Abnormal T cell activation caused by the imbalance of the IL-1/IL-1R antagonist system is responsible for the development of experimental autoimmune encephalomyelitis

International Immunology

Volumn 18, Issue 2, 2006, Pages 399-407

  Matsuki, Taizo ^b   Nakae, Susumu ^c   Sudo, Katsuko ^d   Horai, Reiko ^e   Iwakura, Yoichiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d TOKYO MEDICAL UNIVERSITY   (Japan)

^e NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

Autoimmunity; Cytokines; Dendritic cells; Knockout mouse; T cells

Indexed keywords

AUTOANTIGEN; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PERTUSSIS TOXIN; TUMOR NECROSIS FACTOR ALPHA;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DISEASE SEVERITY; GENE DISRUPTION; GENE TARGETING; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; EPITOPES; FEMALE; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MYELIN-ASSOCIATED GLYCOPROTEIN; RECEPTORS, INTERLEUKIN-1; SIALOGLYCOPROTEINS; T-LYMPHOCYTES;

EID: 31544441415     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxh379     Document Type: Article

References (51)

1. Steinman, L., Martin, R., Bernard, C., Conlon, P. and Oksenberg, J. R. 2002. Multiple sclerosis: Deeper understanding of its pathogenesis reveals new targets for therapy. Annu. Rev. Neurosci. 25:491.
2. Keegan, B. M. and Noseworthy, J. H. 2002. Multiple sclerosis. Annu. Rev. Med. 53:285.
3. Kuchroo, V. K., Anderson, A. C., Waldner, H., Munder, M., Bettelli, E. and Nicholson, L. B. 2002. T cell response in experimental autoimmune encephalomyelitis (EAE): Role of self and cross-reactive antigens in shaping, tuning, and regulating the autopathogenic T cell repertoire. Annu. Rev. Immunol. 20:101.
4. Hemmer, B., Archelos, J. J. and Hartung, H. P. 2002. New concepts in the immunopathogenesis of multiple sclerosis. Nat. Rev. Neurosci. 3:291.
5. Owens, T., Wekerle, H. and Antel, J. 2001. Genetic models for CNS inflammation. Nat. Med. 7:161.
6. Ferber, I. A., Brocke, S., Taylor-Edwards, C. et al. 1996. Mice with a disrupted IFN-γ gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 156:5.
7. Krakowski, M. and Owens, T. 1996. Interferon-γ confers resistance to experimental allergic encephalomyelitis. Eur. J. Immunol. 26: 1641.
8. Willenborg, D. O., Fordham, S., Bernard, C. C., Cowden, W. B. and Ramshaw, I. A. 1996. IFN-γ plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. J. Immunol. 157:3223.
9. Chu, C. Q., Wittmer, S. and Dalton, D. K. 2000. Failure to suppress the expansion of the activated CD4 T cell population in interferon γ-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J. Exp. Med. 192:123.
10. Furlan, R., Brambilla, E., Ruffini, F. et al. 2001. Intrathecal delivery of IFN-γ protects C57BL/6 mice from chronic-progressive experimental autoimmune encephalomyelitis by increasing apoptosis of central nervous system-infiltrating lymphocytes. J. Immunol. 167: 1821.
11. Probert, L., Akassoglou, K., Pasparakis, M., Kontogeorgos, G. and Kollias, G. 1995. Spontaneous inflammatory demyelinating disease in transgenic mice showing central nervous system-specific expression of tumor necrosis factor α. Proc. Natl Acad. Sci. USA 92:11294.
12. Powell, M. B., Mitchell, D., Lederman, J. et al. 1990. Lymphotoxin and tumor necrosis factor-α production by myelin basic protein-specific T cell clones correlates with encephalitogenicity. Int. Immunol. 2:539.
13. Sedgwick, J. D., Riminton, D. S., Cyster, J. G. and Korner, H. 2000. Tumor necrosis factor: A master-regulator of leukocyte movement. Immunol. Today 21:110.
14. Sean Riminton, D., Korner, H., Strickland, D. H., Lemckert, F. A., Pollard, J. D. and Sedgwick, J. D. 1998. Challenging cytokine redundancy: Inflammatory cell movement and clinical course of experimental autoimmune encephalomyelitis are normal in lymphotoxin-deficient, but not tumor necrosis factor-deficient, mice. J. Exp. Med. 187:1517.
