Inhibition of matrix metalloproteinases as a feasible therapeutic target in rheumatoid arthritis

Current Rheumatology Reviews

Volumn 4, Issue 4, 2008, Pages 288-297

  Zafarullah, Muhammad ^a   Ahmad, Rasheed ^a   El Mabrouk, Mohammed ^a   Liacini, Abdelhamid ^a   Qureshi, Hamid Yaqoob ^a  

^a NOTRE DAME HOSPITAL   (Canada)

Author keywords

Aggrecanases; Matrix metalloproteinases; Rheumatoid arthritis; Synthetic inhibitors; Tissue inhibitor metalloproteinases

Indexed keywords

AGGRECANASE; INTERLEUKIN 1; INTERLEUKIN 17; MATRIX METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR INHIBITOR;

ARTICLE; BIOAVAILABILITY; CARTILAGE DEGENERATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; IMMUNOGENICITY; INFLAMMATORY DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHEUMATOID ARTHRITIS; RNA TRANSLATION; SIGNAL TRANSDUCTION;

EID: 84874296190     PISSN: 15733971     EISSN: 18756360     Source Type: Journal    
DOI: 10.2174/157339708786263906     Document Type: Article

References (165)

1. Feldmann M. Pathogenesis of arthritis: recent research progress. Nat Immunol 2001; 2: 771-3.
2. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature 2003; 423: 356-61.
3. Plenge RM, Seielstad M, Padyukov L, et al. TRAF1-C5 as a risk locus for rheumatoid arthritis--a genomewide study. N Engl J Med 2007; 357: 1199-209.
4. Remmers EF, Plenge RM, Lee AT, et al. STAT4 and the risk of rheumatoid arthritis and systemic lupus erythematosus. N Engl J Med 2007; 357: 977-86.
5. Burrage PS, Mix KS, Brinckerhoff CE. Matrix metalloproteinases: role in arthritis. Front Biosci 2006; 11: 529-43.
6. Murphy G, Knauper V, Atkinson S, et al. Matrix metalloproteinases in arthritic disease. Arthritis Res 2002; 4(Suppl 3): S39-S49.
7. Bramono DS, Richmond JC, Weitzel PP, Kaplan DL, Altman GH. Matrix metalloproteinases and their clinical applications in orthopaedics. Clin Orthop Relat Res 2004; (428): 272-85.
8. Nagase H, Kashiwagi M. Aggrecanases and cartilage matrix degradation. Arthritis Res Ther 2003; 5: 94-103.
9. Little CB, Meeker CT, Golub SB, et al. Blocking aggrecanase cleavage in the aggrecan interglobular domain abrogates cartilage erosion and promotes cartilage repair. J Clin Invest 2007; 117: 1627-36.
10. Lindy O, Konttinen YT, Sorsa T, et al. Matrix metalloproteinase 13 (collagenase 3) in human rheumatoid synovium. Arthritis Rheum 1997; 40: 1391-9.
11. Wernicke D, Seyfert C, Gromnica-Ihle E, Stiehl P. The expression of collagenase 3 (MMP-13) mRNA in the synovial tissue is associated with histopathologic type II synovitis in rheumatoid arthritis. Autoimmunity 2006; 39: 307-13.
12. Westhoff CS, Freudiger D, Petrow P, et al. Characterization of collagenase 3 (matrix metalloproteinase 13) messenger RNA expression in the synovial membrane and synovial fibroblasts of patients with rheumatoid arthritis. Arthritis Rheum 1999; 42: 1517-27.
13. Ainola MM, Mandelin JA, Liljestrom MP, Li TF, Hukkanen MV, Konttinen YT. Pannus invasion and cartilage degradation in rheumatoid arthritis: involvement of MMP-3 and interleukin-1beta. Clin Exp Rheumatol 2005; 23: 644-50.
14. Konttinen YT, Ainola M, Valleala H, et al. Analysis of 16 different matrix metalloproteinases (MMP-1 to MMP-20) in the synovial membrane: different profiles in trauma and rheumatoid arthritis. Ann Rheum Dis 1999; 58: 691-7.
15. Fiedorczyk M, Klimiuk PA, Sierakowski S, Gindzienska-Sieskiewicz E, Chwiecko J. Serum matrix metalloproteinases and tissue inhibitors of metalloproteinases in patients with early rheumatoid arthritis. J Rheumatol 2006; 33: 1523-9.
16. Distler JH, Jungel A, Huber LC, et al. The induction of matrix metalloproteinase and cytokine expression in synovial fibroblasts stimulated with immune cell microparticles. Proc Natl Acad Sci USA 2005; 102: 2892-7.
17. McInnes IB, Schett G. Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol 2007; 7: 429-42.
18. Kobayashi M, Squires GR, Mousa A, et al. Role of interleukin-1 and tumor necrosis factor α in matrix degradation of human osteoarthritic cartilage. Arthritis Rheum 2005; 52: 128-35.
