Ameliorated course of glucose-6-phosphate isomerase (G6PI)-induced arthritis in IFN-γ receptor knockout mice exposes an arthritis-promoting role of IFN-γ

Journal of Autoimmunity

Volumn 36, Issue 2, 2011, Pages 161-169

  Frey, Oliver ^a   Mitera, Tania ^b   Kelchtermans, Hilde ^b   Schurgers, Evelien ^b   Kamradt, Thomas ^a   Matthys, Patrick ^b  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

Adjuvant; Animal model; Interferon; Osteoclastogenesis; T helper cells

Indexed keywords

FREUND ADJUVANT; GAMMA INTERFERON RECEPTOR; GLUCOSE 6 PHOSPHATE ISOMERASE; IMMUNOGLOBULIN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; BONE MARROW CELL; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; EX VIVO STUDY; FLOW CYTOMETRY; IMMUNIZATION; IMMUNOGLOBULIN BLOOD LEVEL; IN VIVO STUDY; INFLAMMATION; INNATE IMMUNITY; MOUSE; NONHUMAN; OSTEOCLAST ACTIVITY; PRIORITY JOURNAL; SPLEEN CELL; STIMULATION; WILD TYPE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; B-LYMPHOCYTES; FEMALE; FLOW CYTOMETRY; GENETIC PREDISPOSITION TO DISEASE; GLUCOSE-6-PHOSPHATE ISOMERASE; IMMUNITY, CELLULAR; IMMUNITY, INNATE; IMMUNIZATION; INTERFERON-GAMMA; LYMPHOCYTE COUNT; MALE; MICE; MICE, INBRED DBA; MICE, KNOCKOUT; OSTEOCLASTS; RECEPTORS, INTERFERON; T-LYMPHOCYTES;

EID: 79951942586     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2010.12.006     Document Type: Article

References (44)

