, K., Mercuri, F. A., Pendas, A. M., Llano, E., Perris, R., Di Cesare, P. E., Murphy, G., and Knauper, V. (2000) Matrix metalloproteinases 19 and 20 cleave aggrecan and cartilage oligomeric matrix protein (COMP). FEBS Lett. 478, 52-56
61. Dickinson, S. C., Vankemmelbeke, M. N., Buttle, D. J., Rosenberg, K., Heinegard, D., and Hollander, A. P. (2003) Cleavage of cartilage oligomeric matrix protein (thrombospondin-5) by matrix metalloproteinases and a disintegrin and metalloproteinase with thrombospondin motifs. Matrix Biol. 22, 267-278
62. Bevitt, D. J., Mohamed, J., Catterall, J. B., Li, Z., Arris, C. E., Hiscott, P., Sheridan, C., Langton, K. P., Barker, M. D., Clarke, M. P., and McKie, N. (2003) Expression of ADAMTS metalloproteinases in the retinal pigment epithelium derived cell line ARPE-19: transcriptional regulation by TNFalpha. Biochim. Biophys. Acta 1626, 83-91
63. Martel-Pelletier, J., Welsch, D. J., and Pelletier, J. P. (2001) Metalloproteases and inhibitors in arthritic diseases. Best Pract. Res. Clin. Rheumatol. 15, 805-829
64. Flannery, C. R., Zeng, W., Corcoran, C., Collins-Racie, L. A., Chockalingam, P. S., Hebert, T., Mackie, S. A., McDonagh, T., Crawford, T. K., Tomkinson, K. N., LaVallie, E. R., and Morris, E. A. (2002) Autocatalytic cleavage of ADAMTS-4 (Aggrecanase-1) reveals multiple glycosaminoglycan-binding sites. J. Biol. Chem. 277, 42775-42780
65. Kashiwagi, M., Enghild, J. J., Gendron, C., Hughes, C., Caterson, B., Itoh, Y., and Nagase, H. (2004) Altered proteolytic activities of ADAMTS-4 expressed by C-terminal processing. J. Biol. Chem. 279, 10109-10119