IL-4 confers resistance to IL-27-mediated suppression on CD4+ T cells by impairing signal transducer and activator of transcription 1 signaling

Journal of Allergy and Clinical Immunology

Volumn 132, Issue 4, 2013, Pages

  Chen, Zhihong ^a   Wang, Shanze ^a   Erekosima, Nkiruka ^a   Li, Yapeng ^a   Hong, Jessie ^a   Qi, Xiaopeng ^a   Merkel, Patricia ^a   Nagabhushanam, Vijaya ^a   Choo, Eugene ^a   Katial, Rohit ^a   Alam, Rafeul ^a   Trikha, Anita ^a   Chu, Hong Wei ^b   Zhuang, Yonghua ^a   Jin, Meiling ^a   Bai, Chunxue ^a   Huang, Hua ^a,c  

^a DEPARTMENT OF MEDICINE   (United States)

^b FUDAN UNIVERSITY   (China)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Asthma; IL 27; IL 4; signal transducer and activator of transcription 1 signaling; suppressor of cytokine signaling 3

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 27; INTERLEUKIN 4; MESSENGER RNA; SMALL INTERFERING RNA; STAT1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTHMA; CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UPREGULATION; WESTERN BLOTTING;

EID: 84884900899     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2013.06.035     Document Type: Article

References (53)