1. Billiau A., Matthys P. Interferon-gamma: a historical perspective. Cytokine Growth Factor Rev 2009, 20:97.
2. Schroder K., Hertzog P.J., Ravasi T., Hume D.A. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 2004, 75:163.
3. Hu X., Ivashkiv L.B. Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immun 2009, 31:539.
4. Vermeire K., Heremans H., Vandeputte M., Huang S., Billiau A., Matthys P. Accelerated collagen-induced arthritis in IFN-gamma receptor-deficient mice. J Immunol 1997, 158:5507.
5. Irmler I.M., Gajda M., Brauer R. Exacerbation of antigen-induced arthritis in IFN-gamma-deficient mice as a result of unrestricted IL-17 response. J Immunol 2007, 179:6228.
6. Tran E.H., Prince E.N., Owens T. IFN-gamma shapes immune invasion of the central nervous system via regulation of chemokines. J Immunol 2000, 164:2759.
7. Chu C.Q., Wittmer S., Dalton D.K. Failure to suppress the expansion of the activated CD4 T cell population in interferon gamma-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J Exp Med 2000, 192:123.
8. Jones L.S., Rizzo L.V., Agarwal R.K., Tarrant T.K., Chan C.C., Wiggert B., Caspi R.R. IFN-gamma-deficient mice develop experimental autoimmune uveitis in the context of a deviant effector response. J Immunol 1997, 158:5997.
9. Kelchtermans H., Billiau A., Matthys P. How interferon-gamma keeps autoimmune diseases in check. Trends Immunol 2008, 29:479.
10. Matthys P., Vermeire K., Mitera T., Heremans H., Huang S., Schols D., et al. Enhanced autoimmune arthritis in IFN-gamma receptor-deficient mice is conditioned by mycobacteria in Freund's adjuvant and by increased expansion of Mac-1+ myeloid cells. J Immunol 1999, 163:3503.
11. Kelchtermans H., Struyf S., De Klerck B., Mitera T., Alen M., Geboes L., et al. Protective role of IFN-gamma in collagen-induced arthritis conferred by inhibition of mycobacteria-induced granulocyte chemotactic protein-2 production. J Leukoc Biol 2007, 81:1044.
12. De Klerck B., Carpentier I., Lories R.J., Habraken Y., Piette J., Carmeliet G., et al. Enhanced osteoclast development in collagen-induced arthritis in interferon-gamma receptor knock-out mice as related to increased splenic CD11b+ myelopoiesis. Arthritis Res Ther 2004, 6:R220.
13. Kelchtermans H., Schurgers E., Geboes L., Mitera T., Van Damme J., Van Snick J., et al. Effector mechanisms of interleukin-17 in collagen-induced arthritis in the absence of interferon-gamma and counteraction by interferon-gamma. Arthritis Res Ther 2009, 11:R122.
14. Matthys P., Vermeire K., Billiau A. Mac-1(+) myelopoiesis induced by CFA: a clue to the paradoxical effects of IFN-gamma in autoimmune disease models. Trends Immunol 2001, 22:367.
15. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005, 6:1133.
16. Harrington L.E., Hatton R.D., Mangan P.R., Turner H., Murphy T.L., Murphy K.M., Weaver C.T. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005, 6:1123.
17. 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-gamma. Arthritis Res Ther 2005, 7:R402.
18. Koch M.A., Tucker-Heard G., Perdue N.R., Killebrew J.R., Urdahl K.B., Campbell D.J. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol 2009, 10:595.
19. Schubert D., Maier B., Morawietz L., Krenn V., Kamradt T. Immunization with glucose-6-phosphate isomerase induces T cell-dependent peripheral polyarthritis in genetically unaltered mice. J Immunol 2004, 172:4503.
20. Bruns L., Frey O., Morawietz L., Landgraf C., Volkmer R., Kamradt T. Immunization with an immunodominant self-peptide derived from glucose-6-phosphate isomerase induces arthritis in DBA/1 mice. Arthritis Res Ther 2009, 11:R117.
21. Bockermann R., Schubert D., Kamradt T., Holmdahl R. Induction of a B-cell-dependent chronic arthritis with glucose-6-phosphate isomerase. Arthritis Res Ther 2005, 7:R1316.
22. Frey O., Meisel J., Hutloff A., Bonhagen K., Bruns L., Kroczek R.A., et al. ICOS-blockade inhibits accumulation of polyfunctional Th1/Th17 cells and mitigates autoimmune arthritis. Ann Rheum Dis 2010, 69:1495-1501.
23. Frey O., Reichel A., Bonhagen K., Morawietz L., Rauchhaus U., Kamradt T. Regulatory T cell control the transition from acute into chronic inflammation in glucose-6-phosphate isomerase induced arthritis. Ann Rheum Dis 2010, 69:1511-1518.