19. Goldring MB. The role of the chondrocyte in osteoarthritis. Arthritis Rheum 2000; 43: 1916-26.
20. Goldring MB, Goldring SR. Osteoarthritis. J Cell Physiol 2007; 213: 626-34.
21. Miossec P. Interleukin-17 in fashion, at last: ten years after its description, its cellular source has been identified. Arthritis Rheum 2007; 56: 2111-5.
22. Ye XJ, Tang B, Ma Z, et al. The effects of interleukin-18 on rat articular chondrocytes: a study of mRNA expression and protein synthesis of proinflammatory substances. Clin Exp Immunol 2007; 149: 553-60.
23. Shalom-Barak T, Quach J, Lotz M. Interleukin-17-induced gene expression in articular chondrocytes is associated with activation of mitogen-activated protein kinases and NF-κB. J Biol Chem 1998; 273: 27467-73.
24. Van den Berg WB. Arguments for interleukin 1 as a target in chronic arthritis. Ann Rheum Dis 2000; 59(Suppl 1): i81-4.
25. Maini RN, Elliott MJ, Brennan FM, et al. Monoclonal anti-TNF alpha antibody as a probe of pathogenesis and therapy of rheumatoid disease. Immunol Rev 1995; 144: 195-223.
26. Joosten LAB, Helsen MMA, Saxne T, van de Loo FAJ, Heinegård D, van den Berg WB. IL-1αβ blockade prevents cartilage and bone destruction in murine type II collagen-induced arthritis, whereas TNF-α blockade only ameliorates joint inflammation. J Immunol 1999; 163: 5049-55.
27. Zwerina J, Redlich K, Polzer K, et al. TNF-induced structural joint damage is mediated by IL-1. Proc Natl Acad Sci USA 2007; 104: 11742-7.
28. Westra J, Limburg PC, de BP, van Rijswijk MH. Effects of RWJ 67657, a p38 mitogen activated protein kinase (MAPK) inhibitor, on the production of inflammatory mediators by rheumatoid synovial fibroblasts. Ann Rheum Dis 2004; 63: 1453-9.
29. Hall JP, Kurdi Y, Hsu S, et al. Pharmacologic inhibition of TPL2 blocks inflammatory responses in primary human monocytes, synoviocytes, and blood. J Biol Chem 2007; 282: 33295-304.
30. Xue M, March L, Sambrook PN, Jackson CJ. Differential regulation of matrix metalloproteinase 2 and matrix metalloproteinase 9 by activated protein C: Relevance to inflammation in rheumatoid arthritis. Arthritis Rheum 2007; 56: 2864-74.
31. Abeles AM, Marjanovic N, Park J, et al. Protein isoprenylation regulates secretion of matrix metalloproteinase 1 from rheumatoid synovial fibroblasts: Effects of statins and farnesyl and geranylgeranyl transferase inhibitors. Arthritis Rheum 2007; 56: 2840-53.
32. Cha HS, Boyle DL, Inoue T, et al. A novel spleen tyrosine kinase inhibitor blocks c-Jun N-terminal kinase-mediated gene expression in synoviocytes. J Pharmacol Exp Ther 2006; 317: 571-8.
33. Dai SM, Shan ZZ, Nishioka K, Yudoh K. Implication of interleukin 18 in production of matrix metalloproteinases in articular chondrocytes in arthritis: direct effect on chondrocytes may not be pivotal. Ann Rheum Dis 2005; 64: 735-42.
34. Görtz B, Hayer S, Tuerck B, Zwerina J, Smolen JS, Schett G. Tumour necrosis factor activates the mitogen-activated protein kinases p38α and ERK in the synovial membrane in vivo. Arthritis Res Ther 2005; 7: R1140-R1147.
35. Zwerina J, Hayer S, Redlich K, et al. Activation of p38 MAPK is a key step in tumor necrosis factor-mediated inflammatory bone destruction. Arthritis Rheum 2006; 54: 463-72.
36. Medicherla S, Ma JY, Mangadu R, et al. A selective p38 alpha mitogen-activated protein kinase inhibitor reverses cartilage and bone destruction in mice with collagen-induced arthritis. J Pharmacol Exp Ther 2006; 318: 132-41.
37. Mbalaviele G, Anderson G, Jones A, et al. Inhibition of p38 mitogen-activated protein kinase prevents inflammatory bone destruction. J Pharmacol Exp Ther 2006; 317: 1044-53.
38. Saklatvala J. The p38 MAP kinase pathway as a therapeutic target in inflammatory disease. Curr Opin Pharmacol 2004; 4: 372-7.
39. Han Z, Chang L, Yamanishi Y, Karin M, Firestein GS. Joint damage and inflammation in c-Jun N-terminal kinase 2 knockout mice with passive murine collagen-induced arthritis. Arthritis Rheum 2002; 46: 818-23.
40. Konttinen YT, Salo T, Hanemaaijer R, et al. Collagenase-3 (MMP-13) and its activators in rheumatoid arthritis: localization in the pannus-hard tissue junction and inhibition by alendronate. Matrix Biol 1999; 18: 401-12.
