Human osteoarthritis synovial fluid and joint cartilage contain both aggrecanase- and matrix metalloproteinase-generated aggrecan fragments

Osteoarthritis and Cartilage

Volumn 14, Issue 2, 2006, Pages 101-113

  Struglics, A ^a   Larsson, S ^a   Pratta, M A ^b   Kumar, S ^b   Lark, M W ^c   Lohmander, L Stefan ^a  

^a LUND UNIVERSITY   (Sweden)

^b GLAXOSMITHKLINE   (United States)

^c CENTOCOR INC   (United States)

Author keywords

Aggrecan; Aggrecanase; Cartilage; Matrix metalloproteinase; Osteoarthritis; Synovial fluid

Indexed keywords

AGGRECAN; AGGRECANASE; ANTIBODY; CESIUM CHLORIDE; EPITOPE; GLYCOSAMINOGLYCAN; MATRIX METALLOPROTEINASE; STROMELYSIN;

AMINO TERMINAL SEQUENCE; ARTICLE; ARTICULAR CARTILAGE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; HUMAN; IN VITRO STUDY; KNEE OSTEOARTHRITIS; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SYNOVIAL FLUID; WESTERN BLOTTING;

AGGRECANS; ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; CARTILAGE, ARTICULAR; ENDOPEPTIDASES; EXTRACELLULAR MATRIX PROTEINS; GLYCOSAMINOGLYCANS; HUMANS; KNEE JOINT; LECTINS, C-TYPE; MATRIX METALLOPROTEINASES; OSTEOARTHRITIS; PEPTIDE FRAGMENTS; PROTEASE INHIBITORS; PROTEOCHONDROITIN SULFATES; SYNOVIAL FLUID;

EID: 30544448357     PISSN: 10634584     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.joca.2005.07.018     Document Type: Article

References (44)

