Analysis of ADAMTS4 and MT4-MMP indicates that both are involved in aggrecanolysis in interleukin-1-treated bovine cartilage

Osteoarthritis and Cartilage

Volumn 13, Issue 4, 2005, Pages 269-277

  Patwari, Parth ^a,e,f   Gao, G ^b   Lee, J H ^c   Grodzinsky, A J ^a,c   Sandy, J D ^b,d  

^a USA   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN   (United States)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f Partners Research Facility   (United States)

Author keywords

ADAMTS4; Aggrecan degradation; Esculetin; Mannosamine; MT4 MMP

Indexed keywords

AGGRECAN; AGGRECANASE; AGGRECANASE 1; AGGRECANASE 2; COLLAGENASE 3; ESCULETIN; GLYCOSYLPHOSPHATIDYLINOSITOL; INTERSTITIAL COLLAGENASE; MANNOSAMINE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 17; MESSENGER RNA; METALLOPROTEINASE; PROTEIN P53; PROTEIN P68; RECOMBINANT INTERLEUKIN 1ALPHA; STROMELYSIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; CATTLE; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; DEGRADATION KINETICS; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME RELEASE; EXPLANT; FEMUR; GENE EXPRESSION REGULATION; NEWBORN; NONHUMAN; PATELLA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; TIME; WESTERN BLOTTING;

ADAM PROTEINS; AGGRECANS; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CARTILAGE, ARTICULAR; CATTLE; EXTRACELLULAR MATRIX PROTEINS; INTERLEUKIN-1; LECTINS, C-TYPE; MATRIX METALLOPROTEINASES; POLYMERASE CHAIN REACTION; PROCOLLAGEN N-ENDOPEPTIDASE; PROTEOGLYCANS; RECOMBINANT PROTEINS; TISSUE CULTURE TECHNIQUES; UMBELLIFERONES;

EID: 14944371238     PISSN: 10634584     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.joca.2004.10.023     Document Type: Article

References (50)

