A 4-trifluoromethyl analogue of celecoxib inhibits arthritis by suppressing innate immune cell activation

Arthritis Research and Therapy

Volumn 14, Issue 1, 2012, Pages

  Chiba, Asako ^a   Mizuno, Miho ^a   Tomi, Chiharu ^a   Tajima, Ryohsuke ^a   Alloza, Iraide ^b   di Penta, Alessandra ^b   Yamamura, Takashi ^a   Vandenbroeck, Koen ^b,c   Miyake, Sachiko ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^c BASQUE FOUNDATION FOR SCIENCE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

4 TRIFLUOROMETHYL CELECOXIB DERIVATIVE; CELECOXIB; COLLAGEN ANTIBODY; COLLAGEN TYPE 2; CYCLOOXYGENASE 2; INTERLEUKIN 12; UNCLASSIFIED DRUG; ANTIRHEUMATIC AGENT; CYTOKINE; PYRAZOLE DERIVATIVE; SULFONAMIDE; THIOGLYCOLIC ACID DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; CELL ACTIVATION; CLINICAL ASSESSMENT; COLLAGEN INDUCED ARTHRITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE SEVERITY; DRUG EFFECT; DRUG INHIBITION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; INNATE IMMUNITY; MACROPHAGE; MALE; MAST CELL ACTIVATION; MOUSE; NONHUMAN; ANIMAL; C57BL MOUSE; CELL STRAIN U937; CHEMICALLY INDUCED DISORDER; CHEMISTRY; CYTOLOGY; DBA MOUSE; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; GENETICS; IMMUNE SYSTEM; IMMUNOLOGY; LEUKOCYTE; MACROPHAGE ACTIVATION; MAST CELL; METABOLISM; NEUTROPHIL; PERITONITIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANTIRHEUMATIC AGENTS; ARTHRITIS, EXPERIMENTAL; COLLAGEN TYPE II; CYTOKINES; ENDOPLASMIC RETICULUM STRESS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; HUMANS; IMMUNE SYSTEM; LEUKOCYTES; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MAST CELLS; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; NEUTROPHILS; PERITONITIS; PYRAZOLES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SULFONAMIDES; THIOGLYCOLATES; U937 CELLS;

EID: 84855799948     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3683     Document Type: Article

References (51)