41. Haas CS, Amin MA, Ruth JH, et al. In vivo inhibition of angiogenesis by interleukin-13 gene therapy in a rat model of rheumatoid arthritis. Arthritis Rheum 2007; 56: 2535-48.
42. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003; 374: 1-20.
43. Wong PK, Campbell IK, Egan PJ, Ernst M, Wicks IP. The role of the interleukin-6 family of cytokines in inflammatory arthritis and bone turnover. Arthritis Rheum 2003; 48: 1177-89.
44. Wallace PM, MacMaster JF, Rouleau KA, et al. Regulation of inflammatory responses by oncostatin M. J Immunol 1999; 162: 5547-55.
45. Wahl AF, Wallace PM. Oncostatin M in the anti-inflammatory response. Ann Rheum Dis 2001; 60(Suppl 3): iii75-iii80.
46. Richards CD. Matrix catabolism in arthritis: priming the guns with oncostatin M. J Rheumatol 2004; 31: 2326-8.
47. Hui W, Bell M, Carroll G. Detection of oncostatin M in synovial fluid from patients with rheumatoid arthritis. Ann Rheum Dis 1997; 56: 184-7.
48. Langdon C, Leith J, Smith F, Richards CD. Oncostatin M stimulates monocyte chemoattractant protein-1-and interleukin-1-induced matrix metalloproteinase-1 production by human synovial fibroblasts in vitro. Arthritis Rheum 1997; 40: 2139-46.
49. Manicourt DH, Poilvache P, Van EA, Devogelaer JP, Lenz ME, Thonar EJ. Synovial fluid levels of tumor necrosis factor alpha and oncostatin M correlate with levels of markers of the degradation of crosslinked collagen and cartilage aggrecan in rheumatoid arthritis but not in osteoarthritis. Arthritis Rheum 2000; 43: 281-8.
50. Okamoto H, Yamamura M, Morita Y, Harada S, Makino H, Ota Z. The synovial expression and serum levels of interleukin-6, interleukin-11, leukemia inhibitory factor, and oncostatin M in rheumatoid arthritis. Arthritis Rheum 1997; 40: 1096-105.
51. Cawston TE, Curry VA, Summers CA, et al. The role of oncostatin M in animal and human connective tissue collagen turnover and its localization within the rheumatoid joint. Arthritis Rheum 1998; 41: 1760-71.
52. Van der Pouw Kraan TC, van Gaalen FA, Kasperkovitz PV, et al. Rheumatoid arthritis is a heterogeneous disease: evidence for differences in the activation of the STAT-1 pathway between rheumatoid tissues. Arthritis Rheum 2003; 48: 2132-45.
53. Kasperkovitz PV, Verbeet NL, Smeets TJ, et al. Activation of the STAT1 pathway in rheumatoid arthritis. Ann Rheum Dis 2004; 63: 233-9.
54. Yokota A, Narazaki M, Shima Y, et al. Preferential and persistent activation of the STAT1 pathway in rheumatoid synovial fluid cells. J Rheumatol 2001; 28: 1952-9.
55. De Hooge ASK, van de Loo FAJ, Bennink MB, et al. Adenoviral transfer of murine oncostatin M elicits periosteal bone apposition in knee joints of mice, despite synovial inflammation and upregulated expression of interleukin-6 and receptor activator of nuclear factor-κB ligand. Am J Pathol 2002; 160: 1733-43.
56. Rowan AD, Hui W, Cawston TE, Richards CD. Adenoviral gene transfer of interleukin-1 in combination with oncostatin M induces significant joint damage in a murine model. Am J Pathol 2003; 162: 1975-84.
57. Langdon C, Kerr C, Hassen M, Hara T, Arsenault AL, Richards CD. Murine oncostatin M stimulates mouse synovial fibroblasts in vitro and induces inflammation and destruction in mouse joints in vivo. Am J Pathol 2000; 157: 1187-96.
58. Porter S, Clark IM, Kevorkian L, Edwards DR. The ADAMTS metalloproteinases. Biochem J 2005; 386: 15-27.
59. Plater-Zyberk C, Buckton J, Thompson S, et al. Amelioration of arthritis in two murine models using antibodies to oncostatin M. Arthritis Rheum 2001; 44: 2697-702.
60. Hui W, Rowan AD, Cawston T. Transforming growth factor-β1 blocks the release of collagen fragments from boving nasal cartilage stimulated by oncostatin M in combination with IL-1α. Cytokine 2000; 12: 765-9.
61. Cleaver CS, Rowan AD, Cawston TE. Interleukin 13 blocks the release of collagen from bovine nasal cartilage treated with proinflammatory cytokines. Ann Rheum Dis 2001; 60: 150-7.
62. Elliott S, Rowan AD, Carrere S, Koshy P, Catterall JB, Cawston TE. Esculetin inhibits cartilage resorption induced by interleukin 1alpha in combination with oncostatin M. Ann Rheum Dis 2001; 60: 158-65.