1. M.D. Buschmann A.J. Grodzinsky A molecular model of proteoglycan-associated electrostatic forces in cartilage mechanics J Biomech Eng 117 1995 179-192
2. G. Gao J. Westling V.P. Thompson T.D. Howell P.E. Gottschall J.D. Sandy Activation of the proteolytic activity of ADAMTS4 (aggrecanase-1) by C-terminal truncation J Biol Chem 277 2002 11034-11041
3. Yamaji N, Nishimura K, Abe K, Ohara O, Nagase T, Nomura N, inventors; Yamanouchi Pharmaceutical Co., Ltd., Tokyo, Japan, and Kazusa DNA Research Institute, Chiba, Japan, assignee. Novel Metalloprotease having Aggrecanase Activity. US patent 6716613. April 6, 2004.
4. L.A. Collins-Racie C.R. Flannery W. Zeng C. Corcoran B. Annis-Freeman M.J. Agostino et al. ADAMTS-8 exhibits aggrecanase activity and is expressed in human articular cartilage Matrix Biol 23 2004 219-230
5. S.S. Apte A disintegrin-like and metalloprotease (reprolysin type) with thrombospondin type 1 motifs: The ADAMTS family Int J Biochem Cell Biol 36 2004 981-985
6. M. Llamazares S. Cal V. Quesada C. Lopez-Otin 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 278 2003 13382-13389
7. M.A. Pratta P.A. Scherle G. Yang R.Q. Liu R.C. Newton Induction of aggrecanase 1 (ADAM-TS4) by interleukin-1 occurs through activation of constitutively produced protein Arthritis Rheum 48 2003 119-133
8. E.C. Arner C.E. Hughes C.P. Decicco B. Caterson M.D. Tortorella Cytokine-induced cartilage proteoglycan degradation is mediated by aggrecanase Osteoarthritis Cartilage 6 1998 214-228
9. M.D. Tortorella A.M. Malfait C. Deccico E. Arner The role of ADAM-TS4 (aggrecanase-1) and ADAM-TS5 (aggrecanase-2) in a model of cartilage degradation Osteoarthritis Cartilage 9 2001 539-552
10. J. Westling A.J. Fosang K. Last V.P. Thompson K.N. Tomkinson T. Hebert et al. ADAMTS4 cleaves at the aggrecanase site (Glu373-Ala374) and secondarily at the matrix metalloproteinase site (Asn341-Phe342) in the aggrecan interglobular domain J Biol Chem 277 2002 16059-16066
11. J.D. Sandy C.R. Flannery P.J. Neame L.S. Lohmander The structure of aggrecan fragments in human synovial fluid. Evidence for the involvement in osteoarthritis of a novel proteinase which cleaves the Glu 373-Ala 374 bond of the interglobular domain J Clin Invest 89 1992 1512-1516
12. J.D. Sandy C. Verscharen Analysis of aggrecan in human knee cartilage and synovial fluid indicates that aggrecanase (ADAMTS) activity is responsible for the catabolic turnover and loss of whole aggrecan whereas other protease activity is required for C-terminal processing in vivo Biochem J 358 2001 615-626
13. P. Wang M. Tortorella K. England A.M. Malfait G. Thomas L. Arner Proprotein convertase furin interacts with and cleaves pro-ADAMTS4 (aggrecanase-1) in the trans-Golgi network J Biol Chem 2004
14. M. Kashiwagi J.J. Enghild C. Gendron C. Hughes B. Caterson Y. Itoh et al. Altered proteolytic activities of ADAMTS-4 expressed by C-terminal processing J Biol Chem 279 2004 10109-10119
15. C.R. Flannery W. Zeng C. Corcoran L.A. Collins-Racie P.S. Chockalingam T. Hebert et al. Autocatalytic cleavage of ADAMTS-4 (aggrecanase-1) reveals multiple glycosaminoglycan-binding sites J Biol Chem 277 2002 42775-42780
16. J.D. Sandy V. Thompson C. Verscharen D. Gamett Chondrocyte-mediated catabolism of aggrecan: Evidence for a glycosylphosphatidylinositol-linked protein in the aggrecanase response to interleukin-1 or retinoic acid Arch Biochem Biophys 367 1999 258-264
17. Y. Itoh M. Kajita H. Kinoh H. Mori A. Okada M. Seiki Membrane type 4 matrix metalloproteinase (MT4-MMP, MMP-17) is a glycosylphosphatidylinositol-anchored proteinase J Biol Chem 274 1999 34260-34266
18. G. Gao A. Plaas V.P. Thompson S. Jin F. Zuo J.D. Sandy ADAMTS4 (aggrecanase-1) activation on the cell surface involves C-terminal cleavage by glycosylphosphatidyl inositol-anchored membrane type 4-matrix metalloproteinase and binding of the activated proteinase to chondroitin sulfate and heparan sulfate on syndecan-1 J Biol Chem 279 2004 10042-10051
19. M. Sabatini M. Thomas C. Deschamps C. Lesur G. Rolland G. de Nanteuil et al. Effects of ceramide on aggrecanase activity in rabbit articular cartilage Biochem Biophys Res Commun 283 2001 1105-1110
20. M.Z. Ilic B. Martinac C.J. Handley Effects of long-term exposure to glucosamine and mannosamine on aggrecan degradation in articular cartilage Osteoarthritis Cartilage 11 2003 613-622
21. S. Elliott A.D. Rowan S. Carrere P. Koshy J.B. Catterall T.E. Cawston Esculetin inhibits cartilage resorption induced by interleukin 1alpha in combination with oncostatin M Ann Rheum Dis 60 2001 158-165
22. M.P. Lisanti M.C. Field I.W. Caras A.K. Menon E. Rodriguez-Boulan Mannosamine, a novel inhibitor of glycosylphosphatidylinositol incorporation into proteins EMBO J 10 1991 1969-1977
23. K. Watanabe A. Ito T. Sato T. Saito H. Hayashi Y. Niitani Esculetin suppresses proteoglycan metabolism by inhibiting the production of matrix metalloproteinases in rabbit chondrocytes Eur J Pharmacol 370 1999 297-305
24. J.D. Sandy P.J. Neame R.E. Boynton C.R. Flannery Catabolism of aggrecan in cartilage explants. Identification of a major cleavage site within the interglobular domain J Biol Chem 266 1991 8683-8685
25. R.L. Sah Y.J. Kim J.Y. Doong A.J. Grodzinsky A.H. Plaas J.D. Sandy Biosynthetic response of cartilage explants to dynamic compression J Orthop Res 7 1989 619-636
