Signals mediated by transforming growth factor-β initiate autoimmune encephalomyelitis, but chronic inflammation is needed to sustain disease

Nature Immunology

Volumn 7, Issue 11, 2006, Pages 1151-1156

  Veldhoen, Marc ^a   Hocking, Richard J ^a   Flavell, Richard A ^a   Stockinger, Brigitta ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 17; INTERLEUKIN 23; NEUTRALIZING ANTIBODY; TRANSFORMING GROWTH FACTOR BETA; ZYMOSAN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC INFLAMMATION; CONTROLLED STUDY; CORRELATION FUNCTION; CYTOKINE PRODUCTION; DISEASE COURSE; IMMUNOPATHOGENESIS; IMMUNOSTIMULATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTIC INFILTRATION; MOUSE; MYCOBACTERIUM; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPINAL CORD; T LYMPHOCYTE; TH1 CELL;

ANIMALS; CELL DIFFERENTIATION; CHRONIC DISEASE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNE SERA; INFLAMMATION; INTERLEUKIN-23; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER; TRANSFORMING GROWTH FACTOR BETA;

EID: 33750142276     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1391     Document Type: Article

References (53)

1. H17 and regulatory T cells. Nature 441, 235-238 (2006).
2. Billiau, A. & Matthys, P. Modes of action of Freund's adjuvants in experimental models of autoimmune diseases. J. Leukoc. Biol. 70, 849-860 (2001).
3. 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).
4. Willenborg, D.O., Fordham, S.A., Staykova, M.A., Ramshaw, I.A. & Cowden, W.B. IFN-γ is critical to the control of murine autoimmune encephalomyelitis and regulates both in the periphery and in the target tissue: A possible role for nitric oxide. J. Immunol. 163, 5278-5286 (1999).
5. 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).
6. 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).
7. Zhang, G.X. et al. 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, 2153-2160 (2003).
8. Gutcher, I., Urich, E., Wolter, K., Prinz, M. & Becher, B. Interleukin 18-dependent engagement of interleukin 18 receptor-α is required for autoimmune inflammation. Nat. Immunol. 7, 946-953 (2006).
9. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6, 1123-1132 (2005).
10. Park, H. et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141 (2005).
11. Nakae, S., Nambu, A., Sudo, K. & Iwakura, Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 171, 6173-6177 (2003).
12. Langrish, C.L. et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201, 233-240 (2005).
13. 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).
14. Gorelik, L. & Flavell, R.A. Abrogation of TGFβ signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12, 171-181 (2000).
15. H17 and regulatory T cells. Nature 441, 235-238 (2006).
16. Infante-Duarte, C., Horton, H.F., Byrne, M.C. & Kamradt, T. Microbial lipopeptides induce the production of IL-17 in Th cells. J. Immunol. 165, 6107-6115 (2000).
17. Khader, S.A. et al. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-γ responses if IL-12p70 is available. J. Immunol. 175, 788-795 (2005).
18. Massague, J. The transforming growth factor-β family. Annu. Rev. Cell Biol. 6, 597-641 (1990).
19. Wahl, S.M., Allen, J.B., Costa, G.L., Wong, H.L. & Dasch, J.R. Reversal of acute and chronic synovial inflammation by anti-transforming growth factor β. J. Exp. Med. 177, 225-230 (1993).
20. Wahl, S.M. Transforming growth factor β: The good, the bad, and the ugly. J. Exp. Med. 180, 1587-1590 (1994).
21. + T cells. Int. Immunol. 18, 495-503 (2006).
22. Szczepanik, M., Tutaj, M., Bryniarski, K. & Dittel, B.N. Epicutaneously induced TGF-β-dependent tolerance inhibits experimental autoimmune encephalomyelitis. J. Neuroimmunol. 164, 105-114 (2005).
23. + T cells suppress the progression of allergic encephalomyelitis. J. Leukoc. Biol. 79, 140-146 (2006).
24. Cautain, B. et al. Essential role of TGF-β in the natural resistance to experimental allergic encephalomyelitis in rats. Eur. J. Immunol. 31, 1132-1140 (2001).
25. + regulatory T cells. J. Exp. Med. 201, 737-746 (2005).
26. Yoshitomi, H. et al. A role for fungal β-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J. Exp. Med. 201, 949-960 (2005).
