MMP-mediated collagen breakdown induced by activated protein C in equine cartilage is reduced by corticosteroids

Journal of Orthopaedic Research

Volumn 28, Issue 3, 2010, Pages 370-378

  Garvican, Elaine R ^a   Vaughan Thomas, Anne ^a   Redmond, Colette ^a   Gabriel, Natalie ^a   Clegg, Peter D ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Activated protein C; Collagenolysis; Corticosteroid; MMP; Osteoarthritis

Indexed keywords

ACTIVATED PROTEIN C; COLLAGEN; COLLAGENASE 3; CORTICOSTEROID; DEXAMETHASONE; GELATINASE A; GLYCOSAMINOGLYCAN; HYDROXYPROLINE; INTERLEUKIN 1; MATRIX METALLOPROTEINASE; METHYLPREDNISOLONE ACETATE; SERINE PROTEINASE; TRIAMCINOLONE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL TISSUE; ARTICLE; CARTILAGE; CARTILAGE DEGENERATION; COLLAGEN DEGRADATION; DRUG MECHANISM; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL;

ADRENAL CORTEX HORMONES; ANIMALS; CARTILAGE; COLLAGEN; DEXAMETHASONE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; GLUCOCORTICOIDS; GLYCOSAMINOGLYCANS; HORSES; HUMANS; HYDROXYPROLINE; INTERLEUKIN-1; MATRIX METALLOPROTEINASES; METHYLPREDNISOLONE; PROTEIN C; RECOMBINANT PROTEINS; RNA, MESSENGER; SERINE PROTEASES; TIME FACTORS; TRIAMCINOLONE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 73949151911     PISSN: 07360266     EISSN: None     Source Type: Journal    
DOI: 10.1002/jor.21001     Document Type: Article

References (59)

