Genome-wide regulatory analysis reveals that T-bet controls Th17 lineage differentiation through direct suppression of IRF4

Journal of Immunology

Volumn 191, Issue 12, 2013, Pages 5925-5932

  Gökmen, M Refik ^a,c   Dong, Rong ^a   Kanhere, Aditi ^b,c   Powell, Nick ^a   Perucha, Esperanza ^a   Jackson, Ian ^a   Howard, Jane K ^a   Hernandez Fuentes, Maria ^a   Jenner, Richard G ^b   Lord, Graham M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 17; TRANSCRIPTION FACTOR T BET;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CD4+ T LYMPHOCYTE; CELL LINEAGE; CELL MIGRATION; CELL TRANSFER; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE CONTROL; GENE EXPRESSION; IRF4 GENE; LYMPHOCYTE DIFFERENTIATION; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; STOP CODON; TBX21 GENE; TH17 CELL; TRANSCRIPTION REGULATION; VIRAL GENE DELIVERY SYSTEM;

EID: 84890418697     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202254     Document Type: Article

References (39)

1. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
2. Lord, G. M., R. M. Rao, H. Choe, B. M. Sullivan, A. H. Lichtman, F. W. Luscinskas, and L. H. Glimcher. 2005. T-bet is required for optimal proinflammatory CD4+ T-cell trafficking. Blood 106: 3432-3439.
3. Djuretic, I. M., D. Levanon, V. Negreanu, Y. Groner, A. Rao, and K. M. Ansel. 2007. Transcription factors T-bet and Runx3 cooperate to activate Ifng and silence Il4 in T helper type 1 cells. Nat. Immunol. 8: 145-153.
4. Hwang, E. S., S. J. Szabo, P. L. Schwartzberg, and L. H. Glimcher. 2005. T helper cell fate specified by kinase-mediated interaction of T-bet with GATA-3. Science 307: 430-433.
5. Annunziato, F., L. Cosmi, V. Santarlasci, L. Maggi, F. Liotta, B. Mazzinghi, E. Parente, L. Filì, S. Ferri, F. Frosali, et al. 2007. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204: 1849-1861.
6. Shi, G., C. A. Cox, B. P. Vistica, C. Tan, E. F. Wawrousek, and I. Gery. 2008. Phenotype switching by inflammation-inducing polarized Th17 cells, but not by Th1 cells. J. Immunol. 181: 7205-7213.
7. Ghoreschi, K., A. Laurence, X.-P. Yang, C. M. Tato, M. J. McGeachy, J. E. Konkel, H. L. Ramos, L. Wei, T. S. Davidson, N. Bouladoux, et al. 2010. Generation of pathogenic T(H)17 cells in the absence of TGF-β signalling. Nature 467: 967-971.
8. Zielinski, C. E., F. Mele, D. Aschenbrenner, D. Jarrossay, F. Ronchi, M. Gattorno, S. Monticelli, A. Lanzavecchia, and F. Sallusto. 2012. Pathogen-induced human TH17 cells produce IFN-g or IL-10 and are regulated by IL-1β. Nature 484: 514-518.
9. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259: 1739-1742.
10. Durrant, D. M., S. L. Gaffen, E. P. Riesenfeld, C. G. Irvin, and D. W. Metzger. 2009. Development of allergen-induced airway inflammation in the absence of T-bet regulation is dependent on IL-17. J. Immunol. 183: 5293-5300.
11. Fujiwara, M., K. Hirose, S.-I. Kagami, H. Takatori, H. Wakashin, T. Tamachi, N. Watanabe, Y. Saito, I. Iwamoto, and H. Nakajima. 2007. T-bet inhibits both TH2 cell-mediated eosinophil recruitment and TH17 cell-mediated neutrophil recruitment into the airways. J. Allergy Clin. Immunol. 119: 662-670.
12. Lazarevic, V., X. Chen, J.-H. Shim, E. S. Hwang, E. Jang, A. N. Bolm, M. Oukka, V. K. Kuchroo, and L. H. Glimcher. 2011. T-bet represses T(H)17 differentiation by preventing Runx1-mediated activation of the gene encoding RORγt. Nat. Immunol. 12: 96-104.
13. Mathur, A. N., H. C. Chang, D. G. Zisoulis, R. Kapur, M. L. Belladonna, G. S. Kansas, and M. H. Kaplan. 2006. T-bet is a critical determinant in the instability of the IL-17-secreting T-helper phenotype. Blood 108: 1595-1601.
14. Rangachari, M., N. Mauermann, R. R. Marty, S. Dirnhofer, M. O. Kurrer, V. Komnenovic, J. M. Penninger, and U. Eriksson. 2006. T-bet negatively regulates autoimmune myocarditis by suppressing local production of interleukin 17. J. Exp. Med. 203: 2009-2019.
