Interleukin-6 receptor blockade enhances CD39+ regulatory T cell development in rheumatoid arthritis and in experimental arthritis

Arthritis and Rheumatology

Volumn 66, Issue 2, 2014, Pages 273-283

  Thiolat, A ^a   Semerano, L ^a   Pers, Y M ^b   Biton, J ^a   Lemeiter, D ^a   Portales, P ^c   Quentin, J ^b   Jorgensen, C ^b   Decker, P ^a   Boissier, M C ^a   Louis Plence, P ^b   Bessis, N ^a  

^a UNIVERSITÉ PARIS 13   (France)

^b INSERM   (France)

^c HÔPITAL SAINT ELOI   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD39 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; IMMUNOGLOBULIN G; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MONOCLONAL ANTIBODY; MR 16 1; MR16 1 ANTIBODY; TOCILIZUMAB; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CD39+ REGULATORY T LYMPHOCYTE; CELL EXPANSION; CELL MATURATION; CELL POPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; DRUG RESPONSE; EXPERIMENTAL ARTHRITIS; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FOXP3+CELL; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOPATHOLOGY; IMMUNOTHERAPY; LYMPH NODE; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MALE; MIDDLE AGED; MOUSE; NONHUMAN; OPEN STUDY; PRIORITY JOURNAL; PROSPECTIVE STUDY; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; SPLEEN; T LYMPHOCYTE; TH1 CELL; TH17 CELL; THERAPY EFFECT;

ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD; APYRASE; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, INBRED DBA; MIDDLE AGED; PHENOTYPE; RECEPTORS, INTERLEUKIN-6; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84896262403     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38246     Document Type: Article

References (48)