1. 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 5 1992 1512-1516
2. L.S. Lohmander P.J. Neame J.D. Sandy The structure of aggrecan fragments in human synovial fluid. Evidence that aggrecanase mediates cartilage degradation in inflammatory joint disease, joint injury, and osteoarthritis Arthritis Rheum 36 9 1993 1214-1222
3. K.J. Doege M. Sasaki T. Kimura Y. Yamada Complete coding sequence and deduced primary structure of the human cartilage large aggregating proteoglycan, aggrecan. Human-specific repeats, and additional alternatively spliced forms J Biol Chem 266 2 1991 894-902
4. C.R. Flannery M.W. Lark J.D. Sandy Identification of a stromelysin cleavage site within the interglobular domain of human aggrecan. Evidence for proteolysis at this site in vivo in human articular cartilage J Biol Chem 267 2 1992 1008-1014
5. A.J. Fosang K. Last V. Knauper G. Murphy P.J. Neame Degradation of cartilage aggrecan by collagenase-3 (MMP-13) FEBS Lett 380 1-2 1996 17-20
6. A.M. Malfait R.Q. Liu K. Ijiri S. Komiya M.D. Tortorella Inhibition of ADAM-TS4 and ADAM-TS5 prevents aggrecan degradation in osteoarthritic cartilage J Biol Chem 277 25 2002 22201-22208
7. A.J. Fosang K. Last V. Knauper P.J. Neame G. Murphy T.E. Hardingham et al. Fibroblast and neutrophil collagenases cleave at two sites in the cartilage aggrecan interglobular domain Biochem J 295 Pt 1 1993 273-276
8. C.R. Flannery J.D. Sandy Aggrecan catabolism in cartilage: Studies on the nature of a novel proteinase (aggrecanase) which cleaves the Glu373-Ala374 bond of the interglobular domain (Abstract) Trans Orthop Res Soc 17 1993 677
9. L.J. Bonassar E.H. Frank J.C. Murray C.G. Paguio V.L. Moore M.W. Lark et al. Changes in cartilage composition and physical properties due to stromelysin degradation Arthritis Rheum 38 2 1995 173-183
10. M.D. Tortorella M. Pratta R.Q. Liu J. Austin O.H. Ross I. Abbaszade et al. Sites of aggrecan cleavage by recombinant human aggrecanase-1 (ADAMTS-4) J Biol Chem 275 24 2000 18566-18573
11. 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 6 2002 499-511
12. J.C. Rodriguez-Manzaneque J. Westling S.N. Thai A. Luque V. Knauper G. Murphy et al. ADAMTS1 cleaves aggrecan at multiple sites and is differentially inhibited by metalloproteinase inhibitors Biochem Biophys Res Commun 293 1 2002 501-508
13. A.J. Fosang K. Last R.A. Maciewicz Aggrecan is degraded by matrix metalloproteinases in human arthritis. Evidence that matrix metalloproteinase and aggrecanase activities can be independent J Clin Invest 98 10 1996 2292-2299
14. 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 Pt 3 2001 615-626
15. M.W. Lark E.K. Bayne J. Flanagan C.F. Harper L.A. Hoerrner N.I. Hutchinson et al. Aggrecan degradation in human cartilage. Evidence for both matrix metalloproteinase and aggrecanase activity in normal, osteoarthritic, and rheumatoid joints J Clin Invest 100 1 1997 93-106
16. S.S. Glasson R. Askew B. Sheppard B. Carito T. Blanchet H.L. Ma et al. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis Nature 434 7033 2005 644-648
17. H. Stanton F.M. Rogerson C.J. East S.B. Golub K.E. Lawlor C.T. Meeker et al. ADAMTS5 is the major aggrecanase in mouse cartilage in vivo and in vitro Nature 434 7033 2005 648-652
18. M.D. Tortorella T.C. Burn M.A. Pratta I. Abbaszade J.M. Hollis R. Liu et al. Purification and cloning of aggrecanase-1: A member of the ADAMTS family of proteins Science 284 5420 1999 1664-1666
19. S. Bjornsson Simultaneous preparation and quantitation of proteoglycans by precipitation with Alcian Blue Anal Biochem 210 2 1993 282-291
20. J.D. Sandy A.H. Plaas T.J. Koob Pathways of aggrecan processing in joint tissues. Implications for disease mechanism and monitoring Acta Orthop Scand Suppl 266 1995 26-32
21. M.L. Lemons J.D. Sandy D.K. Anderson D.R. Howland Intact aggrecan and fragments generated by both aggrecanase and metalloproteinase-like activities are present in the developing and adult rat spinal cord and their relative abundance is altered by injury J Neurosci 21 13 2001 4772-4781
22. M.W. Lark J.T. Gordy J.R. Weidner J. Ayala J.H. Kimura H.R. Williams et al. Cell-mediated catabolism of aggrecan. Evidence that cleavage at the "aggrecanase" site (Glu373-Ala374) is a primary event in proteolysis of the interglobular domain J Biol Chem 270 6 1995 2550-2556
