Selective tumor necrosis factor receptor i blockade is antiinflammatory and reveals immunoregulatory role of tumor necrosis factor receptor II in collagen-induced arthritis

Arthritis and Rheumatology

Volumn 66, Issue 10, 2014, Pages 2728-2738

  McCann, Fiona E ^a   Perocheau, Dany P ^a   Ruspi, Gerhard ^a   Blazek, Katrina ^a   Davies, Marie L ^b   Feldmann, Marc ^a   Dean, Jonathan L E ^a   Stoop, A Allart ^b   Williams, Richard O ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b GLAXOSMITHKLINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRHEUMATIC AGENT; CELL PROTEIN; DMS5538; DMS5540; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 17ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; KERATINOCYTE DERIVED CHEMOKINE; MTNFRII FC; RANTES; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL FUNCTION; CELL INFILTRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; DRUG DETERMINATION; DRUG HALF LIFE; EFFECTOR CELL; EX VIVO STUDY; FLUORESCENCE ACTIVATED CELL SORTER; GENE DELETION; IMMUNOREGULATION; IN VIVO STUDY; LIGAND BINDING; LYMPH NODE CELL; MALE; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REGULATORY T LYMPHOCYTE; REMISSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHEUMATOID ARTHRITIS; RNA EXTRACTION; SIGNAL TRANSDUCTION; SPLEEN CELL; T LYMPHOCYTE SUBPOPULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; ARTHRITIS, EXPERIMENTAL; DBA MOUSE; DRUG EFFECTS; IMMUNOLOGY; INFLAMMATION; METABOLISM;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ARTHRITIS, EXPERIMENTAL; CELL PROLIFERATION; FORKHEAD TRANSCRIPTION FACTORS; INFLAMMATION; MALE; MICE; MICE, INBRED DBA; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; T-LYMPHOCYTES, REGULATORY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84908365717     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38755     Document Type: Article

References (49)