26. J.D. Sandy D. Gamett V. Thompson C. Verscharen Chondrocyte-mediated catabolism of aggrecan: Aggrecanase-dependent cleavage induced by interleukin-1 or retinoic acid can be inhibited by glucosamine Biochem J 335 Pt 1 1998 59-66
27. J.D. Sandy Proteoglycan core proteins and catabolic fragments present in tissues and fluids Methods Mol Biol 171 2001 335-345
28. J.B. Fitzgerald M. Jin D. Dean D.J. Wood M.H. Zheng A.J. Grodzinsky Mechanical compression of cartilage explants induces multiple time-dependent gene expression patterns and involves intracellular calcium and cyclic AMP J Biol Chem 2004
29. P. Patwari B. Kurz J.D. Sandy A.J. Grodzinsky Mannosamine inhibits aggrecanase-mediated changes in the physical properties and biochemical composition of articular cartilage Arch Biochem Biophys 374 2000 79-85
30. L.J. Bonassar J.D. Sandy M.W. Lark A.H. Plaas E.H. Frank A.J. Grodzinsky Inhibition of cartilage degradation and changes in physical properties induced by IL-1beta and retinoic acid using matrix metalloproteinase inhibitors Arch Biochem Biophys 344 1997 404-412
31. H. Oshita J.D. Sandy K. Suzuki A. Akaike Y. Bai T. Sasaki Mature bovine articular cartilage contains abundant aggrecan that is C-terminally truncated at Ala719-Ala720, a site which is readily cleaved by m-calpain Biochem J 382 2004 253-259
32. M.D. Tortorella R.Q. Liu T. Burn R.C. Newton E. Arner Characterization of human aggrecanase 2 (ADAM-TS5): Substrate specificity studies and comparison with aggrecanase 1 (ADAM-TS4) Matrix Biol 21 2002 499-511
33. J.D. Sandy J. Westling R.D. Kenagy M.L. Iruela-Arispe C. Verscharen J.C. Rodriguez-Mazaneque et al. 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 2001 13372-13378
34. K. Kuno Y. Okada H. Kawashima H. Nakamura M. Miyasaka H. Ohno et al. ADAMTS-1 cleaves a cartilage proteoglycan, aggrecan FEBS Lett 478 2000 241-245
35. R.P. Somerville J.M. Longpre K.A. Jungers J.M. Engle M. Ross S. Evanko et al. Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1 J Biol Chem 278 2003 9503-9513
36. Z. Dong M. Katar S. Alousi R.S. Berk Expression of membrane-type matrix metalloproteinases 4, 5, and 6 in mouse corneas infected with P. aeruginosa Invest Ophthalmol Vis Sci 42 2001 3223-3227
37. H. Yamada K. Watanabe T. Saito H. Hayashi Y. Niitani T. Kikuchi et al. Esculetin (dihydroxycoumarin) inhibits the production of matrix metalloproteinases in cartilage explants, and oral administration of its prodrug, CPA-926, suppresses cartilage destruction in rabbit experimental osteoarthritis J Rheumatol 26 1999 654-662
38. C.P. Blobel Functional and biochemical characterization of ADAMs and their predicted role in protein ectodomain shedding Inflamm Res 51 2002 83-84
39. R.J. Smith S.C. Speziale B.J. Bowman Properties of interleukin-1 as a complete secretagogue for human neutrophils Biochem Biophys Res Commun 130 1985 1233-1240
40. E.C. Arner M.A. Pratta J.M. Trzaskos C.P. Decicco M.D. Tortorella Generation and characterization of aggrecanase. A soluble, cartilage-derived aggrecan-degrading activity J Biol Chem 274 1999 6594-6601
41. D.J. Buttle C.J. Handley M.Z. Ilic J. Saklatvala M. Murata A.J. Barrett Inhibition of cartilage proteoglycan release by a specific inactivator of cathepsin B and an inhibitor of matrix metalloproteinases. Evidence for two converging pathways of chondrocyte-mediated proteoglycan degradation Arthritis Rheum 36 1993 1709-1717
42. K.M. Bottomley N. Borkakoti D. Bradshaw P.A. Brown M.J. Broadhurst J.M. Budd et al. Inhibition of bovine nasal cartilage degradation by selective matrix metalloproteinase inhibitors Biochem J 323 Pt 2 1997 483-488
43. C.B. Little L. Mittaz C.T. Meeker M. Pritchard A.J. Fosang ADAMTS-1 knockout mice do not exhibit abnormalities in aggrecan turnover in-vivo or in-vitro (Abstract) Trans Orthop Res Soc 29 2004 608
44. S.S. Glasson R. Askew B. Sheppard B.A. Carito T. Blanchet H.-K. Ma et al. Characterization of and osteoarthritis susceptibility in ADAMTS-4-knockout mice Arthritis Rheum 50 2004 2547-2558
45. J. Takeda T. Miyata K. Kawagoe Y. Iida Y. Endo T. Fujita et al. Deficiency of the GPI anchor caused by a somatic mutation of the PIG-A gene in paroxysmal nocturnal hemoglobinuria Cell 73 1993 703-711
46. S. Netzel-Arnett J.D. Hooper R. Szabo E.L. Madison J.P. Quigley T.H. Bugge et al. Membrane anchored serine proteases: A rapidly expanding group of cell surface proteolytic enzymes with potential roles in cancer Cancer Metastasis Rev 22 2003 237-258
47. R. Lang M. Braun N.E. Sounni A. Noel F. Frankenne J.M. Foidart et al. Crystal structure of the catalytic domain of MMP-16/MT3-MMP: characterization of MT-MMP specific features J Mol Biol 336 2004 213-225
48. Y. Wang A.R. Johnson Q.Z. Ye R.D. Dyer Catalytic activities and substrate specificity of the human membrane type 4 matrix metalloproteinase catalytic domain J Biol Chem 274 1999 33043-33049
49. V. Ganu R. Melton W. Wang D. Roberts Matrix metalloproteinase inhibitor CGS 27023A protects COMP and proteoglycan in the bovine articular cartilage but not the release of their fragments from cartilage after prolonged stimulation in vitro with IL-1 alpha Ann N Y Acad Sci 878 1999 607-611
50. T.M. Hering J. Kollar T.D. Huynh Complete coding sequence of bovine aggrecan: Comparative structural analysis Arch Biochem Biophys 345 1997 259-270