23. H. Stanton A.J. Fosang Matrix metalloproteinases are active following guanidine hydrochloride extraction of cartilage: Generation of DIPEN neoepitope during dialysis Matrix Biol 21 5 2002 425-428
24. H. Oshita J.D. Sandy K. Suzuki A. Akaike Y. Bai T. Sasaki et al. 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 Pt 1 2004 253-259
25. 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 18 2002 16059-16066
26. J.M. Day A.I. Olin A.D. Murdoch A. Canfield T. Sasaki R. Timpl et al. Alternative splicing in the aggrecan G3 domain influences binding interactions with tenascin-C and other extracellular matrix proteins J Biol Chem 279 13 2004 12511-12518
27. C.J. Poon A.H. Plaas D.R. Keene D.J. McQuillan K. Last A.J. Fosang N-linked keratan sulphate in the aggrecan interglobular domain potentiates aggrecanase activity J Biol Chem 2005
28. 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 11 2004 10109-10119
29. G. Hashimoto M. Shimoda Y. Okada ADAMTS4 (aggrecanase-1) interaction with the C-terminal domain of fibronectin inhibits proteolysis of aggrecan J Biol Chem 279 31 2004 32483-32491
30. M. Kashiwagi M. Tortorella H. Nagase K. Brew TIMP-3 is a potent inhibitor of aggrecanase 1 (ADAM-TS4) and aggrecanase 2 (ADAM-TS5) J Biol Chem 276 16 2001 12501-12504
31. M.Z. Ilic M.T. Mok O.D. Williamson M.A. Campbell C.E. Hughes C.J. Handley Catabolism of aggrecan by explant cultures of human articular cartilage in the presence of retinoic acid Arch Biochem Biophys 322 1 1995 22-30
32. H. Hedlund E. Hedbom D. Heinegård S. Mengarelli-Widholm F.P. Reinholt O. Svensson Association of the aggrecan keratan sulfate-rich region with collagen in bovine articular cartilage J Biol Chem 274 9 1999 5777-5781
33. M.A. Pratta W. Yao C. Decicco M.D. Tortorella R.Q. Liu R.A. Copeland et al. Aggrecan protects cartilage collagen from proteolytic cleavage J Biol Chem 278 46 2003 45539-45545
34. J.J. Embry W. Knudson G1 domain of aggrecan cointernalizes with hyaluronan via a CD44-mediated mechanism in bovine articular chondrocytes Arthritis Rheum 48 12 2003 3431-3441
35. F.P. Barry L.C. Rosenberg J.U. Gaw T.J. Koob P.J. Neame N- and O-linked keratan sulfate on the hyaluronan binding region of aggrecan from mature and immature bovine cartilage J Biol Chem 270 35 1995 20516-20524
36. A.J. Fosang P.J. Neame K. Last T.E. Hardingham G. Murphy J.A. Hamilton The interglobular domain of cartilage aggrecan is cleaved by PUMP, gelatinases, and cathepsin B J Biol Chem 267 27 1992 19470-19474
37. A.J. Fosang K. Last H. Stanton D.B. Weeks I.K. Campbell T.E. Hardingham et al. Generation and novel distribution of matrix metalloproteinase-derived aggrecan fragments in porcine cartilage explants J Biol Chem 275 42 2000 33027-33037
38. A.J. Fosang K. Last P. Gardiner D.C. Jackson L. Brown Development of a cleavage-site-specific monoclonal antibody for detecting metalloproteinase-derived aggrecan fragments: Detection of fragments in human synovial fluids Biochem J 310 Pt 1 1995 337-343
39. S. Lohmander C.A. Antonopoulos U. Friberg Chemical and metabolic heterogeneity of chondroitin sulfate and keratin sulfate in guinea pig cartilage and nucleus pulposus Biochim Biophys Acta 304 2 1973 430-448
40. S. Lohmander Turnover of proteoglycans in guinea pig costal cartilage Arch Biochem Biophys 180 1 1977 93-101
41. S.S. Mok K. Masuda H.J. Hauselmann M.B. Aydelotte E.J. Thonar Aggrecan synthesized by mature bovine chondrocytes suspended in alginate. Identification of two distinct metabolic matrix pools J Biol Chem 269 52 1994 33021-33027
42. M.Z. Ilic S.R. Haynes G.M. Winter C.J. Handley Kinetics of release of aggrecan from explant cultures of bovine cartilage from different sources and from animals of different ages Acta Orthop Scand Suppl 266 1995 33-37
43. V.C. Hascall J.D. Sandy C.J. Handley Regulation of proteoglycan metabolism in articular cartilage C.W. Archer B. Caterson M. Benjamin J.R. Ralphs Biology of the Synovial Joint 1999 Harwood Academic Publishers Cardiff 101-120
44. P.S. Chockalingam W. Zeng E.A. Morris C.R. Flannery Release of hyaluronan and hyaladherins (aggrecan G1 domain and link proteins) from articular cartilage exposed to ADAMTS-4 (aggrecanase 1) or ADAMTS-5 (aggrecanase 2) Arthritis Rheum 50 9 2004 2839-2848