15. Kassiotis, G. and Kollias, G. 2001. Uncoupling the proinflammatory from the immunosuppressive properties of tumor necrosis factor (TNF) at the p55 TNF receptor level: Implications for pathogenesis and therapy of autoimmune demyelination. J. Exp. Med. 193:427.
16. Kollias, G. and Kontoyiannis, D. 2002. Role of TNF/TNFR in autoimmunity: specific TNF receptor blockade may be advantageous to anti-TNF treatments. Cytokine Growth Factor Rev. 13:315.
17. Tocci, M. J. and Schmidt, J. A. 1997. Interleukin-1: Structure and function. in Remick, D. G. and Friedland, J. S., eds, Cytokines in Health and Disease, 2nd edn, p. 1. Dekker Encyclopedias, Taylor and Francis Group, KY, USA.
18. Tamaru, M., Tomura, K., Sakamoto, S., Tezuka, K., Tamatani, T. and Narumi, S. 1998. Interleukin-1β induces tissue- and cell type-specific expression of adhesion molecules in vivo. Arterioscler. Thromb. Vasc. Biol. 18:1292.
19. Horai, R., Saijo, S., Tanioka, H. et al. 2000. Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. J. Exp. Med. 191:313.
20. Nicklin, M. J., Hughes, D. E., Barton, J. L., Ure, J. M. and Duff, G. W. 2000. Arterial inflammation in mice lacking the interleukin 1 receptor antagonist gene. J. Exp. Med. 191:303.
21. Jacobs, C. A., Baker, P. E., Roux, E. R. et al. 1991. Experimental autoimmune encephalomyelitis is exacerbated by IL-1α and suppressed by soluble IL-1 receptor. J. Immunol. 146:2983.
22. Martin, D. and Near, S. L. 1995. Protective effect of the interleukin-1 receptor antagonist (IL-1ra) on experimental allergic encephalomyelitis in rats. J. Neuroimmunol. 61:241.
23. Schiffenbauer, J., Streit, W. J., Butfiloski, E., LaBow, M., Edwards, C., III and Moldawer, L. L. 2000. The induction of EAE is only partially dependent on TNF receptor signaling but requires the IL-1 type I receptor. Clin. Immunol. 95:117.
24. Mannie, M. D., Dinarello, C. A. and Paterson, P. Y. 1987. Interleukin 1 and myelin basic protein synergistically augment adoptive transfer activity of lymphocytes mediating experimental autoimmune encephalomyelitis in Lewis rats. J. Immunol. 138:4229.
25. Nakae, S., Asano, M., Horai, R., Sakaguchi, N. and Iwakura, Y. 2001. IL-1 enhances T cell-dependent antibody production through induction of CD40 ligand and OX40 on T cells. J. Immunol. 167:90.
26. Eriksson, U., Kurrer, M. O., Sonderegger, I. et al. 2003. Activation of dendritic cells through the interleukin 1 receptor 1 is critical for the induction of autoimmune myocarditis. J. Exp. Med. 197:323.
27. Shornick, L. P., Bisarya, A. K. and Chaplin, D. D. 2001. IL-1β is essential for langerhans cell activation and antigen delivery to the lymph nodes during contact sensitization: Evidence for a dermal source of IL-1β. Cell. Immunol. 211:105.
28. Nakae, S., Naruse-Nakajima, C., Sudo, K., Horai, R., Asano, M. and Iwakura, Y. 2001. IL-1α, but not IL-1β, is required for contact-allergen-specific T cell activation during the sensitization phase in contact hypersensitivity. Int. Immunol. 13:1471.
29. Horai, R., Asano, M., Sudo, K. et al. 1998. Production of mice deficient in genes for interleukin (IL)-1α, IL-1β, IL-1α/β, and IL-1 receptor antagonist shows that IL-1β is crucial in turpentine-induced fever development and glucocorticoid secretion. J. Exp. Med. 187:1463.
30. Nakae, S., Asano, M., Horai, R. and Iwakura, Y. 2001. Interleukin-1β, but not interleukin-1α, is required for T-cell-dependent antibody production. Immunology 104:402.
31. Nakae, S., Komiyama, Y., Nambu, A. et al. 2002. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17:375.
32. Bettelli, E., Das, M. P., Howard, E. D., Weiner, H. L., Sobel, R. A. and Kuchroo, V. K. 1998. IL-10 is critical in the regulation of autoimmune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice. J. Immunol. 161: 3299.