1. H. Huang Suppressing allergic immune responses Front Biosci (Elite Ed) 3 2011 864 870
2. S.J. Szabo, B.M. Sullivan, C. Stemmann, A.R. Satoskar, B.P. Sleckman, and L.H. Glimcher Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells Science 295 2002 338 342
3. S.J. Szabo, S.T. Kim, G.L. Costa, X. Zhang, C.G. Fathman, and L.H. Glimcher A novel transcription factor, T-bet, directs Th1 lineage commitment Cell 100 2000 655 669
4. J. Zhu, D. Jankovic, A.J. Oler, G. Wei, S. Sharma, and G. Hu The transcription factor T-bet is induced by multiple pathways and prevents an endogenous Th2 cell program during Th1 cell responses Immunity 37 2012 660 673
5. T. Usui, J.C. Preiss, Y. Kanno, Z.J. Yao, J.H. Bream, and J.J. O'Shea T-bet regulates Th1 responses through essential effects on GATA-3 function rather than on IFNG gene acetylation and transcription J Exp Med 203 2006 755 766
6. S. Finotto, M.F. Neurath, J.N. Glickman, S. Qin, H.A. Lehr, and F.H. Green Development of spontaneous airway changes consistent with human asthma in mice lacking T-bet Science 295 2002 336 338
7. B.A. Raby, E.S. Hwang, K. Van Steen, K. Tantisira, S. Peng, and A. Litonjua T-bet polymorphisms are associated with asthma and airway hyperresponsiveness Am J Respir Crit Care Med 173 2006 64 70
8. Y. Zhuang, Z. Huang, J. Nishida, M. Brown, L. Zhang, and H. Huang A continuous T-bet expression is required to silence the interleukin-4-producing potential in T helper type 1 cells Immunology 128 2009 34 42
9. M.H. Kaplan, Y.L. Sun, T. Hoey, and M.J. Grusby Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice Nature 382 1996 174 177
10. S. Taki, T. Sato, K. Ogasawara, T. Fukuda, M. Sato, and S. Hida Multistage regulation of Th1-type immune responses by the transcription factor IRF-1 Immunity 6 1997 673 679
11. M. Lohoff, D. Ferrick, H.W. Mittrucker, G.S. Duncan, S. Bischof, and M. Rollinghoff Interferon regulatory factor-1 is required for a T helper 1 immune response in vivo Immunity 6 1997 681 689
12. S. Hida, M. Tadachi, T. Saito, and S. Taki Negative control of basophil expansion by IRF-2 critical for the regulation of Th1/Th2 balance Blood 106 2005 2011 2017
13. A. Fukushima, T. Yamaguchi, W. Ishida, K. Fukata, K. Udaka, and H. Ueno Mice lacking the IFN-gamma receptor or fyn develop severe experimental autoimmune uveoretinitis characterized by different immune responses Immunogenetics 57 2005 337 343
14. J. Hu-Li, H. Huang, J. Ryan, and W.E. Paul In differentiated CD4+ T cells, interleukin 4 production is cytokine-autonomous, whereas interferon gamma production is cytokine-dependent Proc Natl Acad Sci U S A 94 1997 3189 3194
15. M. Messi, I. Giacchetto, K. Nagata, A. Lanzavecchia, G. Natoli, and F. Sallusto Memory and flexibility of cytokine gene expression as separable properties of human T(H)1 and T(H)2 lymphocytes Nat Immunol 4 2003 78 86
16. E. Murphy, K. Shibuya, N. Hosken, P. Openshaw, V. Maino, and K. Davis Reversibility of T helper 1 and 2 populations is lost after long-term stimulation J Exp Med 183 1996 901 913
17. J.P. Huber, H.J. Ramos, M.A. Gill, and J.D. Farrar Cutting edge: type I IFN reverses human Th2 commitment and stability by suppressing GATA3 J Immunol 185 2010 813 817
18. S.J. Szabo, A.S. Dighe, U. Gubler, and K.M. Murphy Regulation of the interleukin (IL)-12R beta 2 subunit expression in developing T helper 1 (Th1) and Th2 cells J Exp Med 185 1997 817 824
19. T. Usui, R. Nishikomori, A. Kitani, and W. Strober GATA-3 suppresses Th1 development by downregulation of Stat4 and not through effects on IL-12Rbeta2 chain or T-bet Immunity 18 2003 415 428
20. A. Villarino, L. Hibbert, L. Lieberman, E. Wilson, T. Mak, and H. Yoshida The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection Immunity 19 2003 645 655
21. R.A. Kastelein, C.A. Hunter, and D.J. Cua Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation Annu Rev Immunol 25 2007 221 242
22. C.A. Hunter New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions Nat Rev Immunol 5 2005 521 531
23. T. Owaki, M. Asakawa, F. Fukai, J. Mizuguchi, and T. Yoshimoto IL-27 induces Th1 differentiation via p38 MAPK/T-bet- and intercellular adhesion molecule-1/LFA-1/ERK1/2-dependent pathways J Immunol 177 2006 7579 7587
24. A. Amadi-Obi, C.R. Yu, X. Liu, R.M. Mahdi, G.L. Clarke, and R.B. Nussenblatt TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1 Nat Med 13 2007 711 718
25. D. Artis, A. Villarino, M. Silverman, W. He, E.M. Thornton, and S. Mu The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity J Immunol 173 2004 5626 5634
26. T. Yoshimoto, K. Yasuda, J. Mizuguchi, and K. Nakanishi 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 2007 4415 4423
27. S. Lucas, N. Ghilardi, J. Li, and F.J. de Sauvage 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 2003 15047 15052