1. Krieckaert CL, Bartelds GM, Lems WF, Wolbink GJ. The effect of immunomodulators on the immunogenicity of TNF-blocking therapeutic monoclonal antibodies: a review. Arthritis Res Ther 2010, 12:217. 10.1186/ar3147, 2991013, 21029481.
2. Feldmann M, Maini SR. Role of cytokines in rheumatoid arthritis: an education in pathophysiology and therapeutics. Immunol Rev 2008, 223:7-19. 10.1111/j.1600-065X.2008.00626.x, 18613827.
3. Buch MH. Sequential use of biologic therapy in rheumatoid arthritis. Curr Opin Rheumatol 2010, 22:321-329. 10.1097/BOR.0b013e328337bd01, 20190641.
4. Nishimoto N, Yoshizaki K, Miyasaka N, Yamamoto K, Kawai S, Takeuchi T, Hashimoto J, Azuma J, Kishimoto T. Treatment of rheumatoid arthritis with humanized anti-interleukin-6 receptor antibody: a multicenter, double-blind, placebo-controlled trial. Arthritis Rheum 2004, 50:1761-1769. 10.1002/art.20303, 15188351.
5. Maini RN, Taylor PC, Szechinski J, Pavelka K, Bröll J, Balint G, Emery P, Raemen F, Petersen J, Smolen J, Thomson D, Kishimoto T, . CHARISMA Study Group Double-blind randomized controlled clinical trial of the interleukin-6 receptor antagonist, tocilizumab, in European patients with rheumatoid arthritis who had an incomplete response to methotrexate. Arthritis Rheum 2006, 54:2817-2829. 10.1002/art.22033, 16947782, CHARISMA Study Group.
6. Genovese MC, McKay JD, Nasonov EL, Mysler EF, da Silva NA, Alecock E, Woodworth T, Gomez-Reino JJ. Interleukin-6 receptor inhibition with tocilizumab reduces disease activity in rheumatoid arthritis with inadequate response to disease-modifying antirheumatic drugs: the tocilizumab in combination with traditional disease-modifying antirheumatic drug therapy study. Arthritis Rheum 2008, 58:2968-2980. 10.1002/art.23940, 18821691.
7. Smolen JS, Beaulieu A, Rubbert-Roth A, Ramos-Remus C, Rovensly J, Alecock E, Woodworth T, Alten R, . OPTION Investigators Effect of interleukin-6 receptor inhibition with tocilizumab in patients with rheumatoid arthritis (OPTION study): a double-blind, placebo-controlled, randomized trial. Lancet 2008, 371:987-997. 10.1016/S0140-6736(08)60453-5, 18358926, OPTION Investigators.
8. Emery P, Fleischmann R, Filipowicz-Sosnowska A, Schechtman J, Szczepanski L, Kavanaugh A, Racewicz AJ, van Vollenhoven RF, Li NF, Agarwal S, Hessey EW, Shaw TM, . DANCER Study Group The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, dose-ranging trial. Arthritis Rheum 2006, 54:1390-1400. 10.1002/art.21778, 16649186, DANCER Study Group.
9. Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, Keystone EC, Loveless JE, Burmester GR, Cravets MW, Hessey EW, Shaw T, Totoritis MC, . REFLEX Trial Group Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 2006, 54:2793-2806. 10.1002/art.22025, 16947627, REFLEX Trial Group.
10. Kremer JM, Westhovens R, Leon M, Di Giorgio E, Alten R, Steinfeld S, Russell A, Dougados M, Emery P, Nuamah IF, Williams GR, Becker JC, Hagerty DT, Moreland LW. Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. N Engl J Med 2003, 349:1907-1915. 10.1056/NEJMoa035075, 14614165.
11. Lopez-Diego RS, Weiner HL. Novel therapeutic strategies for multiple sclerosis-a multifaceted adversary. Nat Rev Drug Discov 2008, 7:909-925. 10.1038/nrd2358, 18974749.
12. Yazici Y. Treatment of rheumatoid arthritis: we are getting there. Lancet 2009, 374:178-180. 10.1016/S0140-6736(09)60792-3, 19560809.
13. Myers LK, Kang AH, Postlethwaite AE, Rosloniec EF, Morham SG, Shlopov BV, Goorha S, Ballou LR. The genetic ablation of cyclooxygenase 2 prevents the development of autoimmune arthritis. Arthritis Rheum 2000, 43:2687-2693. 10.1002/1529-0131(200012)43:12<2687::AID-ANR8>3.0.CO;2-9, 11145026.
14. Trebino CE, Stock JL, Gibbons CP, Naiman BM, Wachtmann TS, Umland JP, Pandher K, Lapointe JM, Saha S, Roach ML, Carter D, Thomas NA, Durtschi BA, McNeish JD, Hambor JE, Jakobsson PJ, Carty TJ, Perez JR, Audoly LP. Impaired inflammatory and pain responses in mice lacking an inducible prostaglandin E synthase. Proc Natl Acad Sci USA 2003, 100:9044-9049. 10.1073/pnas.1332766100, 166435, 12835414.
15. Honda T, Segi-Nishida E, Miyachi Y, Narumiya S. Prostacyclin-IP signaling and prostaglandin E2-EP2/EP4 signaling both mediate joint inflammation in mouse collagen-induced arthritis. J Exp Med 2006, 203:325-335. 10.1084/jem.20051310, 2118213, 16446378.
16. Noguchi M, Kimoto A, Kobayashi S, Yoshino T, Miyata K, Sasamata M. Effect of celecoxib, a cyclooxygenase-2 inhibitor, on the pathophysiology of adjuvant arthritis in rat. Eur J Pharmacol 2005, 513:229-235. 10.1016/j.ejphar.2005.01.058, 15862805.