1. Ehrenstein MR, Evans JG, Singh A, Moore S, Warnes G, Isenberg DA, et al. Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFα therapy. J Exp Med 2004; 200: 277-85.
2. Nadkarni S, Mauri C, Ehrenstein MR,. Anti-TNF-α therapy induces a distinct regulatory T cell population in patients with rheumatoid arthritis via TGF-β. J Exp Med 2007; 204: 33-9.
3. Toubi E, Kessel A, Mahmudov Z, Hallas K, Rozenbaum M, Rosner I,. Increased spontaneous apoptosis of CD4+CD25+ T cells in patients with active rheumatoid arthritis is reduced by infliximab. Ann N Y Acad Sci 2005; 1051: 506-14.
4. Van Amelsfort JM, van Roon JA, Noordegraaf M, Jacobs KM, Bijlsma JW, Lafeber FP, et al. Proinflammatory mediator-induced reversal of CD4+,CD25+ regulatory T cell-mediated suppression in rheumatoid arthritis. Arthritis Rheum 2007; 56: 732-42.
5. hi T-regulatory cells. Blood 2006; 108: 253-61.
6. Huang Z, Yang B, Shi Y, Cai B, Li Y, Feng W, et al. Anti-TNF-α therapy improves Treg and suppresses Teff in patients with rheumatoid arthritis. Cell Immunol 2012; 279: 25-9.
7. Kelchtermans H, De Klerck B, Mitera T, Van Balen M, Bullens D, Billiau A, et al. Defective CD4+CD25+ regulatory T cell functioning in collagen-induced arthritis: an important factor in pathogenesis, counter-regulated by endogenous IFN-γ. Arthritis Res Ther 2005; 7: R402-15.
8. Korn T, Reddy J, Gao W, Bettelli E, Awasthi A, Petersen TR, et al. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat Med 2007; 13: 423-31.
9. Viglietta V, Baecher-Allan C, Weiner HL, Hafler DA,. Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis. J Exp Med 2004; 199: 971-9.
10. + T-cells from patients with type 1 diabetes. Diabetes 2005; 54: 92-9.
11. Ryba M, Marek N, Hak L, Rybarczyk-Kapturska K, Mysliwiec M, Trzonkowski P, et al. Anti-TNF rescue CD4+Foxp3+ regulatory T cells in patients with type 1 diabetes from effects mediated by TNF. Cytokine 2011; 55: 353-61.
12. Chee J, Angstetra E, Mariana L, Graham KL, Carrington EM, Bluethmann H, et al. TNF receptor 1 deficiency increases regulatory T cell function in nonobese diabetic mice. J Immunol 2011; 187: 1702-12.
13. Chen X, Baumel M, Mannel DN, Howard OM, Oppenheim JJ,. Interaction of TNF with TNF receptor type 2 promotes expansion and function of mouse CD4+CD25+ T regulatory cells. J Immunol 2007; 179: 154-61.
14. + T regulatory cells: applicability to tumor-infiltrating T regulatory cells. J Immunol 2008; 180: 6467-71.
15. Chen X, Subleski JJ, Hamano R, Howard OM, Wiltrout RH, Oppenheim JJ,. Co-expression of TNFR2 and CD25 identifies more of the functional CD4+FOXP3+ regulatory T cells in human peripheral blood. Eur J Immunol 2010; 40: 1099-106.
16. Hamano R, Huang J, Yoshimura T, Oppenheim JJ, Chen X,. TNF optimally activates regulatory T cells by inducing TNF receptor superfamily members TNFR2, 4-1BB and OX40. Eur J Immunol 2011; 41: 2010-20.
17. Tsakiri N, Papadopoulos D, Denis MC, Mitsikostas DD, Kollias G,. TNFR2 on non-haematopoietic cells is required for Foxp3+ Treg-cell function and disease suppression in EAE. Eur J Immunol 2012; 42: 403-12.
18. Ma HL, Napierata L, Stedman N, Benoit S, Collins M, Nickerson-Nutter C, et al. Tumor necrosis factor α blockade exacerbates murine psoriasis-like disease by enhancing Th17 function and decreasing expansion of Treg cells. Arthritis Rheum 2010; 62: 430-40.
19. Housley WJ, Adams CO, Nichols FC, Puddington L, Lingenheld EG, Zhu L, et al. Natural but not inducible regulatory T cells require TNF-α signaling for in vivo function. J Immunol 2011; 186: 6779-87.
20. Kleijwegt FS, Laban S, Duinkerken G, Joosten AM, Zaldumbide A, Nikolic T, et al. Critical role for TNF in the induction of human antigen-specific regulatory T cells by tolerogenic dendritic cells. J Immunol 2010; 185: 1412-8.
21. Grinberg-Bleyer Y, Saadoun D, Baeyens A, Billiard F, Goldstein JD, Gregoire S, et al. Pathogenic T cells have a paradoxical protective effect in murine autoimmune diabetes by boosting Tregs. J Clin Invest 2010; 120: 4558-68.
22. Chen G, Goeddel DV,. TNF-R1 signaling: a beautiful pathway. Science 2002; 296: 1634-5.
23. Bluml S, Binder NB, Niederreiter B, Polzer K, Hayer S, Tauber S, et al. Antiinflammatory effects of tumor necrosis factor on hematopoietic cells in a murine model of erosive arthritis. Arthritis Rheum 2010; 62: 1608-19.
24. Peschon JJ, Torrance DS, Stocking KL, Glaccum MB, Otten C, Willis CR, et al. TNF receptor-deficient mice reveal divergent roles for p55 and p75 in several models of inflammation. J Immunol 1998; 160: 943-52.
25. Williams RO,. Collagen-induced arthritis in mice. Copyright © 2014 by the American College of Rheumatology. Methods Mol Med 2007; 136: 191-9.
26. Ward ES, Gussow D, Griffiths AD, Jones PT, Winter G,. Binding activities of a repertoire of single immunoglobulin variable domains secreted from Escherichia coli. Nature 1989; 341: 544-6.
27. Holt LJ, Basran A, Jones K, Chorlton J, Jespers LS, Brewis ND, et al. Anti-serum albumin domain antibodies for extending the half-lives of short lived drugs. Protein Eng Des Sel 2008; 21: 283-8.