27. H17 lineage. Nature 441, 231-234 (2006).
28. 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).
29. Chen, Y. et al. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J. Clin. Invest. 116, 1317-1326 (2006).
30. Fontenot, J.D., Rasmussen, J.P., Gavin, M.A. & Rudensky, A.Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6, 1142-1151 (2005).
31. Zamvil, S. et al. T-cell clones specific for myelin basic protein induce chronic relapsing paralysis and demyelination. Nature 317, 355-358 (1985).
32. Martin, R., McFarland, H.F. & McFarlin, D.E. Immunological aspects of demyelinating diseases. Annu. Rev. Immunol. 10, 153-187 (1992).
33. Smith, S.B. & Waksman, B.H. Passive transfer and labelling studies on the cell infiltrate in experimental allergic encephalomyelitis. J. Pathol. 99, 237-244 (1969).
34. Lafaille, J.J. The role of helper T cell subsets in autoimmune diseases. Cytokine Growth Factor Rev. 9, 139-151 (1998).
35. Samoilova, E.B., Horton, J.L., Hilliard, B., Liu, T.S. & Chen, Y. IL-6-deficient mice are resistant to experimental autoimmune encephalomyelitis: Roles of IL-6 in the activation and differentiation of autoreactive T cells. J. Immunol. 161, 6480-6486 (1998).
36. Gijbels, K., Brocke, S., Abrams, J.S. & Steinman, L. Administration of neutralizing antibodies to interleukin-6 (IL-6) reduces experimental autoimmune encephalomyelitis and is associated with elevated levels of IL-6 bioactivity in central nervous system and circulation. Mol. Med. 1, 795-805 (1995).
37. Fossiez, F. et al. Interleukin-17. Int. Rev. Immunol. 16, 541-551 (1998).
38. Powell, M.B. et al. Lymphotoxin and tumor necrosis factor-α production by myelin basic protein-specific T cell clones correlates with encephalitogenicity. Int. Immunol. 2, 539-544 (1990).
39. Baker, D. et al. Control of established experimental allergic encephalomyelitis by inhibition of tumor necrosis factor (TNF) activity within the central nervous system using monoclonal antibodies and TNF receptor-immunoglobulin fusion proteins. Eur. J. Immunol. 24, 2040-2048 (1994).
40. Jovanovic, D.V. et al. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-β and TNF-α, by human macrophages. J. Immunol. 160, 3513-3521 (1998).
41. Chabas, D. et al. The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease. Science 294, 1731-1735 (2001).
42. Jansson, M., Panoutsakopoulou, V., Baker, J., Klein, L. & Cantor, H. Cutting edge: Attenuated experimental autoimmune encephalomyelitis in eta-1/osteopontin-deficient mice. J. Immunol. 168, 2096-2099 (2002).
43. Ashkar, S. et al. Eta-1 (osteopontin): An early component of type-1 (cell-mediated) immunity. Science 287, 860-864 (2000).
44. Abel, B., Freigang, S., Bachmann, M.F., Boschert, U. & Kopf, M. Osteopontin is not required for the development of Th1 responses and viral immunity. J. Immunol. 175, 6006-6013 (2005).
45. da Silva, A.P. et al. Exacerbated tissue destruction in DSS-induced acute colitis of OPN-null mice is associated with downregulation of TNF-α expression and nonprogrammed cell death. J. Cell. Physiol. 208, 629-639 (2006).
46. Lock, C. et al. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8, 500-508 (2002).
47. Fossiez, F. et al. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J. Exp. Med. 183, 2593-2603 (1996).
48. Komiyama, Y. et al. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177, 566-573 (2006).
49. McKenzie, B.S., Kastelein, R.A. & Cua, D.J. Understanding the IL-23-IL-17 immune pathway. Trends Immunol. 27, 17-23 (2006).
50. Gantner, B.N., Simmons, R.M., Canavera, S.J., Akira, S. & Underhill, D.M. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 197, 1107-1117 (2003).
51. Dillon, S. et al. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J. Clin. Invest. 116, 916-928 (2006).
52. Du, Z. et al. Selective regulation of IL-10 signaling and function by zymosan. J. Immunol. 176, 4785-4792 (2006).
53. Riley, L.W. Of mice, men, and elephants: Mycobacterium tuberculosis cell envelope lipids and pathogenesis. J. Clin. Invest. 116, 1475-1478 (2006).