IL-27 suppresses type 2 immune responses in vivo via direct effects on group 2 innate lymphoid cells

Mucosal Immunology

Volumn 9, Issue 6, 2016, Pages 1384-1394

  Mchedlidze, T ^a   Kindermann, M ^a   Neves, A T ^a   Voehringer, D ^a   Neurath, M F ^a   Wirtz, S ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 27; STAT3 PROTEIN; INTERLEUKIN RECEPTOR;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GROUP 2 INNATE LYMPHOID CELL; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; INTRACELLULAR SIGNALING; LYMPHOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; ANIMAL; EOSINOPHIL; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; LYMPHOCYTE SUBPOPULATION; METABOLISM; PARASITE; PATHOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; EOSINOPHILS; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; IMMUNOMODULATION; INTERLEUKIN-27; LUNG; LYMPHOCYTE SUBSETS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PARASITES; RECEPTORS, INTERLEUKIN; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84991730080     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2016.20     Document Type: Article

References (55)

1. McKenzie, A.N., Spits, H., & Eberl, G. Innate lymphoid cells in inflammation and immunity. Immunity 41, 366-374 (2014
2. Diefenbach, A., Colonna, M., & Koyasu, S. Development, differentiation, and diversity of innate lymphoid cells. Immunity 41, 354-365 (2014
3. Halim, T.Y., et al. Retinoic-Acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 37, 463-474 (2012
4. Wong, S.H., et al. Transcription factor RORalpha is critical for nuocyte development. Nat Immunol 13, 229-236 (2012
5. Hoyler, T., et al. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 37, 634-648 (2012
6. Klein Wolterink R.G. et al. Essential, dose-dependent role for the transcription factor Gata3 in the development of IL-5+ and IL-13+ type 2 innate lymphoid cells Proc Natl Acad Sci U S A 110 10240-10245 2013
7. Spooner, C.J., et al. Specification of type 2 innate lymphocytes by the transcriptional determinant Gfi1. Nat Immunol 14, 1229-1236 (2013
8. Yu, Y., et al. The transcription factor Bcl11b is specifically expressed in group 2 innate lymphoid cells and is essential for their development. J Exp Med 212, 865-874 (2015
9. Walker, J.A., et al. Bcl11b is essential for group 2 innate lymphoid cell development. J Exp Med 212, 875-882 (2015
10. Califano, D., et al. Transcription Factor Bcl11b Controls Identity and Function of Mature Type 2 Innate Lymphoid Cells. Immunity 43, 354-368 (2015
11. von Moltke, J., & Locksley, R.M. I-L-C-2 it: type 2 immunity and group 2 innate lymphoid cells in homeostasis. Curr Opin Immunol 31, 58-65 (2014
12. Koyasu, S., & Moro, K. Th2-type innate immune responses mediated by natural helper cells. Ann N Y Acad Sci 1283, 43-49 (2013
13. Licona-Limon, P., et al. Th9 Cells Drive Host Immunity against Gastrointestinal Worm Infection. Immunity 39, 744-757 (2013
14. McHedlidze, T., et al. Interleukin-33-dependent innate lymphoid cells mediate hepatic fibrosis. Immunity 39, 357-371 (2013
15. Halim, T.Y., Krauss, R.H., Sun, A.C., & Takei, F. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36, 451-463 (2012
16. Christianson, C.A., et al. Persistence of asthma requires multiple feedback circuits involving type 2 innate lymphoid cells and IL-33. J Allergy Clin Immunol 136, 59-68.e14 (2015
17. Turner, J.E., et al. IL-9-mediated survival of type 2 innate lymphoid cells promotes damage control in helminth-induced lung inflammation. J Exp Med 210, 2951-2965 (2013
18. Roediger, B., et al. IL-2 is a critical regulator of group 2 innate lymphoid cell function during pulmonary inflammation. J Allergy Clin Immunol 136, 1653-1663.e7 (2015
19. Neufert, C., et al. IL-27 controls the development of inducible regulatory T cells and Th17 cells via differential effects on STAT1. Eur J Immunol 37, 1809-1816 (2007
20. Wirtz, S., et al. Protection from lethal septic peritonitis by neutralizing the biological function of interleukin 27. J Exp Med 203, 1875-1881 (2006
21. Stumhofer, 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
22. Artis, D., et al. The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity. J Immunol 173, 5626-5634 (2004
23. Miyazaki, Y., et al. Exacerbation of experimental allergic asthma by augmented Th2 responses in WSX-1-deficient mice. J Immunol 175, 2401-2407 (2005
24. Yoshimoto, T., Yoshimoto, T., Yasuda, K., Mizuguchi, J., & Nakanishi, K. IL-27 suppresses Th2 cell development and Th2 cytokines production from polarized Th2 cells: a novel therapeutic way for Th2-mediated allergic inflammation. J Immunol 179, 4415-4423 (2007