63. Hui W, Rowan AD, Cawston T. Insulin-like growth factor 1 blocks collagen release and down regulates matrix metalloproteinase-1,-3,-8, and-13 mRNA expression in bovine nasal cartilage stimulated with oncostatin M in combination with interleukin 1α. Ann Rheum Dis 2001; 60: 254-61.
64. Koshy PJ, Henderson N, Logan C, Life PF, Cawston TE, Rowan AD. Interleukin 17 induces cartilage collagen breakdown: novel synergistic effects in combination with proinflammatory cytokines. Ann Rheum Dis 2002; 61: 704-13.
65. Li WQ, Zafarullah M. Oncostatin M up-regulates tissue inhibitor of metalloproteinases-3 gene expression in articular chondrocytes via de novo transcription, protein synthesis, and tyrosine kinase-and mitogen-activated protein kinase-dependent mechanisms. J Immunol 1998; 161: 5000-7.
66. Li WQ, Dehnade F, Zafarullah M. Oncostatin M-induced matrix metalloproteinase and tissue inhibitor of metalloproteinase-3 genes expression in chondrocytes requires Janus kinase/STAT signaling pathway. J Immunol 2001; 166: 3491-8.
67. El Mabrouk M, Sylvester J, Zafarullah M. Signaling pathways implicated in oncostatin M-induced aggrecanase-1 and matrix metalloproteinase-13 expression in human articular chondrocytes. Biochim Biophys Acta 2007; 1773: 309-20.
68. Rottapel R. Putting the brakes on arthritis: can suppressors of cytokine signaling (SOCS) suppress rheumatoid arthritis? J Clin Invest 2001; 108: 1745-7.
69. Ivashkiv LB, Tassiulas I. Can SOCS make arthritis better? J Clin Invest 2003; 111: 795-7.
70. Wormald S, Hilton DJ. Inhibitors of cytokine signal transduction. J Biol Chem 2004; 279: 821-4.
71. Egan PJ, Lawlor KE, Alexander WS, Wicks IP. Suppressor of cytokine signaling-1 regulates acute inflammatory arthritis and T cell activation. J Clin Invest 2003; 111: 915-24.
72. Ernst M, Inglese M, Waring P, et al. Defective gp130-mediated signal transducer and activator of transcription (STAT) signaling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. J Exp Med 2001; 194: 189-203.
73. Shouda T, Yoshida T, Hanada T, et al. Induction of the cytokine signal regulator SOCS3/CIS3 as a therapeutic strategy for treating inflammatory arthritis. J Clin Invest 2001; 108: 1781-8.
74. Yan C, Boyd DD. Regulation of matrix metalloproteinase gene expression. J Cell Physiol 2007; 211: 19-26.
75. Andriamanalijaona R, Kypriotou M, Bauge C, et al. Comparative effects of 2 antioxidants, selenomethionine and epigallocatechingallate, on catabolic and anabolic gene expression of articular chondrocytes. J Rheumatol 2005; 32: 1958-67.
76. DiBattista JA, Martel-Pelletier J, Wosu LO, Sandor T, Antakly T, Pelletier JP. Glucocorticoid receptor mediated inhibition of interleukin-1 stimulated neutral metalloprotease synthesis in normal human chondrocytes. J Clin Endocrinol Metab 1991; 72: 316-26.
77. Forsyth CB, Cole A, Murphy G, Bienias JL, Im HJ, Loeser RF Jr. Increased matrix metalloproteinase-13 production with aging by human articular chondrocytes in response to catabolic stimuli. J Gerontol A Biol Sci Med Sci 2005; 60: 1118-24.
78. Im HJ, Pacione C, Chubinskaya S, Van Wijnen AJ, Sun Y, Loeser RF. Inhibitory effects of insulin-like growth factor-1 and osteogenic protein-1 on fibronectin fragment-and interleukin-1beta-stimulated matrix metalloproteinase-13 expression in human chondrocytes. J Biol Chem 2003; 278: 25386-94.
79. Sun HB, Malacinski GM, Yokota H. Promoter competition assay for analyzing gene regulation in joint tissue engineering. Front Biosci 2002; 7: a169-a174.
80. Tomita T, Takano H, Tomita N, et al. Transcription factor decoy for NFκB inhibits cytokine and adhesion molecule expressions in synovial cells derived from rheumatoid arthritis. Rheumatology (Oxford) 2000; 39: 749-57.
81. Wen D, Nong Y, Morgan JG, et al. A selective small molecule IκB Kinase β inhibitor blocks nuclear factor κB-mediated inflammatory responses in human fibroblast-like synoviocytes, chondrocytes, and mast cells. J Pharmacol Exp Ther 2006; 317: 989-1001.
82. Wakamatsu K, Nanki T, Miyasaka N, Umezawa K, Kubota T. Effect of a small molecule inhibitor of nuclear factor-κB nuclear translocation in a murine model of arthritis and cultured human synovial cells. Arthritis Res Ther 2005; 7: R1348-59.