33. Kassiotis, G., Kranidioti, K. and Kollias, G. 2001. Defective CD4T cell priming and resistance to experimental autoimmune encephalomyelitis in TNF-deficient mice due to innate immune hyporesponsiveness. J. Neuroimmunol. 119:239.
34. van Kooten, C. and Banchereau, J. 2000. CD40-CD40 ligand. J. Leukoc. Biol. 67:2.
35. Weinberg, A. D., Bourdette, D. N., Sullivan, T. J. et al. 1996. Selective depletion of myelin-reactive T cells with the anti-OX-40 antibody ameliorates autoimmune encephalomyelitis. Nat. Med. 2:183.
36. Horai, R., Nakajima, A., Habiro, K. et al. 2004. TNF-α is crucial for the development of autoimmune arthritis in IL-1 receptor antagonist-deficient mice. J. Clin. Investig. 114:1603.
37. Nakae, S., Saijo, S., Horai, R., Sudo, K., Mori, S. and Iwakura, Y. 2003. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc. Natl Acad. Sci. USA 100:5986.
38. Saijo, S., Asano, M., Horai, R., Yamamoto, H. and Iwakura, Y. 2002. Suppression of autoimmune arthritis in interleukin-1-deficient mice in which T cell activation is impaired due to low levels of CD40 ligand and OX40 expression on T cells. Arthritis Rheum. 46:533.
39. He, J., Gurunathan, S., Iwasaki, A., Ash-Shaheed, B. and Kelsall, B. L. 2000. Primary role for Gi protein signaling in the regulation of interleukin 12 production and the induction of T helper cell type 1 responses. J. Exp. Med. 191:1605.
40. Shive, C. L., Hofstetter, H., Arredondo, L., Shaw, C. and Forsthuber, T. G. 2000. The enhanced antigen-specific production of cylokines induced by pertussis toxin is due to clonal expansion of T cells and not to altered effector functions of long-term memory cells. Eur. J. Immunol. 30:2422.
41. Ryan, M., McCarthy, L., Rappuoli, R., Mahon, B. P. and Mills, K. H. 1998. Pertussis toxin potentiates Th1 and Th2 responses to co-injected antigen: Adjuvant action is associated with enhanced regulatory cytokine production and expression of the co-stimulatory molecules B7-1, B7-2 and CD28. Int. Immunol. 10:651.
42. Nakae, S., Komiyama, Y., Yokoyama, H. et al. 2003. IL-1 is required for allergen-specific Th2 cell activation and the development of airway hypersensitivity response. Int. Immunol. 15:483.
43. Schmitz, N., Kurrer, M. and Kopf, M. 2003. The IL-1 receptor 1 is critical for Th2 cell type airway immune responses in a mild but not in a more severe asthma model. Eur. J. Immunol. 33:991.
44. Frei, K., Eugster, H. P., Bopst, M., Constantinescu, C. S., Lavi, E. and Fontana, A. 1997. Tumor necrosis factor α and lymphotoxin α are not required for induction of acute experimental autoimmune encephalomyelitis. J. Exp. Med. 185:2177.
45. Manoury-Schwartz, B., Chiocchia, G., Bessis, N. et al. 1997. High susceptibility to collagen-induced arthritis in mice lacking IFN-γ receptors. J. Immunol. 158:5501.
46. Lock, C., Hermans, G., Pedotti, R. et al. 2002. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8:500.
47. Aggarwal, S., Ghilardi, N., Xie, M. H., de Sauvage, F. J. and Gurney, A. L. 2003. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278:1910.
48. Cua, D. J., Sherlock, J., Chen, Y. et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421:744.
49. Zhang, G. X., Gran, B., Yu, S. et al. 2003. Induction of experimental autoimmune encephalomyelitis in IL-12 receptor-β2-deficient mice: IL-12 responsiveness is not required in the pathogenesis of inflammatory demyelination in the central nervous system. J. Immunol. 170:2153.
50. Gran, B., Chu, N., Zhang, G. X. et al. 2004. Early administration of IL-12 suppresses EAE through induction of interferon-γ. J. Neuroimmunol. 156:123.
51. Langrish, C. L., Chen, Y., Blumenschein, W. M. et al. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201:233.