17. Tsuboi H, Nampei A, Matsui Y, Hashimoto J, Kawai S, Ochi T, Yoshikawa H. Celecoxib prevents juxta-articular osteopenia and growth plate destruction adjacent to inflamed joints in rats with collagen-induced arthritis. Mod Rheumatol 2007, 17:115-122. 10.1007/s10165-007-0552-4, 17437166.
18. Taketa T, Sakai A, Tanaka S, Nakai K, Menuki K, Yamane H, Tanaka K, Nakamura T. Selective cyclooxygenase-2 inhibitor prevents reduction of trabecular b:one mass in collagen-induced arthritic mice in association with suppression of RANKL/OPG ratio and IL-6 mRNA expression in synovial tissues but not in bone marrow cells. J Bone Miner Metab 2008, 26:143-151. 10.1007/s00774-007-0808-2, 18301970.
19. Anderson GD, Keys KL, De Ciechi PA, Masferrer JL. Combination therapies that inhibit cyclooxygenase-2 and leukotriene synthesis prevent disease in murine collagen induced arthritis. Inflamm Res 2009, 58:109-117. 10.1007/s00011-009-8149-3, 19184362.
20. Page TH, Turner JJ, Brown AC, Timms EM, Inglis JJ, Brennan FM, Foxwell BM, Ray KP, Feldmann M. Nonsteroidal anti-inflammatory drugs increase TNF production in rheumatoid synovial membrane cultures and whole blood. J Immunol 2010, 185:3694-3701. 10.4049/jimmunol.1000906, 20713883.
21. Grosch S, Tegeder I, Niederberger E, Brautigam L, Geisslinger G. COX-2 independent induction of cell cycle arrest and apoptosis in colon cancer cells by the selective COX-2 inhibitor celecoxib. FASEB J 2001, 15:2742-2744.
22. Miyamoto K, Miyake S, Mizuno M, Oka N, Kusunoki S, Yamamura T. Selective COX-2-inhibitor celecoxib prevents experimental autoimmune encephalomyelitis through COX-2-independent pathway. Brain 2006, 129:1984-1992. 10.1093/brain/awl170, 16835249.
23. Alloza I, Baxter A, Chen Q, Matthiesen R, Vandenbroeck K. Celecoxib inhibits interleukin-12 alphabeta and beta2 folding and secretion by a novel COX2-independent mechanism involving chaperones of the endoplasmic reticulum. Mol Pharmacol 2006, 69:1579-1587. 10.1124/mol.105.020669, 16467190.
24. McLaughlin M, Alloza I, Quoc HP, Scott CJ, Hirabayashi Y, Vandenbroeck K. Inhibition of secretion of interleukin (IL)-12/23 family cytokines by 4-trifluoromethyl-celecoxib is coupled to degradation via the endoplasmic reticulum stress protein HERP. J Biol Chem 2010, 285:6960-6969. 10.1074/jbc.M109.056614, 2844145, 20054003.
25. Kaieda S, Tomi C, Oki S, Yamamura T, Miyake S. Activation of invariant natural killer T cells by synthetic glycolipid ligands suppresses autoantigody-induced arthritis. Arthritis Rheum 2007, 56:1836-1845. 10.1002/art.22714, 17530712.
26. McLaughlin M, Vandenbroeck K. The endoplasmic reticulum protein folding factory and its chaperones: new targets for drug discovery?. Br J Pharmacol 2011, 162:328-345. 10.1111/j.1476-5381.2010.01064.x, 3031055, 20942857.
27. Wheeler MC, Rizzi M, Sasik R, Almanza G, Hardiman G, Zanetti M. KDEL-retained antigen in B lymphocytes induces a proinflammatory response: a posible role for endoplasmic reticulum stress in adaptive T cell immunity. J Immunol 2008, 181:256-264.
28. Andrei C, Dazzi C, Lotti L, Torrisi MR, Chimini G, Rubartelli A. The secretory route of the leaderless protein interleukin 1beta involves exocytosis of endolysosome-related vesicles. Mol Biol Cell 1999, 10:1463-1475. 25302, 10233156.
29. Lee DM, Friend DS, Gurish MF, Benoist C, Mathis D, Brenner MB. Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 2002, 297:1689-1692. 10.1126/science.1073176, 12215644.
30. Kagari T, Doi H, Shimozato T. The importance of IL-1 beta and TNF-alpha, and the noninvolvement of IL-6, in the development of monoclonal antibody-induced arthritis. J Immunol 2002, 169:1459-1466.
31. Chen M, Lam BK, Kanaoka Y, Nigrovic PA, Audoly LP, Austen KF, Lee DM. Neutrophil-derived leukotriene B4 is required for inflammatory arthritis. J Exp Med 2006, 203:837-842. 10.1084/jem.20052371, 2118292, 16567388.
32. Kim ND, Chou RC, Seung E, Tager AM, Luster AD. A unique requirement for the leukotriene B4 receptor BLT1 for neutrophil recruitment in inflammatory arthritis. J Exp Med 2006, 203:829-835. 10.1084/jem.20052349, 2118298, 16567386.
33. Zhou JS, Xing W, Friend DS, Austen KF, Katz HR. Mast cell deficiency in Kit(W-sh) mice does not impair antibody-mediated arthritis. J Exp Med 2007, 204:2797-802. 10.1084/jem.20071391, 2118523, 17998392.