83. Bondeson J, Lauder S, Wainwright S, et al. Adenoviral gene transfer of the endogenous inhibitor IαBβ into human osteoarthritis synovial fibroblasts demonstrates that several matrix metalloproteinases and aggrecanases are nuclear factor-κB-dependent. J Rheumatol 2007; 34: 523-33.
84. LaVallie ER, Chockalingam PS, Collins-Racie LA, et al. Protein kinase Cζ is up-regulated in osteoarthritic cartilage and is required for activation of NF-κB by tumor necrosis factor and interleukin-1 in articular chondrocytes. J Biol Chem 2006; 281(34): 24124-37.
85. Roman-Blas JA, Jimenez SA. NF-κB as a potential therapeutic target in osteoarthritis and rheumatoid arthritis. Osteoarthritis Cartilage 2006; 14: 839-48.
86. Redlich K, Kiener HP, Schett G, et al. Overexpression of transcription factor Ets-1 in rheumatoid arthritis synovial membrane: regulation of expression and activation by interleukin-1 and tumor necrosis factor α. Arthritis Rheum 2001; 44: 266-74.
87. White LA, Maute C, Brinckerhoff CE. ETS sites in the promoters of the matrix metalloproteinases collagenase (MMP-1) and stromelysin (MMP-3) are auxiliary elements that regulate basal and phorbol-induced transcription. Connect Tissue Res 1997; 36: 321-35.
88. Baillat D, Leprivier G, Regnier D, et al. Stromelysin-1 expression is activated in vivo by Ets-1 through palindromic head-to-head Ets binding sites present in the promoter. Oncogene 2006; 25: 5764-76.
89. Forough R, Weylie B, Collins C, et al. Transcription factor Ets-1 regulates fibroblast growth factor-1-mediated angiogenesis in vivo: role of Ets-1 in the regulation of the PI3K/AKT/MMP-1 pathway. J Vasc Res 2006; 43: 327-37.
90. Hahne JC, Fuchs T, El MH, Okuducu AF, Bories JC, Wernert N. Expression pattern of matrix metalloproteinase and TIMP genes in fibroblasts derived from Ets-1 knock-out mice compared to wild-type mouse fibroblasts. Int J Mol Med 2006; 18: 153-9.
91. Mix KS, Attur MG, Al-Mussawir H, Abramson SB, Brinckerhoff CE, Murphy EP. Transcriptional repression of matrix metalloproteinase gene expression by the orphan nuclear receptor NURR1 in cartilage. J Biol Chem 2007; 282: 9492-504.
92. Takeba Y, Suzuki N, Wakisaka S, et al. Involvement of cAMP responsive element binding protein (CREB) in the synovial cell hyperfunction in patients with rheumatoid arthritis. Clin Exp Rheumatol 2000; 18: 47-55.
93. Liacini A, Sylvester J, Li WQ, Zafarullah M. Inhibition of interleukin-1-stimulated MAP kinases, activating protein-1 (AP-1) and nuclear factor kappa B (NF-κB) transcription factors down-regulates matrix metalloproteinase gene expression in articular chondrocytes. Matrix Biol 2002; 21: 251-62.
94. Liacini A, Sylvester J, Li WQ, et al. Induction of matrix metalloproteinase-13 gene expression by TNF-α is mediated by MAP kinases, AP-1, and NF-κB transcription factors in articular chondrocytes. Exp Cell Res 2003; 288: 208-17.
95. Sylvester J, Liacini A, Li WQ, Zafarullah M. Interleukin-17 signal transduction pathways implicated in inducing matrix metalloproteinase-3,-13 and aggrecanase-1 genes in articular chondrocytes. Cell Signal 2004; 16: 469-76.
96. Tardif G, Pelletier JP, Dupuis M, Geng C, Cloutier JM, Martel-Pelletier J. Collagenase 3 production by human osteoarthritic chondrocytes in response to growth factors and cytokines is a function of the physiologic state of the cells. Arthritis Rheum 1999; 42: 1147-58.
97. Moulharat N, Lesur C, Thomas M, et al. Effects of transforming growth factor-beta on aggrecanase production and proteoglycan degradation by human chondrocytes in vitro. Osteoarthritis Cartilage 2004; 12: 296-305.
98. Vankemmelbeke MN, Holen I, Wilson AG, et al. Expression and activity of ADAMTS-5 in synovium. Eur J Biochem 2001; 268: 1259-68.
99. Yamanishi Y, Boyle DL, Clark M, et al. Expression and regulation of aggrecanase in arthritis: the role of TGF-α. J Immunol 2002; 168: 1405-12.
100. Mi Z, Ghivizzani SC, Lechman E, Glorioso JC, Evans CH, Robbins PD. Adverse effects of adenovirus-mediated gene transfer of human transforming growth factor beta 1 into rabbit knees. Arthritis Res Ther 2003; 5: R132-R139.
