Interleukin 18-independent engagement of interleukin 18 receptor-α is required for autoimmune inflammation

Nature Immunology

Volumn 7, Issue 9, 2006, Pages 946-953

  Gutcher, Ilona ^a   Urich, Eduard ^a   Wolter, Karina ^b   Prinz, Marco ^b   Becher, Burkhard ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12; INTERLEUKIN 12P35; INTERLEUKIN 18; INTERLEUKIN 18 RECEPTOR; INTERLEUKIN 18 RECEPTOR ALPHA; INTERLEUKIN 23; INTERLEUKIN 23P40; UNCLASSIFIED DRUG;

ACCESSORY CELL; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNE DISEASE; BONE MARROW CELL; CELL MATURATION; CELL POLARITY; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DISEASE PREDISPOSITION; FEMALE; HELPER CELL; IMMUNOPATHOGENESIS; INFLAMMATORY DISEASE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TH1 CELL;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; INTERLEUKIN-12; INTERLEUKIN-17; INTERLEUKIN-18; INTERLEUKIN-23; MICE; MICE, KNOCKOUT; MITOGENS; RECEPTORS, INTERLEUKIN-18; TH1 CELLS;

EID: 33747623280     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1377     Document Type: Article

References (52)

1. + T-cell subsets in autoimmunity. Curr. Opin. Immunol. 9, 872-883 (1997).
2. Brand, D.D., Kang, A.H. & Rosloniec, E.F. Immunopathogenesis of collagen arthritis. Springer Semin. Immunopathol. 25, 3-18 (2003).
3. Renno, T., Krakowski, M., Piccirillo, C., Lin, J.Y. & Owens, T. TNF-α expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis. Regulation by Th1 cytokines. J. Immunol. 154, 944-953 (1995).
4. Merrill, J.E. at al. Inflammatory leukocytes and cytokines in the peptide-induced disease of experimental allergic encephalomyelitis in SJL and B10.PL mice. Proc. Natl. Acad. Sci. USA 89, 574-578 (1992).
5. Racke, M.K. et al. Cytokine-induced immune deviation as a therapy for inflammatory autoimmune disease. J. Exp. Med. 180, 1961-1966 (1994).
6. van der Veen, R.C. & Stohlman, S.A. Encephalitogenic Th1 cells are inhibited by Th2 cells with related peptide specificity: relative roles of interleukin (IL-4 and IL-10. J. Neuroimmunol. 48, 213-220 (1993).
7. Chen, Y., Kuchroo, V.K., Inobe, J., Hafler, D.A. & Weiner, H.L. Regulatory T cell clones induced by oral tolerance: Suppression of autoimmune encephalomyelitis. Science 265, 1237-1240 (1994).
8. Frei, K. et al. Tumor necrosis factor α and lymphotoxin α are not required for induction of acute experimental autoimmune encephalomyelitis. J. Exp. Med. 185, 2177-2182 (1997).
9. Willenborg, D.O., Fordham, S., Bernard, C.C., Cowden, W.B. & Ramshaw, I.A. IFN-γ plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. J. Immunol. 157, 3223-3227 (1996).
10. Chu, C.Q., Wittmer, S. & Dalton, D.K. 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, 123-128 (2000).
11. Ferber, I.A. et al. Mice with a disrupted IFN-γ gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 156, 5-7 (1996).
12. Becher, B., Durell, B.G. & Noelle, R.J. Experimental autoimmune encephalitis and inflammation in the absence of interleukin-12. J. Clin. Invest. 110, 493-497 (2002).
13. Langrish, C.L. et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201, 233-240 (2005).
14. Park, H. et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141 (2005).
15. Okamura, H. et al. Cloning of a new cytokine that induces IFN-γ production by T cells. Nature 378, 88-91 (1995).
16. Dinarello, C.A. IL-18: A TH1-inducing, proinflammatory cytokine and new member of the IL-1 family. J. Allergy Clin. Immunol. 103, 11-24 (1999).
17. Dinarello, C.A. Interleukin-18. Methods 19, 121-132 (1999).
18. Adachi, O. et al. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9, 143-150 (1998).
19. Suzuki, N. et al. IL-1 receptor-associated kinase 4 is essential for IL-18-mediated NK and Th1 cell responses. J. Immunol. 170, 4031-4035 (2003).
20. O'Neill, L.A. & Dinarello, C.A. The IL-1 receptor/toll-like receptor superfamily: Crucial receptors for inflammation and host defense. Immunol. Today 21, 206-209 (2000).
21. Kaser, A. et al. Interleukin-18 attracts plasmacytoid dendritic cells (DC2s) and promotes Th1 induction by DC2s through IL-18 receptor expression. Blood 103, 648-655 (2004).
22. - T cell subsets to express IL-18 receptor and produce IFN-γ in response to IL-18. J. Immunol. 160, 3759-3765 (1998).
23. Xu, D. et al. Selective expression and functions of interleukin 18 receptor on T helper (Th) type 1 but not Th2 cells. J. Exp. Med. 188, 1485-1492 (1998).
