Paradoxical effects of a synthetic metalloproteinase inhibitor that blocks both P55 and P75 TNF receptor shedding and TNFα processing in RA synovial membrane cell cultures

Journal of Clinical Investigation

Volumn 97, Issue 12, 1996, Pages 2833-2841

  Williams, Lynn M ^a   Gibbons, Deena L ^a,c   Gearing, Andrew ^b   Maini, Ravinder N ^a   Feldmann, Marc ^a   Brennan, Fionula M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Neures Ltd   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

matrix metalloproteinase; rheumatoid arthritis; TNF receptor; tumor necrosis factor

Indexed keywords

BB 2275; HYDROXAMIC ACID; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; METALLOPROTEINASE INHIBITOR; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; PHORBOL 13 ACETATE 12 MYRISTATE; PHYTOHEMAGGLUTININ; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ANTIBODY; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL DEATH; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; GENE EXPRESSION; HELA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MONOCYTE; PRIORITY JOURNAL; PROTEIN PROCESSING; RHABDOMYOSARCOMA; RHEUMATOID ARTHRITIS; SYNOVIOCYTE; T LYMPHOCYTE;

EID: 0029891449     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118739     Document Type: Article

References (48)

1. Brennan, F.M., R.N. Maini, and M. Feldmann. 1992. TNFα - a pivotal role in rheumatoid arthritis? Br J. Rheumatol. 31:293-298.
2. Brennan, F.M., D. Chantry, A. Jackson, R. Maini, and M. Feldmann. 1989. Inhibitory effect of TNFα antibodies on synovial cell interleukin-1 production in rheumatoid arthritis. Lancet. 2:244-247.
3. Haworth, C., F.M. Brennan, D. Chantry, M. Turner, R.N. Maini, and M. Feldmann. 1991. Expression of granulocyte-macrophage colony-stimulating factor in rheumatoid arthritis: regulation by tumor necrosis factor-α. Eur. J. Immunol. 21:2575-2579.
4. Butler, D., R.N. Maini, M. Feldmann, and F.M. Brennan. 1995. Blockade of TNFα with chimeric and TNFα monoclonal antibody, cA2 reduces (IL-6 and IL-8) release in RA NMC cultures: A comparison with IL-1ra. Eur. Cytokine Netw. 6:225-230.
5. Gray, P.W., K. Barrett, D. Chantry, M. Turner, and M. Feldmann. 1990. Cloning of human tumor necrosis factor (TNF) receptor cDNA and expression of recombinanl soluble TNF-binding protein. Proc. Natl. Acad. Sci. USA. 87: 7380-7384.
6. Smith, C.A., T. Davis, D. Anderson, L. Solam, M.P. Beckmann, R. Jerzy, S.K. Dower, D. Cosman, and R.G. Goodwin. 1990. A receptor for tumor necrosis factor defines an unusual family of cellular and viral proteins. Science (Wash. DC). 248:1019-1023.
7. Brennan, F.M., D.L. Gibbons, T. Mitchell, A.P. Cope, R.N. Maini, and M. Feldmann. 1992. Enhanced expression of tumor necrosis factor receptor mRNA and protein in mononuclear cells isolated from rheumatoid arthritis synovial joints. Eur. J. Immunol. 22:1907-1912.
8. Chu, C.Q., M. Field, M. Feldmann, and R.N. Maini. 1991. Localization of tumor necrosis factor α in synovial tissues and at the cartilage-pannus junction in patients with rheumatoid arthritis. Arthritis Rheum. 34:1125-1132.
9. Deleuran, B.W., C.Q. Chu, M. Field, F.M. Brennan, T. Mitchell, M. Feldmann, and R.N. Maini. 1992. Localization of tumor necrosis factor receptors in the synovial tissue and cartilage-pannus junction in patients with rheumatoid arthritis. Implications for local actions of tumor necrosis factor α. Arthritis Rheum. 35:1170-1178.
10. Katsikis, P., C.Q. Chu, F.M. Brennan, R.N. Maini, and M. Feldmann. 1994. Immunoregulatory role of interleukin 10 (IL-10) in Rheumatoid Arthritis. J. Exp. Med. 179:1517-1527.
11. Cope, A.P., D. Aderka, M. Doherty, H. Engelmann, D. Gibbons, A.C. Jones, F. M. Brennan, R.N. Maini, D. Wallach, and M. Feldmann. 1992. Increased levels of soluble tumor necrosis factor receptors in the sera and synovial fluid of patients with rheumatic diseases. Arthritis Rheum. 35:1150-1169.