24. 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.
25. Tanaka-Watanabe Y., Matsumoto I., Iwanami K., Inoue A., Goto D., Ito S., et al. B cells play a crucial role as antigen-presenting cells and collaborate with inflammatory cytokines in glucose-6-phosphate isomerase-induced arthritis. Clin Exp Immunol 2009, 155:285.
26. Svendsen P., Andersen C.B., Willcox N., Coyle A.J., Holmdahl R., Kamradt T., Fugger L. Tracking of proinflammatory collagen-specific T cells in early and late collagen-induced arthritis in humanized mice. J Immunol 2004, 173:7037.
27. Ranges G.E., Sriram S., Cooper S.M. Prevention of type II collagen-induced arthritis by in vivo treatment with anti-L3T4. J Exp Med 1985, 162:1105.
28. Stuart J.M., Dixon F.J. Serum transfer of collagen-induced arthritis in mice. J Exp Med 1983, 158:378.
29. Holmdahl R., Jansson L., Larsson A., Jonsson R. Arthritis in DBA/1 mice induced with passively transferred type II collagen immune serum. Immunohistopathology and serum levels of anti-type II collagen auto-antibodies. Scand J Immunol 1990, 31:147.
30. Huang S., Hendriks W., Althage A., Hemmi S., Bluethmann H., Kamijo R., et al. Immune response in mice that lack the interferon-gamma receptor. Science 1993, 259:1742.
31. Diarra D., Stolina M., Polzer K., Zwerina J., Ominsky M.S., Dwyer D., et al. Dickkopf-1 is a master regulator of joint remodeling. Nat Med 2007, 13:156.
32. Iwanami K., Matsumoto I., Tanaka Y., Inoue A., Goto D., Ito S., et al. Arthritogenic T cell epitope in glucose-6-phosphate isomerase-induced arthritis. Arthritis Res Ther 2008, 10:R130.
33. Chattopadhyay P.K., Yu J., Roederer M. A live-cell assay to detect antigen-specific CD4+ T cells with diverse cytokine profiles. Nat Med 2005, 11:1113.
34. Frentsch M., Arbach O., Kirchhoff D., Moewes B., Worm M., Rothe M., et al. Direct access to CD4+ T cells specific for defined antigens according to CD154 expression. Nat Med 2005, 11:1118.
35. Kirchhoff D., Frentsch M., Leclerk P., Bumann D., Rausch S., Hartmann S., et al. Identification and isolation of murine antigen-reactive T cells according to CD154 expression. Eur J Immunol 2007, 37:2370.
36. Geboes L., De Klerck B., Van Balen M., Kelchtermans H., Mitera T., Boon L., et al. Freund's complete adjuvant induces arthritis in mice lacking a functional interferon-gamma receptor by triggering tumor necrosis factor alpha-driven osteoclastogenesis. Arthritis Rheum 2007, 56:2595.
37. Matsumoto I., Zhang H., Yasukochi T., Iwanami K., Tanaka Y., Inoue A., et al. Therapeutic effects of antibodies to tumor necrosis factor-alpha, interleukin-6 and cytotoxic T-lymphocyte antigen 4 immunoglobulin in mice with glucose-6-phosphate isomerase induced arthritis. Arthritis Res Ther 2008, 10:R66.
38. Boehm U., Klamp T., Groot M., Howard J.C. Cellular responses to interferon-gamma. Annu Rev Immunol 1997, 15:749.
39. Chu C.Q., Swart D., Alcorn D., Tocker J., Elkon K.B. Interferon-gamma regulates susceptibility to collagen-induced arthritis through suppression of interleukin-17. Arthritis Rheum 2007, 56:1145.
40. Shen F., Ruddy M.J., Plamondon P., Gaffen S.L. Cytokines link osteoblasts and inflammation: microarray analysis of interleukin-17- and TNF-alpha-induced genes in bone cells. J Leukoc Biol 2005, 77:388.
41. Manoury-Schwartz B., Chiocchia G., Bessis N., Abehsira-Amar O., Batteux F., Muller S., et al. High susceptibility to collagen-induced arthritis in mice lacking IFN-gamma receptors. J Immunol 1997, 158:5501.
42. Guedez Y.B., Whittington K.B., Clayton J.L., Joosten L.A., van de Loo F.A., van den Berg W.B., Rosloniec E.F. Genetic ablation of interferon-gamma up-regulates interleukin-1beta expression and enables the elicitation of collagen-induced arthritis in a nonsusceptible mouse strain. Arthritis Rheum 2001, 44:2413.
43. Kaplan C., Valdez J.C., Chandrasekaran R., Eibel H., Mikecz K., Glant T.T., Finnegan A. Th1 and Th2 cytokines regulate proteoglycan-specific autoantibody isotypes and arthritis. Arthritis Res 2002, 4:54.
44. Doodes P.D., Cao Y., Hamel K.M., Wang Y., Rodeghero R.L., Mikecz K., et al. IFN-gamma regulates the requirement for IL-17 in proteoglycan-induced arthritis. J Immunol 2010, 184:1552.