24. Yoshimoto, T. et al. IL-12 up-regulates IL-18 receptor expression on T cells, Th1 cells, and 8 cells: Synergism with IL-18 for IFN-γ production. J. Immunol. 161, 3400-3407 (1998).
25. Boraschi, D. et al. Cytokines in inflammation. Joint Workshop of the Deutsche Gesellschaft fur Immunologie (DGfI) and the Gruppo di Cooperazione in Immunologia (GCI) Assergi (L'Aquila, Italy), February 8-11, 1998. Eur. Cytokine Netw. 9, 205-212 (1998).
26. Torigoe, K. et al. Purification and characterization of the human interleukin-18 receptor. J. Biol. Chem. 272, 25737-25742 (1997).
27. Cua, D.J. et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421, 744-748 (2003).
28. Gran, B. et al. IL-12p35-deficient mice are susceptible to experimental autoimmune encephalomyelitis: Evidence for redundancy in the IL-12 system in the induction of central nervous system autoimmune demyelination. J. Immunol. 169, 7104-7110 (2002).
29. Gran, B. et al. Early administration of IL-12 suppresses EAE through induction of interferon-γ. J. Neuroimmunol. 156, 123-131 (2004).
30. Wei, X.Q. et al. Altered immune responses and susceptibility to Leishmania major and Staphylococcus aureus infection in IL-18-deficient mice. J. Immunol. 163, 2821-2828 (1999).
31. Kinjo, Y. et al. Contribution of IL-18 to Th1 response and host defense against infection by Mycobacteurium tuberculosis: A comparative study with IL-12p40. J. Immunol. 169, 323-329 (2002).
32. Santos, L.L. et al. IL-18 is redundant in T-cell responses and in joint inflammation in antigen-induced arthritis. Immunol. Cell Biol. 84, 166-173 (2006).
33. Hoshino, K. et al Cutting egde: Generation of IL-18 receptor-deficient mice: Evidence for IL-1 receptor-related protein as an essential IL-18 binding receptor. J. Immunol. 162, 5041-5044 (1999).
34. Hickey, W.F. Migration of hematogenous cells through the blood-brain barrier and the initiation of CNS inflammation. Brain Pathol. 1, 97-105 (1991).
35. Wekerle, H., Sun, D., Oropeza-Wekerle, R.L. & Meyermann, R. Immune reactivity in the nervous system: Modulation of T-lymphocyte activation by glial cells. J. Exp. Biol. 132, 43-57 (1987).
36. McColl, S.R. et al. Treatment with anti-granulocyte antibodies inhibits the effector phase of experimental autoimmune encephalomyelitis. J. Immunol. 161, 6421-6426 (1998).
37. Becher, B., Durell, B.G. & Noelle, R.J. IL-23 produced by CNS-resident cells controls T cell encephalitogenicity during the effector phase of experimental autoimmume encephalomyelitis. J. Clin. Invest. 112, 1186-1191 (2003).
38. Shi, F.D., Takeda, K., Akira, S., Sarvetnick, N. & Ljunggren, H.G. IL-18 directs autoreactive T cells and promotes autodestruction in the central nervous system via induction of IFN-γ by NK cells. J. Immunol, 165, 3099-3104 (2000).
39. Leung, B.P. et al. A role for IL-18 in neutrophil activation. J. Immunol. 167, 2879-2886 (2001).
40. Becher, B., Durell, B.G., Miga, A.V., Hickey, W.F. & Noelle, R.J. The clinical course of experimental autoimmune encephalomyelitis and inflammation is controlled by the expression of CD40 within the central nervous system. J. Exp. Med. 193, 967-974 (2001).
41. Grater, M. et al. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat. Med. 11, 328-334 (2005).
42. Vermot-Desroches, C. et al. Monoclonal antibodies specific for the IL-18 receptor. Cell. Immunol. 236, 101-104 (2005).
43. Oppmann, B. et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13, 715-725 (2000).
44. Aggarwal, S., Ghilardi, N., Xie, M.H., de Sauvage, F.J. & Gurney, A.L. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278, 1910-1914 (2003).
45. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6, 1123-1132 (2005).
46. Su, S.B. et al. Essential role of the MyD88 pathway, but nonessential roles of TLRs 2, 4, and 9, in the adjuvant effect promoting Th1-mediated autoimmunity. J. Immunol. 175, 6303-6310 (2005).
47. Jiang, H.R. et al. IL-18 not required for IRBP peptide-induced EAU: studies in gene-deficient mice. Invest. Ophthalmol. Vis. Sci. 42, 177-182 (2001).
48. Sims, J.E. IL-1 and IL-18 receptors, and their extended family. Curr. Opin. Immunol. 14, 117-122 (2002).
49. Veldhoen, M., Hocking, R.J., Atkins, C.J., Locksley, R.M. & Stockinger, B. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24, 179-189 (2006).
50. H17 and regulatory T cells. Nature 441, 235-238 (2006).
51. H17 lineage. Nature 441, 231-234 (2006).
52. Stockinger, B. & Hausmann, B. Functional recognition of in vivo processed self antigen. Int. Immunol. 6, 247-254 (1994).