28. Notley CA, Inglis JJ, Alzabin S, McCann FE, McNamee KE, Williams RO,. Blockade of tumor necrosis factor in collagen-induced arthritis reveals a novel immunoregulatory pathway for Th1 and Th17 cells. J Exp Med 2008; 205: 2491-7.
29. Bluml S, Scheinecker C, Smolen JS, Redlich K,. Targeting TNF receptors in rheumatoid arthritis. Int Immunol 2012; 24: 275-81.
30. Tada Y, Ho A, Koarada S, Morito F, Ushiyama O, Suzuki N, et al. Collagen-induced arthritis in TNF receptor-1-deficient mice: TNF receptor-2 can modulate arthritis in the absence of TNF receptor-1. Clin Immunol 2001; 99: 325-33.
31. Armaka M, Apostolaki M, Jacques P, Kontoyiannis DL, Elewaut D, Kollias G,. Mesenchymal cell targeting by TNF as a common pathogenic principle in chronic inflammatory joint and intestinal diseases. J Exp Med 2008; 205: 331-7.
32. Elicabe RJ, Cargnelutti E, Serer MI, Stege PW, Valdez SR, Toscano MA, et al. Lack of TNFR p55 results in heightened expression of IFN-γ and IL-17 during the development of reactive arthritis. J Immunol 2010; 185: 4485-95.
33. Aerts NE, De Knop KJ, Leysen J, Ebo DG, Bridts CH, Weyler JJ, et al. Increased IL-17 production by peripheral T helper cells after tumour necrosis factor blockade in rheumatoid arthritis is accompanied by inhibition of migration-associated chemokine receptor expression. Rheumatology 2010; 49: 2264-72.
34. Alzabin S, Abraham SM, Taher TE, Palfreeman A, Hull D, McNamee K, et al. Incomplete response of inflammatory arthritis to TNFα blockade is associated with the Th17 pathway. Ann Rheum Dis 2012; 71: 1741-8.
35. Stummvoll GH, DiPaolo RJ, Huter EN, Davidson TS, Glass D, Ward JM, et al. Th1, Th2, and Th17 effector T cell-induced autoimmune gastritis differs in pathological pattern and in susceptibility to suppression by regulatory T cells. J Immunol 2008; 181: 1908-16.
36. Flores-Borja F, Jury EC, Mauri C, Ehrenstein MR,. Defects in CTLA-4 are associated with abnormal regulatory T cell function in rheumatoid arthritis. Proc Natl Acad Sci U S A 2008; 105: 19396-401.
37. Ghoreschi K, Laurence A, Yang XP, Hirahara K, O'Shea JJ,. T helper 17 cell heterogeneity and pathogenicity in autoimmune disease. Trends Immunol 2011; 32: 395-401.
38. Lubberts E,. Th17 cytokines and arthritis. Semin Immunopathol 2010; 32: 43-53.
39. Chen X, Wu X, Zhou Q, Howard OM, Netea MG, Oppenheim JJ,. TNFR2 is critical for the stabilization of the CD4+Foxp3+ regulatory T cell phenotype in the inflammatory environment. J Immunol 2013; 190: 1076-84.
40. McGovern JL, Nguyen DX, Notley CA, Mauri C, Isenberg DA, Ehrenstein MR,. Th17 cells are restrained by Treg cells via the inhibition of interleukin-6 in patients with rheumatoid arthritis responding to anti-tumor necrosis factor antibody therapy. Arthritis Rheum 2012; 64: 3129-38.
41. Kaymakcalan Z, Sakorafas P, Bose S, Scesney S, Xiong L, Hanzatian DK, et al. Comparisons of affinities, avidities, and complement activation of adalimumab, infliximab, and etanercept in binding to soluble and membrane tumor necrosis factor. Clin Immunol 2009; 131: 308-16.
42. Lipsky PE, van der Heijde DM, St. Clair EW, Furst DE, Breedveld FC, Kalden JR, et al, for the Anti-Tumor Necrosis Factor Trial in Rheumatoid Arthritis with Concomitant Therapy Study Group. Infliximab and methotrexate in the treatment of rheumatoid arthritis. N Engl J Med 2000; 343: 1594-602.
43. Weinblatt ME, Kremer JM, Bankhurst AD, Bulpitt KJ, Fleischmann RM, Fox RI, et al. A trial of etanercept, a recombinant tumor necrosis factor receptor:Fc fusion protein, in patients with rheumatoid arthritis receiving methotrexate. N Engl J Med 1999; 340: 253-9.
44. Mugnier B, Balandraud N, Darque A, Roudier C, Roudier J, Reviron D,. Polymorphism at position -308 of the tumor necrosis factor α gene influences outcome of infliximab therapy in rheumatoid arthritis. Arthritis Rheum 2003; 48: 1849-52.
45. Padyukov L, Lampa J, Heimburger M, Ernestam S, Cederholm T, Lundkvist I, et al. Genetic markers for the efficacy of tumour necrosis factor blocking therapy in rheumatoid arthritis. Ann Rheum Dis 2003; 62: 526-9.
46. Martinez A, Salido M, Bonilla G, Pascual-Salcedo D, Fernandez-Arquero M, de Miguel S, et al. Association of the major histocompatibility complex with response to infliximab therapy in rheumatoid arthritis patients. Arthritis Rheum 2004; 50: 1077-82.
47. Cui J, Stahl EA, Saevarsdottir S, Miceli C, Diogo D, Trynka G, et al. Genome-wide association study and gene expression analysis identifies CD84 as a predictor of response to etanercept therapy in rheumatoid arthritis. PLoS Genetics 2013; 9: e1003394.
48. Van Schouwenburg PA, Rispens T, Wolbink GJ,. Immunogenicity of anti-TNF biologic therapies for rheumatoid arthritis. Nat Rev Rheumatol 2013; 9: 164-72.
49. Chen DY, Chen YM, Chen HH, Hsieh CW, Lin CC, Lan JL,. Increasing levels of circulating Th17 cells and interleukin-17 in rheumatoid arthritis patients with an inadequate response to anti-TNF-α therapy. Arthritis Res Ther 2011; 13: R126.