Aggrecan degradation in human cartilage: Evidence for both matrix metalloproteinase and aggrecanase activity in normal, osteoarthritic, and rheumatoid joints

Journal of Clinical Investigation

Volumn 100, Issue 1, 1997, Pages 93-106

  Lark, Michael W ^a,c   Bayne, Ellen K ^a   Flanagan, Jamie ^a   Harper, Coral F ^a   Hoerrner, Lori A ^a   Hutchinson, Nancy I ^a   Singer, Irwin I ^a   Donatelli, Susan A ^a   Weidner, Jeffrey R ^a   Williams, Hollis R ^a   Mumford, Richard A ^a   Lohmander, L Stefan ^b  

^a MERCK RESEARCH LABORATORIES   (United States)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

^c GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Aggrecan; Aggrecanase; Cartilage; Matrix metalloproteinases; Osteoarthritis

Indexed keywords

AGGRECAN; MATRIX METALLOPROTEINASE;

ARTICLE; ARTICULAR CARTILAGE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN TISSUE; OSTEOARTHRITIS; PATHOGENESIS; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS;

EID: 18744437369     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119526     Document Type: Article

References (48)

1. Dean, D.D., J. Martel-Pelletier, J.-P. Pelletier, D.S. Howell, and J.F.J. Woessner. 1989. Evidence for metalloproteinase and metalloproteinase inhibitor imbalance in human osteoarthritic cartilage. J. Clin. Invest. 84:678-685.
2. Gravallese, E.M, J.M. Darling, A.L. Ladd, J.N. Katz, and L.H. Glimcher. 1991. In situ hybridization studies of stromelysin and collagenase expression in rheumatoid synovium. Arthritis Rheum. 34:1076-1084.
3. McCachren, S.S. 1991. Expression of metalloproteinases and metalloproteinase inhibitor in human arthritic synovium. Arthritis Rheum. 34:1085-1093.
4. Firestein, G.S., M.M. Paine, and B.H. Littman. 1991. Gene expression (collagenase, tissue inhibitor of metalloproteinases, complement, and HLA-DR) in rheumatoid arthritis and osteoarthritis synovium. Quantitative analysis and effect of intraarticular corticosteroids. Arthritis Rheum. 34:1094-1105.
5. Walakovits, L.A., V.L. Moore, N. Bhardwaj, G.S. Gallick, and M.W. Lark. 1991. Detection of high levels of stromelysin and collagenase in synovial fluid from patients with rheumatoid arthritis and post-traumatic knee injury. Arthritis Rheum. 35:35-42.
6. Nguyen, Q., J.S. Mort, and P.J. Roughley. 1992. Preferential mRNA expression of prostromelysin relative to procollagenase and in situ localization in human articular cartilage. J. Clin. Invest. 89:1189-1197.
7. Lohmander, L.S., L.A. Hoerrner, and M.W. Lark. 1993. Metalloproteinases, tissue inhibitor and proteoglycan fragments in knee synovial fluid in human osteoarthritis. Arthritis Rheum. 36:181-189.
8. Wolfe, G.C., K.L. MacNaul, F.F. Buechel, J. McDonnell, L.A. Hoerrner, M.W. Lark, V.L. Moore, and N.I. Hutchinson. 1993. Differential in vivo expression of collagenase messenger RNA in synovium and cartilage. Quantitative comparison with stromelysin messenger RNA levels in human rheumatoid arthritis and osteoarthritis patients and in two animal models of acute inflammatory arthritis. Arthritis Rheum. 36:1540-1547.
9. Lohmander, L.S., L.A. Hoerrner, and M.W. Lark. 1995. Increased concentrations of collagenase (MMP-1) in joint fluid after knee injury and in osteoarthritis. Trans. Orthop. Res. Soc. 20:9. (Abstr.)
10. Nguyen, Q., G. Murphy, P.J. Roughley, and J.S. Mort. 1989. Degradation of proteoglycan aggregate by a cartilage metalloproteinase. Evidence for the involvement of stromelysin in the generation of link protein heterogeneity in situ. Biochem. J. 259:61-67.
11. Flannery, C.R., M.W. Lark, and J.D. Sandy. 1992. 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. 267:1008-1014.