12. Brennan, F.M., D. Gibbons, A. Cope, P. Katsikis, R.N. Maini, and M. Feldmann. 1995. TNF inhibitors are produced spontaneously by rheumatoid and osteoarthritic synovial joint cell cultures: evidence of feedback control of TNF action. Scand. J. Immunol. 42:158-165.
13. Seckinger, P., S. Isaaz, and J.M. Dayer. 1989. Purification and biologic characterization of a specific tumor necrosis factor alpha inhibitor. J. Biol. Chem. 264:11966-11973.
14. Engelmann, H., D. Aderka, M. Rubinstein, D. Rotman, and D. Wallach. 1989. A tumor necrosis factor-binding protein purified to homogeneity from human urine protects cells from tumor necrosis factor toxicity. J. Biol. Chem. 264:11974-11980.
15. Gullberg, U., M. Lantz, L. Lindvall, I. Olsson, and A. Himmler. 1992. Involvement of an Asn/Val cleavage site in the production of a soluble form of a human tumor necrosis factor (TNF) receptor. Site-directed mutagenesis of a putative cleavage site in the p55 TNF receptor chain. Eur. J. Cell Biol. 58:307-312.
16. Porteu, F., M. Brockhaus, D. Wallach, H. Engelmann, and C.F. Nathan. 1991. Human neutrophil elastase releases a ligand-binding fragment from the 75-kDa tumor necrosis factor (TNF) receptor. Comparison with the proteolytic activity responsible for shedding of TNF receptors from stimulated neutrophils. J. Biol. Chem. 266:18846-18853.
17. Brinckerhoff, C.E. 1991. Joint destruction in arthritis: metalloproteinases in the spotlight. Arthritis Rheum. 34:1073-1975.
18. Gearing, A.J.H., P. Beckett, M. Christodoulou, M. Churchill, J. Clements, A.H. Davidson, A.H. Drummond, W.A. Galloway, R. Gilbert, J.L. Gordon et al. 1994. Processing of tumour necrosis factor-α precursor by metalloproteinases. Nature (Lond.). 370:555-557.
19. Cope, A.P., D.L. Gibbons, D. Aderka, B.M. Foxwell, D. Wallach, R.N. Maini, M. Feldmann, and F.M. Brennan. 1993. Differential regulation of tumour necrosis factor receptors (TNF-R) by IL-4; upregulalion of P55 and P75 TNF-R on synovial joint mononuclear cells. Cytokine. 5:205-212.
20. Leeuwenberg, J.F.M., G.M.M.A. Jeunhomme, and W.A. Buurman. 1994. Slow release of soluble TNF receptors by monocytes in vitro. J. Immunol. 154:4036-4043.
21. Engelberts, I., A. Moller, G.J.M. Schoen, C.J. van der Linden, and W.A. Buurman. 1991. Evaluation of human TNF in plasma by ELISA. Lymphokine Cytokine Res. 10:60-76.
22. Meager, A. 1991. A cytotoxic assay for tumor necrosis factor using a human rhabdomyosarcoma cell line. J. Immunol. Methods. 144:141-143.
23. Knight, C.G., F. Willenbrock, and G. Murphy. 1992. A novel coumarin-labelled peptide for sensitive continuous assays of the matrix metalloproteinases. FEBS Lett. 296(3):263-266.
24. McGeehan, G.M., J.D. Becherer, J. Bast R.C., C.M. Boyer, B. Champion, K. M. Connolly, J.G. Conway, P. Furdon, S. Karp, S. Kidao et al. 1994. Regulation of tumour necrosis factor-α processing by a metalloproteinase inhibitor. Nature (Lond.). 370:558-561.
25. Mohler, K., P.R. Sleath, J.N. Fitzner, D.P. Cerretti, M. Alderson, S.S. Kerwar, D.S. Torrance, C. Otten-Evans, T. Greenstreet, K. Weerawarna et al. 1994. Protection against a lethal dose of endotoxin by an inhibitor of tumour necrosis factor processing. Nature (Lond.). 370:218-220.
26. Imamura, K., D. Spriggs, and D. Kufe. 1987. Expression of tumour necrosis factor receptors on human monocytes and internalization of receptor bound ligand. J. Immunol. 139:2989-2992.
27. Lantz, M., S. Malik, M.L. Slevin, and I. Olsson. 1990. Infusion of tumor necrosis factor (TNF) causes an increase in circulating TNF-binding protein in humans. Cytokine. 2:402-406.
28. Kruys, V., K. Kemmer, A. Shakov, V. Jongeneel, and B. Beutler. 1992. Constitutive activity of the tumor necrosis factor promoter is canceled by the 3′ untranslated region in nonmacrophage cell lines; a trans-dominant factor overcomes this suppressive effect. Proc. Natl. Acad. Sci. USA. 89:673-677.
29. Joyce, D.A., D. Gibbons, P. Green, M. Feldmann, and F.M. Brennan. 1994. Two inhibitors of pro-inflammatory cytokine release, IL-10 and IL-4, have contrasting effects on release of soluble p75 TNF receptor by cultured monocytes. Eur. J. Immunol. 24:2699-2705.