101. Glansbeek HL, van Beuningen HM, Vitters EL, van der Kraan PM, van den Berg WB. Stimulation of articular cartilage repair in established arthritis by local administration of transforming growth factor-beta into murine knee joints. Lab Invest 1998; 78: 133-42.
102. Scharstuhl A, Glansbeek HL, van Beuningen HM, Vitters EL, van der Kraan PM, van den Berg WB. Inhibition of endogenous TGF-α during experimental osteoarthritis prevents osteophyte formation and impairs cartilage repair. J Immunol 2002; 169: 507-14.
103. Brandes ME, Allen JB, Ogawa Y, Wahl SM. Transforming growth factor beta 1 suppresses acute and chronic arthritis in experimental animals. J Clin Invest 1991; 87: 1108-13.
104. Chernajovsky Y, Adams G, Triantaphyllopoulos K, Ledda MF, Podhajcer OL. Pathogenic lymphoid cells engineered to express TGF β1 ameliorate disease in a collagen-induced arthritis model. Gene Ther 1997; 4: 553-9.
105. Close DR. Matrix metalloproteinase inhibitors in rheumatic diseases. Ann Rheum Dis 2001; 60(Suppl 3): iii620-67.
106. Skiles JW, Gonnella NC, Jeng AY. The design, structure, and clinical update of small molecular weight matrix metalloproteinase inhibitors. Curr Med Chem 2004; 11: 2911-77.
107. Kontogiorgis CA, Papaioannou P, Hadjipavlou-Litina DJ. Matrix metalloproteinase inhibitors: a review on pharmacophore mapping and (Q)SARs results. Curr Med Chem 2005; 12: 339-55.
108. Levin JI. The design and synthesis of aryl hydroxamic acid inhibitors of MMPs and TACE. Curr Top Med Chem 2004; 4: 1289-310.
109. Rao BG. Recent developments in the design of specific Matrix Metalloproteinase inhibitors aided by structural and computational studies. Curr Pharm Des 2005; 11: 295-322.
110. Van Marle S, van Vliet A, Sollie F, Kambayashi Y, Yamada-Sawada T. Safety, tolerability and pharmacokinetics of oral S-3304, a novel matrix metalloproteinase inhibitor, in single and multiple dose escalation studies in healthy volunteers. Int J Clin Pharmacol Ther 2005; 43: 282-93.
111. Ishikawa T, Nishigaki F, Miyata S, et al. Prevention of progressive joint destruction in adjuvant induced arthritis in rats by a novel matrix metalloproteinase inhibitor, FR217840. Eur J Pharmacol 2005; 508: 239-47.
112. Yao W, Wasserman ZR, Chao M, et al. Design and synthesis of a series of (2R)-N(4)-hydroxy-2-(3-hydroxybenzyl)-N(1)-[(1S,2R)-2-hydroxy-2,3-dihydro-1H-inden-1-yl]butanediamide derivatives as potent, selective, and orally bioavailable aggrecanase inhibitors. J Med Chem 2001; 44: 3347-50.
113. Yao W, Chao M, Wasserman ZR, et al. Potent P1’ biphenylmethyl substituted aggrecanase inhibitors. Bioorg Med Chem Lett 2002; 12: 101-4.
114. Xiang JS, Hu Y, Rush TS, et al. Synthesis and biological evaluation of biphenylsulfonamide carboxylate aggrecanase-1 inhibitors. Bioorg Med Chem Lett 2006; 16: 311-6.
115. Cherney RJ, Mo R, Meyer DT, et al. Potent and selective aggrecanase inhibitors containing cyclic P1 substituents. Bioorg Med Chem Lett 2003; 13: 1297-300.
116. Simard N, Boire G, de Brum-Fernandes AJ, St-Pierre Y. A novel approach to measure the contribution of matrix metalloproteinase in the overall net proteolytic activity present in synovial fluids of patients with arthritis. Arthritis Res Ther 2006; 8: R125.
117. Bursavich MG, Gilbert AM, Lombardi S, et al. Synthesis and evaluation of aryl thioxothiazolidinone inhibitors of ADAMTS-5 (Aggrecanase-2). Bioorg Med Chem Lett 2007; 17: 1185-8.
118. Mosyak L, Georgiadis K, Shane T, et al. Crystal structures of the two major aggrecan degrading enzymes, ADAMTS4 and ADAMTS5. Protein Sci 2008; 17: 16-21.
119. Shieh HS, Mathis KJ, Williams JM, et al. High resolution crystal structure of the catalytic domain of ADAMTS-5 (aggrecanase-2). J Biol Chem 2008; 283: 1501-7.
120. Zhang Y, Xu J, Levin J, et al. Identification and characterization of 4-[[4-(2-butynyloxy)phenyl]sulfonyl]-N-hydroxy-2,2-dimethyl-(3S)thiomorpholinecar boxamide (TMI-1), a novel dual tumor necrosis factor-alpha-converting enzyme/matrix metalloprotease inhibitor for the treatment of rheumatoid arthritis. J Pharmacol Exp Ther 2004; 309: 348-55.