12. Fosang, A.J., K. Last, V. Knäuper, P.J. Neame, G. Murphy, T.E. Hardingham, H. Tschesche, and J.A. Hamilton. 1993. Fibroblast and neutrophil collagenases cleave at two sites in the cartilage aggrecan interglobular domain. Biochem. J. 295:273-276.
13. Fosang, A.J., P.J. Neame, T.E. Hardingham, G. Murphy, and J.A. Hamilton. 1991. Cleavage of cartilage proteoglycan between G1 and G2 domains by stromelysin. J. Biol. Chem. 266:15579-15582.
14. Wu, J.-J., M.W. Lark, L.E. Chun, and D.R. Eyre. 1991. Sites of stromelysin cleavage in collagen types II, IX, X, and XI of cartilage. J. Biol. Chem. 266: 5625-5628.
15. Liu, J.J., D. Cassidy, A. Allan, P.J. Neame, J.S. Mort, and P.J. Roughley. 1992. Link protein shows species variation in its susceptibility to proteolysis. J. Orthop Res. 10:621-630.
16. Hollander, A.P., T.F. Heathfield, C. Webber, Y. Iwata, R. Bourne, C. Rorabeck, and A.R. Poole. 1994. Increased damage to type II collagen in osteoarthritic cartilage detected by a new immunoassay. J. Clin. Invest. 93:1722-1732.
17. Roughley, P.J., R.J. White, and A.R. Poole. 1985. Identification of a hyaluronic acid-binding protein that interferes with the preparation of high-buoyant density proteoglycan aggregates from adult human articular cartilage. Biochem. J. 231:129-138.
18. Bayliss, M.T., M.W.A. Holmes, and H. Muir. 1989. Age-related changes in the stoichiometry of binding region, link protein and hyaluronic acid in human articular cartilage. Trans. Orthop. Res. Soc. 14:32. (Abstr.)
19. Sandy, J.D., P.J. Neame, R.E. Boynton, and C.R. Flannery. 1991. Catabolism of aggrecan in cartilage explants. Identification of a major cleavage site within the interglobular domain. J. Biol. Chem. 266:8683-8695.
20. Ilic, M.Z., C.H. Handley, H.C. Robinson, and M.T. Mok. 1992. Mechanism of catabolism of aggrecan by articular cartilage. Arch. Biochem. Biophys. 294:115-122.
21. Loulakis, P., A. Shrikande, G. Davis, and C.A. Maniglia. 1992. N-terminal sequence of proteoglycan fragments isolated from medium of interleukin-1-treated articular-cartilage cultures. Biochem. J. 284:589-593.
22. Plaas, A.H., and J.D. Sandy. 1993. A cartilage explant system for studies on aggrecan structure, biosynthesis and catabolism in discrete zones of the mammalian growth plate. Matrix. 13:135-147.
23. 374) is a primary event in proteolysis of the interglobular domain. J. Biol. Chem. 270:2550-2556.
24. Hughes, C.E., B. Caterson, A.J. Fosang, P.J. Roughley, and J.S. Mort. 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.
25. Lohmander, L.S., P. Neame, and J.D. Sandy. 1993. 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. 36:1214-1222.
26. Sandy, J.D., C.R. Flannery, P.J. Neame, and L.S. Lohmander. 1992. 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. 89:1512-1516.
27. Fosang, A.J., K. Last, P.J. Neame, G. Murphy, V. Knäuper, H. Tschesche, C. Hughes, B. Caterson, and T.E. Hardingham. 1994. Neutrophil collagenase (MMP-8) cleaves at the aggrecanase site E373-A-374 in the interglobular domain of cartilage aggrecan. Biochem. J. 304:347-351.
28. Lark, M.W., H. Williams, L.A. Hoerrner, J.R. Weidner, J.M. Ayala, C.F. Harper, A. Christen, J. Olszewski, Z. Konteatis, R. Webber, et al. 1995. Quantification of a matrix metalloproteinase-generated aggrecan G1 fragment using monospecific anti-peptide serum. Biochem. J. 307:245-252.
29. Doege, K.J., M. Sasaki, T. Kimura, and Y. Yamada. 1991. Complete coding sequence and deduced primary structure of the human cartilage large aggregating proteoglycan, aggrecan. J. Biol. Chem. 266:894-902.
30. Hascall, V.C., and J.H. Kimura. 1982. Proteoglycans: isolation and characterization. Methods Enzymol. 82:769-800.
31. Woessner, J.F., Jr. 1961. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch. Biochem. Biophys. 93:440-447.