34. Chou RC, Kim ND, Sadik CD, Seung E, Lan Y, Byme MH, Haribabu B, Iwakura Y, Luster AD. Lipid-cytokine-chemokine cascade drives neutrophil recruitment in a murine model of inflammatory arthritis. Immunity 2010, 33:266-278. 10.1016/j.immuni.2010.07.018, 3155777, 20727790.
35. Nandakumar KS, Svensson L, Holmdahl R. Collagen type II-specific monoclonal antibody-induced arthritis in mice: description of the disease and the influence of age, sex, and genes. Am J Pathol 2003, 163:1827-1837. 10.1016/S0002-9440(10)63542-0, 1892447, 14578183.
36. Zhu J, Song X, Lin HP, Young DC, Yan S, Marquez VE, Chen CS. Using cyclooxygenase-2 inhibitors as molecular platforms to develop a new class of apoptosis-inducing agents. J Natl Cancer Inst 2002, 94:1745-1757. 10.1093/jnci/94.23.1745, 12464646.
37. Johnson AJ, Hsu AL, Lin HP, Song X, Chen CS. The cyclo-oxygenase-2 inhibitor celecoxib perturbs intracellular calcium by inhibiting endoplasmic reticulum Ca2+-ATPases: a plausible link with its anti-tumour effect and cardiovascular risks. Biochem J 2002, 366:831-837. 1222837, 12076251.
38. Gitlin JM, Loftin CD. Cyclooxygenase-2 inhibition increases lipopolysaccharide-induced atherosclerosis in mice. Cardiovasc Res 2009, 81:400-407. 2639107, 18948273.
39. Wipke BT, Allen PM. Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J Immunol 2010, 167:1601-1608.
40. Bromley M, Fisher WD, Woolley DE. Mast cells at sites of cartilage erosion in the rheumatoid joint. Ann Rheum Dis 1984, 43:76-79. 10.1136/ard.43.1.76, 1001227, 6696523.
41. Kiener HP, Baghestanian M, Dominkus M, Walchshofer S, Ghannadan M, Willheim M, Sillaber C, Graninger WB, Smolen JS, Valent P. Expression of the C5a receptor (CD88) on synovial mast cells in patients with rheumatoid arthritis. Arthritis Rheum 1998, 41:233-245. 10.1002/1529-0131(199802)41:2<233::AID-ART7>3.0.CO;2-V, 9485081.
42. Sawamukai N, Yukawa S, Saito K, Nakayamada S, Kambayashi T, Tanaka Y. Mast cell-derived tryptase inhibits apoptosis of human rheumatoid synovial fibroblasts via rho-mediated signaling. Arthritis Rheum 2010, 62:952-959. 10.1002/art.27331, 20131259.
43. Eklund KK. Mast cells in the pathogenesis of rheumatic diseases and as potential targets for anti-rheumatic therapy. Immunol Rev 2007, 217:38-52. 10.1111/j.1600-065X.2007.00504.x, 17498050.
44. Hueber AJ, Asquith DL, Miller AM, Reilly J, Kerr S, Leipe J, Melendez AJ, Mclnnes IB. Mast cells express IL-17A in rheumatoid arthritis synovium. J Immunol 2010, 184:3336-3340. 10.4049/jimmunol.0903566, 20200272.
45. Liu J, Divoux A, Sun J, Zhang J, Clement K, Glickman JN, Sukhova GK, Wolters PJ, Du J, Gorgun CZ, Doria A, Libby P, Blumberg RS, Kahn BB, Hotamisligil GS, Shi GP. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med 2009, 15:940-945. 10.1038/nm.1994, 2736875, 19633655.
46. Matsukawa A, Kudo S, Maeda T, Numata K, Watanabe H, Takeda K, Akira S, Ito T. Stat3 in resident macrophages are a repressor protein of inflammatory response. J Immunol 2005, 175:3354-3359.
47. Zhang Y, Ramos BF, Jakschik BA. Neutrophil recruitment by tumor necrosis factor from mast cells in immune complex peritonitis. Science 192 258:1957-1959.
48. Bresalier RS, Sandler RS, Quan H, Bolognese JA, Oxenius B, Horgan K, Lines C, Riddell R, Morton D, Lanas A, Konstam MA, Baron JA. Adenomatous Polyp Prevention on Vioxx (APPROVe) Trial Investigators. Cardiovascular events associated with rofecoxib in a colorectal adenoma chemoprevention trial. N Eng J Med 2005, 352:1092-1102.
49. Bertagnolli MM, Eagle CJ, Zauber AG, Redston M, Breazna A, Kim K, Tang J, Rosenstein RB, Umar A, Bagheri D, Collins NT, Burn J, Chung DC, Dewar T, Foley TR, Hoffman N, Macrae F, Pruitt RE, Saltzman JR, Salzberg B, Sylwestrowicz T, Hawk ET, . Adenoma Prevention with Celecoxib Study Investigators Five-year efficacy and safety analysis of the adenoma prevention with celecoxib trial. Cancer Prev Res (Phila) 2009, 2:310-321. Adenoma Prevention with Celecoxib Study Investigators.
50. Aid S, Langenbach R, Bosetti F. Neuroinflammatory response to lipopolysaccharide is exacerbated in mice genetically deficient in cyclooxygenase-2. J Neuroinflammation 2008, 5:17-30. 10.1186/1742-2094-5-17, 2409311, 18489773.
51. Kobayashi T, Tahara Y, Matsumoto M, Iguchi M, Sano H, Murayama T, Arai H, Oida H, Yurugi-Kobayashi T, Yamashita JK, Katagiri H, Majima M, Yokode M, Kita T, Narumiya S. Roles of thromboxane A(2) and prostacyclin in the development of atherosclerosis in apoE-deficient mice. J Clin Invest 2004, 114:784-794. 516261, 15372102.