28. M.A. Meraz, J.M. White, K.C. Sheehan, E.A. Bach, S.J. Rodig, and A.S. Dighe Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway Cell 84 1996 431 442
29. G. Le Gros, S.Z. Ben-Sasson, R. Seder, F.D. Finkelman, and W.E. Paul Generation of interleukin 4 (IL-4)-producing cells in vivo and in vitro: IL-2 and IL-4 are required for in vitro generation of IL-4-producing cells J Exp Med 172 1990 921 929
30. G.L. Stritesky, R. Muthukrishnan, S. Sehra, R. Goswami, D. Pham, and J. Travers The transcription factor STAT3 is required for T helper 2 cell development Immunity 34 2011 39 49
31. C. Neufert, C. Becker, S. Wirtz, M.C. Fantini, B. Weigmann, and P.R. Galle IL-27 controls the development of inducible regulatory T cells and Th17 cells via differential effects on STAT1 Eur J Immunol 37 2007 1809 1816
32. Y. Zhuang, Z. Huang, J. Nishida, L. Zhang, and H. Huang Signaling pathways that lead to the silencing of the interleukin-4-producing potential in Th1 cells J Interferon Cytokine Res 29 2009 399 406
33. T. Pecaric-Petkovic, S.A. Didichenko, S. Kaempfer, N. Spiegl, and C.A. Dahinden Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33 Blood 113 2009 1526 1534
34. D.Y. Leung, P.S. Gao, D.N. Grigoryev, N.M. Rafaels, J.E. Streib, and M.D. Howell Human atopic dermatitis complicated by eczema herpeticum is associated with abnormalities in IFN-gamma response J Allergy Clin Immunol 127 2011 965 973 e1-5
35. G. Le Gros, S.Z. Ben-Sasson, R. Seder, F.D. Finkelman, and W.E. Paul Generation of interleukin 4 (IL-4)-producing cells in vivo and in vitro: IL-2 and IL-4 are required for in vitro generation of IL-4-producing cells J Immunol 181 2008 2943 2951
36. J.C. Kam, S.J. Szefler, W. Surs, E.R. Sher, and D.Y. Leung Combination IL-2 and IL-4 reduces glucocorticoid receptor-binding affinity and T cell response to glucocorticoids J Immunol 151 1993 3460 3466
37. Q. Liang, L. Guo, S. Gogate, Z. Karim, A. Hanifi, and D.Y. Leung IL-2 and IL-4 stimulate MEK1 expression and contribute to T cell resistance against suppression by TGF-beta and IL-10 in asthma J Immunol 185 2010 5704 5713
38. J.J. O'Shea, M. Gadina, and Y. Kanno Cytokine signaling: birth of a pathway J Immunol 187 2011 5475 5478
39. S. Dupuis, C. Dargemont, C. Fieschi, N. Thomassin, S. Rosenzweig, and J. Harris Impairment of mycobacterial but not viral immunity by a germline human STAT1 mutation Science 293 2001 300 303
40. S. Dupuis, E. Jouanguy, S. Al-Hajjar, C. Fieschi, I.Z. Al-Mohsen, and S. Al-Jumaah Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency Nat Genet 33 2003 388 391
41. L.L. Elo, H. Jarvenpaa, S. Tuomela, S. Raghav, H. Ahlfors, and K. Laurila Genome-wide profiling of interleukin-4 and STAT6 transcription factor regulation of human Th2 cell programming Immunity 32 2010 852 862
42. M. Kraft, G.H. Cassell, J.E. Henson, H. Watson, J. Williamson, and B.P. Marmion Detection of Mycoplasma pneumoniae in the airways of adults with chronic asthma Am J Respir Crit Care Med 158 1998 998 1001
43. D.E. Dulek, and R.S. Peebles Jr. Viruses and asthma Biochim Biophys Acta 1810 2011 1080 1090
44. R.S. Peebles Jr., and T.V. Hartert Respiratory viruses and asthma Curr Opin Pulm Med 6 2000 10 14
45. M. Kubo, T. Hanada, and A. Yoshimura Suppressors of cytokine signaling and immunity Nat Immunol 4 2003 1169 1176
46. J. Schmitz, M. Weissenbach, S. Haan, P.C. Heinrich, and F. Schaper SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130 J Biol Chem 275 2000 12848 12856
47. S.J. Cohney, D. Sanden, N.A. Cacalano, A. Yoshimura, A. Mui, and T.S. Migone SOCS-3 is tyrosine phosphorylated in response to interleukin-2 and suppresses STAT5 phosphorylation and lymphocyte proliferation Mol Cell Biol 19 1999 4980 4988
48. B.A. Croker, D.L. Krebs, J.G. Zhang, S. Wormald, T.A. Willson, and E.G. Stanley SOCS3 negatively regulates IL-6 signaling in vivo Nat Immunol 4 2003 540 545
49. S. Canfield, Y. Lee, A. Schroder, and P. Rothman Cutting edge: IL-4 induces suppressor of cytokine signaling-3 expression in B cells by a mechanism dependent on activation of p38 MAPK J Immunol 174 2005 2494 2498
50. Y. Seki, H. Inoue, N. Nagata, K. Hayashi, S. Fukuyama, and K. Matsumoto SOCS-3 regulates onset and maintenance of T(H)2-mediated allergic responses Nat Med 9 2003 1047 1054
51. Y. Zhuang, Z. Huang, J. Nishida, M. Brown, L. Zhang, and H. Huang A continuous T-bet expression is required to silence the interleukin-4-producing potential in T helper type 1 cells Immunology 128 2009 34 42
52. X. Qi, J. Nishida, L. Chaves, K. Ohmori, and H. Huang CCAAT/enhancer-binding protein alpha (C/EBPalpha) is critical for interleukin-4 expression in response to FcepsilonRI receptor cross-linking J Biol Chem 286 2011 16063 16073
53. Z. Huang, J. Xin, J. Coleman, and H. Huang IFN-gamma suppresses STAT6 phosphorylation by inhibiting its recruitment to the IL-4 receptor J Immunol 174 2005 1332 1337