25. Moro, K., et al. Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses. Nat Immunol 17, 76-86 (2016
26. Duerr,C.U., et al. Type I interferon restricts type 2 immunopathology through the regulation of group 2 innate lymphoid cells. Nat Immunol 17, 65-75 (2016
27. Pflanz, S., et al. WSX-1 and glycoprotein 130 constitute a signaltransducing receptor for IL-27. J Immunol 172, 2225-2231 (2004
28. Neill, D.R., et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464, 1367-1370 (2010
29. Motomura, Y., et al. Basophil-derived interleukin-4 controls the function of natural helper cells, amember of ILC2s, in lung inflammation. Immunity 40, 758-771 (2014
30. Robinette, M.L., et al. Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat Immunol 16, 306-317 (2015
31. Huang, Y., et al. IL-25-responsive, lineage-negative KLRG1(hi) cells are multipotential inflammatory type 2 innate lymphoid cells. Nat Immunol 16, 161-169 (2015
32. Saenz, S.A., et al. IL-25 simultaneously elicits distinct populations of innate lymphoid cells and multipotent progenitor type 2 (MPPtype2) cells. J Exp Med 210, 1823-1837 (2013
33. Villarino, A., et al. The IL-27 R (WSX-1) is required to suppress T cell hyperactivity during infection. Immunity 19, 645-655 (2003
34. Owaki, T., et al. A role for IL-27 in early regulation of Th1 differentiation. J Immunol 175, 2191-2200 (2005
35. Molofsky, A.B., et al. Interleukin-33 and Interferon-gamma Counter- Regulate Group 2 Innate Lymphoid Cell Activation during Immune Perturbation. Immunity 43, 161-174 (2015
36. Yoshida, H., & Hunter, C.A. The immunobiology of interleukin-27. Annu Rev Immunol 33, 417-443 (2015
37. Hunter, C.A., & Kastelein, R. Interleukin-27: balancing protective and pathological immunity. Immunity 37, 960-969 (2012
38. Mesaros, A., et al. Activation of Stat3 signaling in AgRP neurons promotes locomotor activity. Cell Metab 7, 236-248 (2008
39. Price, A.E., et al. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Natl Acad Sci U S A 107, 11489-11494 (2010
40. Hung, L.Y., et al. IL-33 drives biphasic IL-13 production for noncanonical Type 2 immunity against hookworms. Proc Natl Acad Sci U S A 110, 282-287 (2013
41. Oeser, K., Schwartz, C., & Voehringer, D. Conditional IL-4/IL-13-deficient mice reveal a critical role of innate immune cells for protective immunity against gastrointestinal helminths. Mucosal immunology 8, 672-682 (2015
42. Paul, W.E., & Zhu, J. How are T(H)2-type immune responses initiated and amplified?. Nat Rev Immunol 10, 225-235 (2010
43. Pflanz, S., et al. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4+ Tcells. Immunity 16, 779-790 (2002
44. Mascanfroni, I.D., et al. IL-27 acts on DCs to suppress the T cell response and autoimmunity by inducing expression of the immunoregulatory molecule CD39. Nat Immunol 14, 1054-1063 (2013
45. Dokmeci, E., et al. EBI3 deficiency leads to diminished T helper type 1 and increased T helper type 2 mediated airway inflammation. Immunology 132, 559-566 (2011
46. Fujita, H., et al. Production of both IL-27 and IFN-gammaafter the treatment with a ligand for invariant NK T cells is responsible for the suppression of Th2 response and allergic inflammation in a mouse experimental asthma model. J Immunol 183, 254-260 (2009
47. Halim, T.Y., et al. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40, 425-435 (2014
48. Oliphant, C.J., et al. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity 41, 283-295 (2014
49. Lucas, S., Ghilardi, N., Li, J., & De Sauvage, F.J. IL-27 regulates IL-12 responsiveness of naive CD4+ T cells through Stat1-dependent and - independent mechanisms. Proc Natl Acad Sci U S A 100, 15047-15052 (2003
50. Wohlfert, E.A., et al. GATA3 controls Foxp3(+) regulatory Tcell fate during inflammation in mice. J Clin Invest 121, 4503-4515 (2011
51. Yang, X.O., et al. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 282, 9358-9363 (2007
52. Mjosberg, J., et al. The transcription factorGATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 37, 649-659 (2012
53. Urban, J.F. Jr., et al. IFN inhibits inflammatory responses and protective immunity in mice infected with the nematode parasite, Nippostrongylus brasiliensis. J Immunol 151, 7086-7094 (1993
54. Murray, P.J. Understanding and exploiting the endogenous interleukin-10/ STAT3-mediated anti-inflammatory response. Curr Opin Pharmacol 6, 379-386 (2006
55. Chou, S.J., et al. Geniculocortical input drives genetic distinctions between primary and higher-order visual areas. Science 340, 1239-1242 (2013