32. MacLean, I.W., and P.K. Nakane. 1974. Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J. Histochem. Cytochem. 35:647-655.
33. Shu, S., G. Ju, and L. Fan. 1988. The glucose oxidase-DAB nickel method in peroxidase histochemistry of the nervous system. Neurosci. Lett. 85: 169-171.
34. Mankin, H.J., H. Dorfman, L. Lippiello, and A. Zarins. 1971. Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J. Bone Jt. Surg. (Am.) Vol. 53:523-537.
35. Lark, M.W., L.A. Walakovits, T.K. Shah, J. Vanmiddlesworth, P.M. Cameron, and T.-Y. Lin. 1990. Production and purification of prostromelysin and procollagenase from IL-1 beta-stimulated human gingival fibroblasts. Connect. Tissue Res. 25:49-65.
36. Teahan, J., R. Harrison, M. Izquierdo, and R.L. Stein. 1989. Substrate specificity of human fibroblast stromelysin. Hydrolysis of substance P and its analogues. Biochemistry. 28:8497-8501.
37. Singer, I.I., S. Scott, D.W. Kawka, E.K. Bayne, S.A. Donatelli, J.R. Weidner, H.R. Williams, R.A. Mumford, M.W. Lark, J. McDonnell, et al. 1995. Aggrecanase and metalloproteinase-specific aggrecan neoepitopes are induced in the articular cartilage of mice with collagen II arthritis. Trans. Orthop. Res. Soc. 20:330.
38. Fosang, A.J., K. Last, and R.A. Maciewicz. 1996. Aggrecan is degraded by matrix metalloproteinases in human arthritis. Evidence that matrix metalloproteinases and aggrecanase activities can be independent. J. Clin. Invest. 98: 2292-2299.
39. Lohmander, S. 1977. Turnover of proteoglycans in guinea pig costal cartilage. Arch. Biochem. Biophys. 180:93-101.
40. Sandy, J.D. 1992. Extracellular metabolism of aggrecan. In Articular Cartilage and Osteoarthritis. K.E. Kuettner, R. Schleyerbach, J.G. Peyron, and V.C. Hascall, editors. Raven Press, Ltd., New York, 21-33.
41. Mok, S.S., K. Masuda, H.J. Häuselmann, M.B. Aydelotte and E.J.-M.A. Thonar. 1994. Aggrecan synthesized by mature chondrocytes suspended in alginate. Identification of two distinct metabolic pools. J. Biol. Chem. 269:33021-33027.
42. Singer, I.I., D.W. Kawka, E.K. Bayne, S.A. Donatelli, J.R. Weidner, H.R. Williams, J.M. Ayala, R.A. Mumford, M.W. Lark, T.T. Glant, et al. 1995. VDIPEN, a metalloproteinase-generated neoepitope, is induced and immunolocalized in articular cartilage during inflammatory arthritis. J. Clin. Invest. 95:2178-2186.
43. Hollander, A.P., I. Pidoux, A. Reiner, C. Rorabeck, R. Bourne, and A.R. Poole. 1995. Damage to type II collagen in aging and osteoarthritis starts at the articular surface, originates around chondrocytes, and extends into the cartilage with progressive degeneration. J. Clin. Invest. 96:2859-2869.
44. Bayne, E.K, K.L. MacNaul, S.A. Donatelli, A. Christen, P.R. Griffin, L.A. Hoerrner, J.R. Calaycay, J.M. Ayala, K. Chapman, W. Hagmann, et al. 1995. Use of an antibody against the matrix metalloproteinase-generated aggrecan neoepitope FVDIPEN-COOH to assess the effects of stromelysin in a rabbit model of cartilage degradation. Arthritis Rheum. 38:1400-1409.
45. Saxne, T., and D. Heinegård. 1992. Synovial fluid analysis of two groups of proteoglycan epitopes distinguishes early and late cartilage lesions. Arthritis Rheum. 35:385-390.
46. Sandy, J.D., A.H.K. Plaas, and T.J. Koob. 1995. Pathways of aggrecan processing in joint tissues - implications for disease mechanism and monitoring. Acta Orthop. Scand. 66 (Suppl. 266):26-32.
47. Morales, T.I., and V.C. Hascall. 1988. Correlated metabolism of proleoglycans and hyaluronic acid in bovine articular cartilage organ cultures. J. Biol. Chem. 263:3632-3638.
48. Morales, T.I., and V.C. Hascall. 1989. Effects of interleukins and lipopolysaccharides on protein and carbohydrate metabolism in bovine articular cartilage organ cultures. Connect. Tissue Res. 19:255-275.