121. Thabet MM, Huizinga TW. Drug evaluation: apratastat, a novel TACE/MMP inhibitor for rheumatoid arthritis. Curr Opin Investig Drugs 2006; 7: 1014-9.
122. Engel CK, Pirard B, Schimanski S, et al. Structural basis for the highly selective inhibition of MMP-13. Chem Biol 2005; 12: 181-9.
123. Johnson AR, Pavlovsky AG, Ortwine DF, et al. Discovery and characterization of a novel inhibitor of matrix metalloprotease-13 that reduces cartilage damage in vivo without joint fibroplasia side effects. J Biol Chem 2007; 282: 27781-91.
124. Rutkauskaite E, Zacharias W, Schedel J, et al. Ribozymes that inhibit the production of matrix metalloproteinase 1 reduce the invasiveness of rheumatoid arthritis synovial fibroblasts. Arthritis Rheum 2004; 50: 1448-56.
125. Rutkauskaite E, Volkmer D, Shigeyama Y, et al. Retroviral gene transfer of an antisense construct against membrane type 1 matrix metalloproteinase reduces the invasiveness of rheumatoid arthritis synovial fibroblasts. Arthritis Rheum 2005; 52: 2010-4.
126. Song RH, Tortorella MD, Malfait AM, et al. Aggrecan degradation in human articular cartilage explants is mediated by both ADAMTS-4 and ADAMTS-5. Arthritis Rheum 2007; 56: 575-85.
127. Beehler BC, Brinckerhoff CE, Ostrowski J. Selective retinoic acid receptor ligands for rheumatoid arthritis. Curr Opin Investig Drugs 2004; 5: 1153-7.
128. Malemud CJ. Matrix metalloproteinases: role in skeletal development and growth plate disorders. Front Biosci 2006; 11: 1702-15.
129. Milner JM, Cawston TE. Matrix metalloproteinase knockout studies and the potential use of matrix metalloproteinase inhibitors in the rheumatic diseases. Curr Drug Targets Inflamm Allergy 2005; 4: 363-75.
130. Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 2002; 115: 3719-27.
131. Mohammed FF, Smookler DS, Khokha R. Metalloproteinases, inflammation, and rheumatoid arthritis. Ann Rheum Dis 2003; 62(Suppl 2): ii43-ii7.
132. Brew K, Dinakarpandian D, Nagase H. Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 2000; 1477: 267-83.
133. Murphy G, Lee MH. What are the roles of metalloproteinases in cartilage and bone damage? Ann Rheum Dis 2005; 64(Suppl 4): ii44-ii47.
134. Apparailly F, Noel D, Millet V, et al. Paradoxical effects of tissue inhibitor of metalloproteinases 1 gene transfer in collageninduced arthritis. Arthritis Rheum 2001; 44: 1444-54.
135. Schett G, Hayer S, Tohidast-Akrad M, et al. Adenovirus-based overexpression of tissue inhibitor of metalloproteinases 1 reduces tissue damage in the joints of tumor necrosis factor α transgenic mice. Arthritis Rheum 2001; 44: 2888-98.
136. Arner EC. Aggrecanase-mediated cartilage degradation. Curr Opin Pharmacol 2002; 2: 322-9.
137. Günther M, Haubeck HD, van de Leur LE, et al. Transforming growth factor beta 1 regulates tissue inhibitor of metalloproteinases-1 expression in differentiated human articular chondrocytes. Arthritis Rheum 1994; 37: 395-405.
138. Su S, Dehnade F, Zafarullah M. Regulation of tissue inhibitor of metalloproteinases-3 gene expression by transforming growth factor-beta and dexamethasone in bovine and human articular chondrocytes. DNA Cell Biol 1996; 15: 1039-48.
139. Yu WH, Yu S, Meng Q, Brew K, Woessner JF Jr. TIMP-3 binds to sulfated glycosaminoglycans of the extracellular matrix. J Biol Chem 2000; 275: 31226-32.
140. Lee MH, Atkinson S, Murphy G. Identification of the extracellular matrix (ECM) binding motifs of tissue inhibitor of metalloproteinases (TIMP)-3 and effective transfer to TIMP-1. J Biol Chem 2007; 282: 6887-98.
141. Hashimoto G, Aoki T, Nakamura H, Tanzawa K, Okada Y. Inhibition of ADAMTS4 (aggrecanase-1) by tissue inhibitors of metalloproteinases (TIMP-1, 2, 3 and 4). FEBS Lett 2001; 494: 192-5.
142. Kashiwagi M, Tortorella M, Nagase H, Brew K. TIMP-3 is a potent inhibitor of aggrecanase 1 (ADAM-TS4) and aggrecanase 2 (ADAMTS5). J Biol Chem 2001; 276: 12501-4.
143. Gendron C, Kashiwagi M, Hughes C, Caterson B, Nagase H. TIMP-3 inhibits aggrecanase-mediated glycosaminoglycan release from cartilage explants stimulated by catabolic factors. FEBS Lett 2003; 555: 431-6.