1. Alonzi T, Fattori E, Lazzaro D, Costa P, Probert L, Kollias G, et al. Interleukin 6 is required for the development of collageninduced arthritis. J Exp Med 1998;187: 461-8.
2. Takagi N, Mihara M, Moriya Y, Nishimoto N, Yoshizaki K, Kishimoto T, et al. Blockage of interleukin-6 receptor ameliorates joint disease in murine collagen-induced arthritis. Arthritis Rheum 1998;41: 2117-21.
3. Madhok R, Crilly A, Watson J, Capell HA. Serum interleukin 6 levels in rheumatoid arthritis: correlations with clinical and laboratory indices of disease activity. Ann Rheum Dis 1993;52: 232-4.
4. Tak PP, Kalden JR. Advances in rheumatology: new targeted therapeutics. Arthritis Res Ther 2011;13 Suppl 1:S5.
5. Dienz O, Eaton SM, Bond JP, Neveu W, Moquin D, Noubade R, et al. The induction of antibody production by IL-6 is indirectly mediated by IL-21 produced by CD4- T cells. J Exp Med 2009;206: 69-78.
6. Boissier MC. Cell and cytokine imbalances in rheumatoid synovitis. Joint Bone Spine 2011;78: 230-4.
7. Hirota K, Hashimoto M, Yoshitomi H, Tanaka S, Nomura T, Yamaguchi T, et al. T cell self-reactivity forms a cytokine milieu for spontaneous development of IL-17- Th cells that cause autoimmune arthritis. J Exp Med 2007;204: 41-7.
8. Geboes L, Dumoutier L, Kelchtermans H, Schurgers E, Mitera T, Renauld JC, et al. Proinflammatory role of the Th17 cytokine interleukin-22 in collagen-induced arthritis in C57BL/6 mice. Arthritis Rheum 2009;60: 390-5.
9. Nakae S, Nambu A, Sudo K, Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol 2003;171: 6173-7.
10. Samson M, Audia S, Janikashvili N, Ciudad M, Trad M, Fraszczak J, et al. Inhibition of interleukin-6 function corrects Th17/Treg cell imbalance in patients with rheumatoid arthritis. Arthritis Rheum 2012;64: 2499-503.
11. Bettelli E, Oukka M, Kuchroo VK. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007;8: 345-50.
12. Doganci A. The IL-6R alpha chain controls lung CD4-CD25- Treg development and function during allergic airway inflammation in vivo. J Clin Invest 2005;115: 313-25.
13. Oberg HH, Wesch D, Grussel S, Rose-John S, Kabelitz D. Differential expression of CD126 and CD130 mediates different STAT-3 phosphorylation in CD4-CD25- and CD25high regulatory T cells. Int Immunol 2006;18: 555-63.
14. Fujimoto M, Serada S, Mihara M, Uchiyama Y, Yoshida H, Koike N, et al. Interleukin-6 blockade suppresses autoimmune arthritis in mice by the inhibition of inflammatory Th17 responses. Arthritis Rheum 2008;58: 3710-9.
15. Morgan ME, Sutmuller RP, Witteveen HJ, van Duivenvoorde LM, Zanelli E, Melief CJ, et al. CD25- cell depletion hastens the onset of severe disease in collagen-induced arthritis. Arthritis Rheum 2003;48: 1452-60.
16. Nguyen LT, Jacobs J, Mathis D, Benoist C. Where FoxP3- dependent regulatory T cells impinge on the development of inflammatory arthritis. Arthritis Rheum 2007;56: 509-20.
17. Jiao Z, Wang W, Jia R, Li J, You H, Chen L, et al. Accumulation of FoxP3-expressing CD4-CD25- T cells with distinct chemokine receptors in synovial fluid of patients with active rheumatoid arthritis. Scand J Rheumatol 2007;36: 428-33.
18. Lin SC, Chen KH, Lin CH, Kuo CC, Ling QD, Chan CH. The quantitative analysis of peripheral blood FOXP3-expressing T cells in systemic lupus erythematosus and rheumatoid arthritis patients. Eur J Clin Invest 2007;37: 987-96.
19. 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-TNFalpha therapy. J Exp Med 2004;200: 277-85.
20. Cao D, van Vollenhoven R, Klareskog L, Trollmo C, Malmstrom V. CD25brightCD4- regulatory T cells are enriched in inflamed joints of patients with chronic rheumatic disease. Arthritis Res Ther 2004;6:R335-46.
21. 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.
22. Van Amelsfort JM, Jacobs KM, Bijlsma JW, Lafeber FP, Taams LS. CD4(-)CD25(-) regulatory T cells in rheumatoid arthritis: differences in the presence, phenotype, and function between peripheral blood and synovial fluid. Arthritis Rheum 2004;50: 2775-85.
23. Nadkarni S, Mauri C, Ehrenstein MR. Anti-TNF-alpha therapy induces a distinct regulatory T cell population in patients with rheumatoid arthritis via TGF-beta. J Exp Med 2007;204: 33-9.
24. Biton J, Semerano L, Delavallee L, Lemeiter D, Laborie M, Grouard-Vogel G, et al. Interplay between TNF and regulatory T cells in a TNF-driven murine model of arthritis. J Immunol 2011;186: 3899-910.
25. Biton J, Boissier MC, Bessis N. TNFalpha: activator or inhibitor of regulatory T cells? Joint Bone Spine 2011;79: 119-23.
26. Aricha R, Mizrachi K, Fuchs S, Souroujon MC. Blocking of IL-6 suppresses experimental autoimmune myasthenia gravis. J Autoimmun 2011;36: 135-41.
27. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO 3rd, et al. 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 2010;62: 2569-81.
28. Van Gestel AM, Prevoo ML, van 't Hof MA, van Rijswijk MH, van de Putte LB de, van Riel PL. Development and validation of the European League Against Rheumatism response criteria for rheumatoid arthritis: comparison with the preliminary American College of Rheumatology and the World Health Organization/International League Against Rheumatism criteria. Arthritis Rheum 1996;39: 34-40.
29. Clavel G, Valvason C, Yamaoka K, Lemeiter D, Laroche L, Boissier MC, et al. Relationship between angiogenesis and inflammation in experimental arthritis. Eur Cytokine Netw 2006;17: 202-10.
30. Denys A, Thiolat A, Descamps D, Lemeiter D, Benihoud K, Bessis N, et al. Intra-articular electrotransfer of mouse soluble tumour necrosis factor receptor in a murine model of rheumatoid arthritis. J Gene Med 2010;12: 659-68.
31. Borsellino G, Kleinewietfeld M, Di Mitri D, Sternjak A, Diamantini A, Giometto R, et al. Expression of ectonucleotidase CD39 by Foxp3- Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 2007;110: 1225-32.
32. Bilate A, Lafaille J. Induced CD4(-)Foxp3(-) regulatory T cells in immune tolerance. Ann Rev Immunol 2012;30: 733-91.
33. Fletcher JM, Lonergan R, Costelloe L, Kinsella K, Moran B, O'Farrelly C, et al. CD39-Foxp3- regulatory T cells suppress pathogenic Th17 cells and are impaired in multiple sclerosis. J Immunol 2009;183: 7602-10.
34. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441: 235-8.
35. Yoshida H, Hashizume M, Mihara M. IL-6 blockade preferentially inhibits Th17 differentiation in collagen-induced arthritis. Rheumatol Int 2011;31: 127-31.
36. Serada S, Fujimoto M, Mihara M, Koike N, Ohsugi Y, Nomura S, et al. IL-6 blockade inhibits the induction of myelin antigenspecific Th17 cells and Th1 cells in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 2008;105: 9041-6.
37. Hohki S, Ohguro N, Haruta H, Nakai K, Terabe F, Serada S, et al. Blockade of interleukin-6 signaling suppresses experimental autoimmune uveoretinitis by the inhibition of inflammatory Th17 responses. Exp Eye Res 2010;91: 162-70.
38. Lissilaa R, Buatois V, Magistrelli G, Williams A, Jones G, Herren S, et al. Although IL-6 trans-signaling is sufficient to drive local immune responses, classical IL-6 signaling is obligate for the induction of T cell-mediated autoimmunity. J Immunol 2010;185: 5512-33.
39. Iwanami K, Matsumoto I, Tanaka-Watanabe Y, Inoue A, Mihara M, Ohsugi Y, et al. Crucial role of the interleukin-6/interleukin-17 cytokine axis in the induction of arthritis by glucose-6-phosphate isomerase. Arthritis Rheum 2008;58: 754-63.
40. Tanaka T, Kishimoto T. Immunotherapeutic implication of IL-6 blockade. Immunotherapy 2012;4: 87-192.
41. Thornton AM, Korty PE, Tran DQ, Wohlfert EA, Murray PE, Belkaid Y, et al. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3- T regulatory cells. J Immunol 2010;184: 3433-41.
42. Akimova T, Beier U, Wang L, Levine MH, Hancock WW. Helios expression is a marker of T cell activation and proliferation. PloS One 2011;6:e24226.
43. Gottschalk RA, Corse E, Allison JP. Response to comment on "expression of Helios in peripherally induced Foxp3- regulatory T cells." J Immunol 2012;189: 500-1.
44. Ye ZJ, Zhou Q, Zhang JC, Li X, Wu C, Qin SM, et al. CD39- regulatory T cells suppress generation and differentiation of Th17 cells in human malignant pleural effusion via a LAP-dependent mechanism. Respir Res 2011;12:77.
45. Sauer AV, Brigida I, Carriglio N, Hernandez RJ, Scaramuzza S, Clavenna D, et al. Alterations in the adenosine metabolism and CD39/CD73 adenosinergic machinery cause loss of Treg cell function and autoimmunity in ADA-deficient SCID. Blood 2012; 119: 1428-39.
46. Kochetkova I, Golden S, Holderness K, Callis G, Pascual DW. IL-35 stimulation of CD39- regulatory T cells confers protection against collagen II-induced arthritis via the production of IL-10. J Immunol 2010;184: 7144-53.
47. Kochetkova I, Thornburg T, Callis G, Pascual DW. Segregated regulatory CD39-CD4- T cell function: TGF-beta-producing Foxp3- and IL-10-producing Foxp3- cells are interdependent for protection against collagen-induced arthritis. J Immunol 2011;187: 4654-66.
48. Chen M, Su W, Lin X, Guo Z, Wang J, Zhang Q, et al. Adoptive transfer of human gingiva-derived mesenchymal stem cells ameliorates collagen-induced arthritis via suppressing Th1 and Th17 cells and enhancement of regulatory T cell differentiation. Arthritis Rheum 2013;65: 1181-93.