Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells

Nature Immunology

Volumn 8, Issue 12, 2007, Pages 1372-1379

  Fitzgerald, Denise C ^a   Zhang, Guang Xian ^a   El Behi, Mohamed ^a   Fonseca Kelly, Zoë ^a   Li, Hongme ^a   Yu, Shuo ^a   Saris, Christiaan J ^b   Gran, Bruno ^a,c   Ciric, Bogoljub ^a   Rostami, Abdolmohamad ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b Department of Inflammation Research ^*  (United States)

^c QUEEN S MEDICAL CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 27; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR T BET;

ADOPTIVE TRANSFER; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE SEVERITY; EFFECTOR CELL; ENCEPHALITIS; FEMALE; IMMUNE DEFICIENCY; IMMUNITY; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; T LYMPHOCYTE; UPREGULATION;

ANIMALS; AUTOIMMUNITY; CENTRAL NERVOUS SYSTEM DISEASES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-17; LYMPHOCYTE ACTIVATION; MICE; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 36248970702     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1540     Document Type: Article

References (45)

1. + T cells through Statl-dependent and -independent mechanisms. Proc. Natl. Acad. Sci. USA 100, 15047-15052 (2003).
2. Owaki, T., Asakawa, M., Fukai, F., Mizuguchi, J. & Yoshimoto, T. IL-27 induces Thl differentiation via p38 MAPK/T-bet- and intercellular adhesion molecule-1/LFA-1/ERK1/2-dependent pathways. J. Immunol. 177, 7579-7587 (2006).
3. Owaki, T. et al. A role for IL-27 in early regulation of Th1 differentiation. J. Immunol. 175, 2191-2200 (2005).
4. Takeda, A. et al. Cutting edge: Role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 duriung initial Th1 commitment. J. Immunol. 170, 4886-4890 (2003).
5. Miyazaki, Y. et al. Exacerbation of experimental allergic asthma by augmented Th2 responses in WSX-1-deficient mice. J. Immunol. 175, 2401-2407 (2005).
6. Rosas, L.E. et al. Interleukin-27R (WSX-1/T-cell cytokine receptor) gene-deficient mice display enhanced resistance to Leishmania donovani infection but develop severe liver immunopathology. Am. J. Pathol. 168, 158-169 (2006).
7. Villarino, A. et al. The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection. Immunity 19, 645-655 (2003).
8. H17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat. Med. 13, 711-718 (2007).
9. Batten, M. et al. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7, 929-936 (2006).
10. Stumhofel, J.S. et al. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7, 937-945 (2006).
11. + T cells. Immunity 16, 779-790 (2002).
12. Pflanz, S. et al. WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27. J. Immunol. 172, 2225-2231 (2004).
13. Larousserie, F. et al. Differential effects of IL-27 on human B cell subsets. J. Immunol. 176, 5890-5897 (2006).
14. Villarino, A.V. et al. Positive and negative regulation of the IL-27 receptor during lymphoid cell activation. J. Immunol. 174 7684-7691 (2005).
15. Wirtz, S. et al. Protection from lethal septic peritonitis by neutralizing the biological function of interleukin 27. J. Exp. Med. 203, 1875-1881 (2006).
16. Owaki, T. et al. IL-27 suppresses CD28-mediated IL-2 production through suppressor of cytokine signaling 3. J. Immunol. 176, 2773-2780 (2006).
17. Villarino, A.V. et al. IL-27 limits IL-2 production during Th1 differentiation. J. Immunol. 176, 237-247 (2006).
18. + T cells partially through STAT3-dependent mechanism. J. Immunol. 177, 5377-5385 (2006).
19. Hamano, S. et al. WSX-1 is required for resistance to Trypanosoma cruzi infection by regulation at proinflammatory cytokine production. Immunity 19, 657-667 (2003).
20. + T cells. J. Immunol. 175, 7093-7097 (2005).
21. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886 (2003).
22. - cells to develop suppressive activity: The role of IL-2, TGF-β, and IL-10. J. Immunol. 172, 5213-5221 (2004).
23. Sullivan, B.M., Juedes, A., Szabo, S.J., von Herrath, M. & Glimcher, L.H. Antigen-driven effector CD8 T cell function regulated by T-bet. Proc. Natl. Acad. Sci. USA 100, 15818-15823 (2003).
24. Szabo, S.J. et al. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100, 655-669 (2000).
25. Ejrnaes, M. et al. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 203, 2461-2472 (2006).
26. Maeda, H. et al. TGF-β enhances macrophage ability to produce IL-10 in normal and tumor-bearing mice. J. Immunol. 155, 4926-4932 (1995).
27. Sullivan, B.M. et al. Increased susceptibility of mice lacking T-bet to infection with Mycobacterium tuberculosis correlates with increased IL-10 and decreased IFN-γ production. J. Immunol. 175, 4593-4602 (2005).
28. Morris, S.C. et al. Effects of IL-12 on in vivo cytokine gene expression and Ig isotype selection. J. Immunol. 152, 1047-1056 (1994).
29. McRae, B.L., Picker, L.J. & van Seventer, G.A. Human recombinant interferon-beta influences T helper subset differentiation by regulating cytokine secretion pattern and expression of homing receptors. Eur. J. Immunol. 27, 2650-2656 (1997).
30. Fitzgerald, D.C. et al. Suppressive effect of IL-27 on encephalitogenic Th17 cells and the effector phase of experimental autoimmune encephalomyelitis. J. Immunol. 179, 3268-3275 (2007).
31. Langrish, C.L. et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201, 233-240 (2005).
32. + effector T cells develop via a lineage distinct from the T helpertype 1 and 2 lineages. Nat Immunol. 6, 1123-1132 (2005).
33. Park, H. et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141 (2005).
34. Taga, K. & Tosato, G. IL-10 inhibits human T cell proliferation and IL-2 production. J. Immunol. 148, 1143-1148 (1992).
35. Deshpande, P., King, I.L. & Segal, B.M. IL-12 driven upregulation of P-selectin ligand on myelin-specific T cells is a critical step in an animal model of autoimmune demyelination. J. Neuroimmunol. 173 35-44 (2006).
36. Ito, A. et al. Transfer of severe experimental autoimmune encephalomyelitis by IL-12- and IL-18-potentiated T cells is estrogen sensitive. J. Immunol., 170, 4B02-4809 (2003). 1
37. Bettelli, E. et al. 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, 3299-3306 (1998).
38. Samoilova, E.B., Horton, J.L. & Chen, Y. Acceleration of experimental autoimmune encephalomyelitis in interleukin-10-deficient mice: Roles of interleukin-10 in disease progression and recovery. Cell. Immunol. 188, 118-124 (1998).
39. 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).
40. Wirtz, S. et al. EBV-induced gene 3 transcription is induced by TLR signaling in primary dendritic cells via NF-κB activation. J. Immunol. 174, 2814-2824 (2005).
41. Moore, K.W., de Waal Malefyt, R., Coffman, R.L. & O'Garra, A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683-765 (2001).
42. - Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204, 285-297 (2007).
43. - Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204, 273-283 (2007).
44. Roers, A. et al. Tcell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J. Exp. Med. 200, 1289-1297 (2004).
45. O'Garra, A. & Vieira, P. T(H)1 cells control themselves by producing interleukin-10. Nat. Rev. Immunol. 7, 425-428 (2007).