144. Knauper V, Lopez-Otin C, Smith B, Knight G, Murphy G. Biochemical characterization of human collagenase-3. J Biol Chem 1996; 271: 1544-50.
145. Amour A, Slocombe PM, Webster A, et al. TNF-α converting enzyme (TACE) is inhibited by TIMP-3. FEBS Lett 1998; 435: 39-44.
146. Lee MH, Knauper V, Becherer JD, Murphy G. Full-length and NTIMP-3 display equal inhibitory activities toward TNF-α convertase. Biochem Biophys Res Commun 2001; 280: 945-50.
147. Wei S, Kashiwagi M, Kota S, Xie Z, Nagase H, Brew K. Reactive site mutations in tissue inhibitor of metalloproteinase-3 disrupt inhibition of matrix metalloproteinases but not tumor necrosis factor-α-converting enzyme. J Biol Chem 2005; 280: 32877-82.
148. Mahmoodi M, Sahebjam S, Smookler D, Khokha R, Mort JS. Lack of tissue inhibitor of metalloproteinases-3 results in an enhanced inflammatory response in antigen-induced arthritis. Am J Pathol 2005; 166: 1733-40.
149. Sahebjam S, Khokha R, Mort JS. Increased collagen and aggrecan degradation with age in the joints of Timp3 (-/-) mice. Arthritis Rheum 2007; 56: 905-9.
150. Drynda A, Quax PH, Neumann M, et al. Gene transfer of tissue inhibitor of metalloproteinases-3 reverses the inhibitory effects of TNF-α on Fas-induced apoptosis in rheumatoid arthritis synovial fibroblasts. J Immunol 2005; 174: 6524-31.
151. Anand-Apte B, Pepper MS, Voest E, et al. Inhibition of angiogenesis by tissue inhibitor of metalloproteinase-3. Invest Ophthalmol Vis Sci 1997; 38: 817-23.
152. Qi JH, Ebrahem Q, Moore N, et al. A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med 2003; 9: 407-15.
153. Nagase H, Brew K. Engineering of tissue inhibitor of metalloproteinases mutants as potential therapeutics. Arthritis Res 2002; 4(Suppl 3): S51-S61.
154. Lee MH, Verma V, Maskos K, et al. Engineering N-terminal domain of tissue inhibitor of metalloproteinase (TIMP)-3 to be a better inhibitor against tumour necrosis factor-α-converting enzyme. Biochem J 2002; 364: 227-34.
155. Van der Laan WH, Quax PH, Seemayer CA, et al. Cartilage degradation and invasion by rheumatoid synovial fibroblasts is inhibited by gene transfer of TIMP-1 and TIMP-3. Gene Ther 2003; 10: 234-42.
156. Bokarewa M, Dahlberg L, Tarkowski A. Expression and functional properties of antibodies to tissue inhibitors of metalloproteinases (TIMPs) in rheumatoid arthritis. Arthritis Res Ther 2005; 7: R1014-22.
157. Su S, Grover J, Roughley PJ, et al. Expression of the tissue inhibitor of metalloproteinases (TIMP) gene family in normal and osteoarthritic joints. Rheumatol Int 1999; 18: 183-91.
158. Takizawa M, Ohuchi E, Yamanaka H, et al. Production of tissue inhibitor of metalloproteinases 3 is selectively enhanced by calcium pentosan polysulfate in human rheumatoid synovial fibroblasts. Arthritis Rheum 2000; 43: 812-20.
159. Liu YE, Wang M, Greene J, et al. Preparation and characterization of recombinant tissue inhibitor of metalloproteinase 4 (TIMP-4). J Biol Chem 1997; 272: 20479-83.
160. Stratmann B, Farr M, Tschesche H. Characterization of C-terminally truncated human tissue inhibitor of metalloproteinases-4 expressed in Pichia pastoris. Biol Chem 2001; 382: 987-91.
161. Huang W, Li WQ, Dehnade F, Zafarullah M. Tissue inhibitor of metalloproteinases-4 (TIMP-4) gene expression is increased in human osteoarthritic femoral head cartilage. J Cell Biochem 2002; 85: 295-303.
162. Celiker MY, Ramamurthy N, Xu JW, et al. Inhibition of adjuvant-induced arthritis by systemic tissue inhibitor of metalloproteinases 4 gene delivery. Arthritis Rheum 2002; 46: 3361-8.
163. Ramamurthy NS, Greenwald RA, Celiker MY, Shi EY. Experimental arthritis in rats induces biomarkers of periodontitis which are ameliorated by gene therapy with tissue inhibitor of matrix metalloproteinases. J Periodontol 2005; 76: 229-33.
164. Sekut L, Connolly K. AntiTNF-alpha agents in the treatment of inflammation. Expert Opin Investig Drugs 1998; 7: 1825-39.
165. Hu J, Van den Steen PE, Sang QX, Opdenakker G. Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases. Nat Rev Drug Discov 2007; 6: 480-98.