30. Butler, D., B. Scallon, A. Meager, M. Kissonerghis, A. Corcoran, Y. Chernajovsky, M. Feldmann, J. Ghrayeb, and F. Brennan. 1994. TNF receptor fusion proteins are effective inhibitors of TNF-mediated cytotoxicity on human KYM-1D4 rhabdomyosarcoma cells. Cytokine. 6:616-623.
31. Chandler, S., R. Coates, A. Gearing, J. Lury, G. Wells, and E. Bone. 1995. Matrix metalloproteinases degrade myelin basic protein. Neurosci. Lett. 201:223-226.
32. Rubin, L.A., C.C. Kurman, M.E. Fritz, W.E. Biddison, B. Boutin, R. Yarchoan, and D.L. Nelson. 1985. Soluble interleukin 2 receptors are released from activated human lymphoid cells in vitro. J. Immunol. 135:3172-3177.
33. Novick, D., H. Engelmann, D. Wallach, and M. Rubinstein. 1989. Soluble cytokine receptors are present in normal human urine. J. Exp. Med. 170: 1409-1414.
34. Symons, J.A., J.A. Eastgate, and G.W. Duff. 1991. Purification and characterization of a novel soluble receptor for interleukin-1. J. Exp. Med. 174: 1251-1254.
35. Mosley, B., M.P. Beckmann, C.J. March, R.L. Idzerda, S.D. Gimpel, T. VandenBos, D. Friend, A. Alpert, D. Anderson, J. Jackson et al. 1989. The murine interleukin-4 receptor: molecular cloning and characterization of secreted and membrane bound forms. Cell. 59:335-348.
36. Goodwin, R.G., D. Friend, S.F. Ziegler, R. Jerzy, B.A. Falk, S. Gimpel, D. Cosman, S.K. Dower, C.J. March, A.E. Namen, and L.S. Park. 1990. Cloning of the human and murine interleukin-7 receptors: demonstration of a soluble form and homology to a new receptor superfamily. Cell. 60:941-951.
37. Downing, J.R., M.F. Roussel, and C.J. Sherr. 1989. Ligand and protein kinase C downmodulate the colony-stimulating factor 1 receptor by independent mechanisms. Mol. Cell. Biol. 9:2890-2896.
38. Novick, D., B. Cohen, and M. Rubinstein. 1994. The human interferon α/β receptor: characterization and molecular cloning. Cell. 77:391-400.
39. Porteu, F., and C. Nathan. 1990. Shedding of tumor necrosis factor receptors by activated human neutrophils. J. Exp. Med. 172:599-607.
40. Hwang, C., M. Gatanaga, G.A. Granger, and T. Gatanaga. 1993. Mechanism of release of soluble forems of tumor necrosis factor/lymphotoxin receptors by phorbol myristate acetate-stimulated human THP-1 cells in vitro. J. Immunol. 151:5631-5638.
41. de Waal-Malefyt, R., J. Abrams, B. Bennett, C.G. Figdor, and J.E. Vries de. 1991. Interleukin (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174:1209-1220.
42. Stetler-Stevensom, W., H.C. Krutzch, I.M.K. Wacher, M.K. Marguiles, and L. A. Liotta. 1989. The activation of the human type IV collagenase proenzyme. J. Biol. Chem. 164:1353-1356.
43. DiStefano, P.S., D.M. Chelsea, C.M. Schick, and J.F. McKelvy. 1993. Involvement of a metalloprotease in low-affinity nerve growth factor receptor truncation: inhibition of truncation in vitro and in vivo. J. Neurosci. 13:2405-2414.
44. Crowe, P.D., B.N. Walter, K.M. Mohler, C. Otten-Evans, R.A. Black, and C.F. Ware. 1994. A metalloprotease inhibitor blocks shedding of the 80 kD TNF receptor and TNF processing in T lymphocytes. J. Exp. Med 181:1205-1210.
45. Aderka, D., H. Engelmann, Y. Maar, C. Brakebusch, and D. Wallach. 1992. Stabilization of the bioactivity of tumour necrosis factor by its soluble receptors. J. Exp. Med. 175:323-329.
46. Elliott, M.J., R.N. Maini, M. Feldmann, A. Long-Fox, P. Charles, H. Bijl, and J.N. Woody. 1994. Repeated therapy with monoclonal antibody to tumour necrosis factor α (cA2) in patients with rheumatoid arthritis. Lancet. 344: 1125-1127.
47. DiMartino, M., W. High, W.A. Galloway, and M.J. Crimmin. 1994. Pre-clinical antiarthritic activity of MMP inhibitors. Ann. NY Acad. Sci. 732:411-413.
48. Conway, J.C., J.A. Wakefield, R.H. Brown, B.E. Marron, L. Sekut, A. Stimpson, A.B. McElroy, J.A. Menius, J.J. Jeffreys, R.L. Clark. G.M. McGeehan, and K.M. Connolly. 1995. Inhibition of cartilage and bone destruction in adjuvant arthritis in the rat by a matrix metalloproteinase inhibitor. J. Exp. Med. 182:449-458.