1. Poole AR. 1996. Pathologic manifestations of joint disease in the athletic horse. In: McIllwraith CW, Trotter GW, editors. Joint disease in the horse. Philadelphia: WB Saunders. p 87-104.
2. Evans CH, Mears DC, Stanitski CL. 1982. Ferrographic analysis of wear in human joints. Evaluation by comparison with arthroscopic examination of symptomatic knees. J Bone Joint Surg [Br] 64:572-578.
3. Eyre D. 2002. Collagen of articular cartilage. Arthritis Res 4:30-35.
4. Roughley PJ. 2001. Articular cartilage and changes in arthritis - noncollagenous proteins and proteoglycans in the extracellular matrix of cartilage. Arthritis Res 3:342-347.
5. Billinghurst RC, Dahlberg L, Ionescu M, et al. 1997. Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J Clin Invest 99:1534-1545.
6. Goldring MB. 2000. The role of chondrocytes in osteoarthritis. Arthritis Rheum 43:1916-1926.
7. Pratta MA, Yao W, Decicco C, et al. 2003. Aggrecan protects cartilage collagen from proteolytic cleavage. J Biol Chem 278:45539-45545.
8. Wilson CG, Palmer AW, Zuo F, et al. 2006. Selective and nonselective metalloproteinase inhibitors reduce IL-1-induced cartilage degradation and loss of mechanical properties. Matrix Biol 26:259-268.
9. Tanabe S, Sugo T, Matsuda M. 1991. Synthesis of protein C in human umbilical vein endothelial cells. J Biochem 109:924-928.
10. Buisson-Legendre N, Smith S, March L, et al. 2004. Elevation of activated protein C in synovial joints in rheumatoid arthritis and its correlation with matrix metalloproteinase 2. Arthritis Rheum 50:2152-2156.
11. Joyce DE, Grinnell BW. 2002. Recombinant human activated protein C attenuates the inflammatory response in endothelium and monocytes by modulating nuclear factor-κB. Crit Care Med 30 (5 Suppl):S288-S293.
12. Toltl LJ, Shin LY, Liaw PC. 2007. Activated protein C in sepsis and beyond: update2006. Front Biosci 12:1963-1972.
13. Jackson C, Nguyen M, Arkell J, et al. 2001. Selective matrix metalloproteinase (MMP) inhibition in rheumatoid arthritis - targetting gelatinase A activation. Inflamm Res 50:183-186.
14. Xue M, March L, Sambrook P, et al. 2007. Differential regulation of matrix metalloproteinase 2 and matrix metalloproteinase 9 by activated protein C. Arthritis Rheum 56:2864-2874.
15. Cheng T, Petraglia AL, Li Z, et al. 2006. Activated protein C inhibits tissue plasminogen activator-induced brain hemorrhage. Nat Med 12:1278-1285.
16. Jackson MT, Smith MM, Smith SM, et al. 2009. Activation of cartilage matrix metalloproteinases by activated protein C. Arthritis Rheum 60:780-791.
17. Milner J, Rowan A, Cawston T. 2006. Metalloproteinase and inhibitor expression profiling of resorbing cartilage reveals pro-collagenase activation as a critical step for collagenolysis. Arthritis Res Ther 8:R142.
18. Milner JM, Elliott SF, Cawston TE. 2001. Activation of procollagenases is a key control point in cartilage collagen degradation: interaction of serine and metalloproteinase pathways. Arthritis Rheum 44:2084-2096.
19. Centeno LM, Moore ME. 1994. Preferred intraarticular corticosteroids and associated practice: a survey of members of the American College of Rheumatology. Arthritis Care Res 7:151-155.
20. Jones A, Doherty M. 1996. Intra-articular corticosteroids are effective in osteoarthritis but there are no clinical predictors of response. Ann Rheum Dis 55:829-832.
21. Frisbie DD, Kawcak CE, Trotter GW, et al. 1997. Effects of triamcinolone acetonide on an in vivo equine osteochondral fragment exercise model. Equine Vet J 29:349-359.
22. DiBattista JA, Martel-Pelletier J, Wosu LO, et al. 1991. Glucocorticoid receptor mediated inhibition of interleukin-1 stimulated neutral metalloproteinase synthesis in normal human chondrocytes. J Clin Endocrinol Metab 72:316-326.
23. Wheat JD. 1995. The use of hydrocortisone in the treatment of joint and tendon disorders in large animals. J Am Vet Med Assoc 127:64-67.
24. Creamer P. 1999. Intra-articular corticosteroid treatment in osteoarthritis. Curr Opin Rheumatol 11:417-421.
25. Trotter GW, McIlwriath CW, Yovich JV, et al. 1991. Effects of intraarticular administration of methylprednisolone acetate on normal equine articular cartilage. Am J Vet Res 52:83-87.
26. Shoemaker RS, Bertone AL, Martin GS, et al. 1992. Effects of intraarticular administration of methylprednisolone acetate on normal articular cartilage and on healing of experimentally induced osteochondral defects in horses. Am J Vet Res 53:1446-1453.
27. Jolly AC, Whittem T, Jolly AC, et al. 1995. The dose-related effects of phenylbutazone and a methylprednisolone acetate formulation (Depo-Medrol(R)) on cultured explants of equine carpal articular cartilage. J Vet Pharmacol Ther 18:429-437.
28. Silbermann M, von der Mark K, Maor G, et al. 1987. Dexamethasone impairs growth and collagen-synthesis in condylar cartilage in vitro. Bone Miner 2:87-106.
29. Murphy DJ, Todhunter RJ, Fubini SL, et al. 2000. The effects of methylprednisolone on normal and monocyte-conditioned medium-treated articular cartilage from dogs and horses. Vet Surg 29:546-557.
30. Frisbie DD, Nixon AJ. 1997. Insulin-like growth factor-1 and corticosteroid modulation of chondrocyte metabolic and mitogenic activity in interleukin-1 conditioned equine cartilage. Am J Vet Res 58:524-530.
31. Sandler EA, Frisbie DD, McIlwraith CW. 2004. A dose titration of triamcinolone acetonide on insulin-like growth factor-1 and interleukin-1- conditioned equine cartilage explants. Equine Vet J 36:58-63.
32. Pelletier JP, Mineau F, Raynauld JP, et al. 1994. Intraarticular injections with methylprednisolone acetate reduce osteoarthritic lesions in parallel with chondrocyte stromelysin synthesis in experimental osteoarthritis. Arthritis Rheum 37:414-423.
33. Stricker SJ, Lozman PR, Makowski AL, et al. 1996. Chondroprotective effect of betamethasone in lapine pyogenic arthritis. J Pediatr Orthop 16:231-236.
34. Richardson DW, Dodge GR. 2003. Dose-dependent effects of corticosteroids on the expression of matrix-related genes in normal and cytokine-treated articular chondrocytes. Inflamm Res 52:39-49.
35. Fubini S, Todhunter R, Burton-Wurster N, et al. 2001. Corticosteroids alter the differentiated phenotype of articular chondrocytes. J Orthop Res 19:688-695.
36. Dudhia J, Scott CM, Draper ER, et al. 2007. Aging enhances a mechanically-induced reduction in tendon strength by an active process involving matrix metalloproteinase activity. Aging Cell 6:547-560.
37. Farndale RW, Sayers CA, Barrett AJ. 1982. A direct spectrophotometric microassay for sulphated glycosaminoglycans in cartilage cultures. Connect Tissue Res 9:247-248.
38. Berg RA. 1982. Determination of 3- and 4-hydroxyproline. Methods Enzymol 82:372-398.
39. Knäuper V, López-Otin C, Smith B, et al. 1996. Biochemical characterization of human collagenase-3. J Biol Chem 271:1544-1550.
40. Garvican ER, Vaughan-Thomas A, Redmond C, et al. 2008. Chondrocytes harvested from osteochondritis dissecans cartilage are able to undergo limited in vitro chondrogenesis despite having perturbations of cell phenotype in vivo. J Orthop Res 26:1133-1140.
41. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method. Methods 25:402-408.
42. Clegg PD, Burke RM, Coughlan AR, et al. 1997. Characterisation of equine matrix metalloproteinase 2 and 9; and identification of the cellular sources of these enzymes in joints. Equine Vet J 29:335-342.
43. Martel-Pelletier J, Boileau C, Pelletier JP, et al. 2008. Cartilage in normal and osteoarthritic conditions. Best Pract Res Clin Rheumatol 22:351-384.
44. Sumer EU, Sondergaard BC, Rousseau JC, et al. 2007. MMP and non-MMP-mediated release of aggrecan and its fragments from articular cartilage: a comparative study of three different aggrecan and glycosaminoglycan assays. Osteoarthritis Cartilage 15:212-221.
45. Sugimoto K, Iizawa T, Harada H, et al. 2004. Cartilage degradation independent of MMP/aggrecanases. Osteoarthritis Cartilage 12:1006-1014.
46. Xue M, Thompson P, Kelso I, et al. 2004. Activated protein C stimulates proliferation, migration and wound closure, inhibits apoptosis and upregulates MMP-2 activity in cultured human keratinocytes. Exp Cell Res 299:119-127.
47. Knauper V, Will H, Lopez-Otin C, et al. 1996. Cellular mechanisms for human procollagenase-3 (MMP- 13) activation. Evidence that MT1-MMP (MMP-14) and gelatinase A (MMP-2) are able to generate active enzyme. J Biol Chem 271:17124-17131.
48. Dahlberg L, Billinghurst C, Manner P, et al. 2000. Collagenase-mediated cleavage of type II collagen is selectively enhanced I osteoarthritis cartilage and can be arrested with a synthetic inhibitor which spares collagenase-1 (MMP-1). Arthritis Rheum 43:673-682.
49. Minond D, Lauer-Fields JL, Cudic M. 2006. The roles of substrate thermal stability and P2 and P10 subsite identity on matrix metalloproteinase triple-helical peptidase activity and collagen specificity. J Biol Chem 281:38302-38313.
50. Gearing AJ, Beckett P, Christodoulou M, et al. 1994. Processing of tumour necrosis factor-a precursor by metalloproteinases. Nature 370:555-557.
51. Schonbeck U, Mach F, Libby P. 1998. Generation of biologically active IL-1 by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 processing. J Immunol 161:3340-3346.
52. Fukudome K, Esmon CT. 1994. Identification, cloning, and regulation of a novel endothelial cell protein C/activated protein C receptor. J Biol Chem 269:26486-26491.
53. Esmon CT. 2004. Structure and functions of the endothelial cell protein C receptor. Crit Care Med 32 (Suppl 5):S298-S301.
54. Yamane S, Cheng E, You Z, et al. 2007. Gene expression profiling of mouse articular and growth plate cartilage. Tissue Eng 13:2163-2173.
55. Riewald M, Petrovan RJ, Donner A, et al. 2002. Activation of endothelial cell protease activated receptor 1 by the protein C pathway. Science 296:1880-1882.
56. Kobayashi M, Squires GR, Mousa A, et al. 2005. Role of interleukin-1 and tumor necrosis factor- in matrix degradation of human osteoarthritic cartilage. Arthritis Rheum 52: 128-135.
57. Bau B, Gebhard PM, Haag J, et al. 2002. Relative messenger RNA expression profiling of collagenases and aggrecanases in human articular chondrocytes in vivo and in vitro. Arthritis Rheum 46:2648-2657.
58. Cortial D, Gouttenoire J, Rousseau CF, et al. 2006. Activation by IL-1 of bovine articular chondrocytes in culture within a 3D collagen-based scaffold. An in vitro model to address the effect of compounds with therapeutic potential in osteoarthritis. Osteoarthritis Cartilage 14:631-640.
59. Tung JT, Fenton JI, Arnold C, et al. 2002. Recombinant equine interleukin-1 induces putative mediators of articular cartilage degradation in equine chondrocytes. Can J Vet Res 66:19-25.