15. Villarino, A. V., E. Gallo, and A. K. Abbas. 2010. STAT1-activating cytokines limit Th17 responses through both T-bet-dependent and -independent mechanisms. J. Immunol. 185: 6461-6471.
16. Zhang, Y., T. Liu, C. A. Meyer, J. Eeckhoute, D. S. Johnson, B. E. Bernstein, C. Nussbaum, R. M. Myers, M. Brown, W. Li, and X. S. Liu. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9: R137.1-R137.9
17. Kanhere, A., A. Hertweck, U. Bhatia, M. R. Gökmen, E. Perucha, I. Jackson, G. M. Lord, and R. G. Jenner. 2012. T-bet and GATA3 orchestrate Th1 and Th2 differentiation through lineage-specific targeting of distal regulatory elements. Nat Commun 3: 1268.
18. Jenner, R. G., M. J. Townsend, I. Jackson, K. Sun, R. D. Bouwman, R. A. Young, L. H. Glimcher, and G. M. Lord. 2009. The transcription factors T-bet and GATA-3 control alternative pathways of T-cell differentiation through a shared set of target genes. Proc. Natl. Acad. Sci. USA 106: 17876-17881.
19. Brüstle, A., S. Heink, M. Huber, C. Rosenplänter, C. Stadelmann, P. Yu, E. Arpaia, T. W. Mak, T. Kamradt, and M. Lohoff. 2007. The development of inflammatory T(H)-17 cells requires interferon-regulatory factor 4. Nat. Immunol. 8: 958-966.
20. Huber, M., A. Brüstle, K. Reinhard, A. Guralnik, G. Walter, A. Mahiny, E. von Löw, and M. Lohoff. 2008. IRF4 is essential for IL-21-mediated induction, amplification, and stabilization of the Th17 phenotype. Proc. Natl. Acad. Sci. USA 105: 20846-20851.
21. Wei, G., L. Wei, J. Zhu, C. Zang, J. Hu-Li, Z. Yao, K. Cui, Y. Kanno, T.-Y. Roh, W. T. Watford, et al. 2009. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30: 155-167.
22. Schmidt, D., M. D. Wilson, B. Ballester, P. C. Schwalie, G. D. Brown, A. Marshall, C. Kutter, S. Watt, C. P. Martinez-Jimenez, S. Mackay, et al. 2010. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328: 1036-1040.
23. Oestreich, K. J., and A. S. Weinmann. 2012. T-bet employs diverse regulatory mechanisms to repress transcription. Trends Immunol. 33: 78-83.
24. Neurath, M. F., B. Weigmann, S. Finotto, J. Glickman, E. Nieuwenhuis, H. Iijima, A. Mizoguchi, E. Mizoguchi, J. Mudter, P. R. Galle, et al. 2002. The transcription factor T-bet regulates mucosal T cell activation in experimental colitis and Crohn's disease. J. Exp. Med. 195: 1129-1143.
25. Powrie, F., M. W. Leach, S. Mauze, S. Menon, L. B. Caddle, and R. L. Coffman. 1994. Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. Immunity 1: 553-562.
26. Harrington, L. E., R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132.
27. Park, H., Z. Li, X. O.Yang, S.H. Chang, R. Nurieva, Y.-H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. Adistinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141.
28. Matsuda, J. L., T. C. George, J. Hagman, and L. Gapin. 2007. Temporal dissection of T-bet functions. J. Immunol. 178: 3457-3465.
29. Wu, H.-J., I. I. Ivanov, J. Darce, K. Hattori, T. Shima, Y. Umesaki, D. R. Littman, C. Benoist, and D. Mathis. 2010. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32: 815-827.
30. Oestreich, K. J., and A. S. Weinmann. 2012. Master regulators or lineage-specifying? Changing views on CD4+ T cell transcription factors. Nat. Rev. Immunol. 12: 799-804.
31. Oestreich, K. J., A. C. Huang, and A. S. Weinmann. 2011. The lineage-defining factors T-bet and Bcl-6 collaborate to regulate Th1 gene expression patterns. J. Exp. Med. 208: 1001-1013.
32. Ciofani, M., A. Madar, C. Galan, M. Sellars, K. Mace, F. Pauli, A. Agarwal, W. Huang, C. N. Parkurst, M. Muratet, et al. 2012. A validated regulatory network for Th17 cell specification. Cell 151: 289-303.
33. Mudter, J., J. Yu, C. Zufferey, A. Brüstle, S. Wirtz, B. Weigmann, A. Hoffman, M. Schenk, P. R. Galle, H. A. Lehr, et al. 2011. IRF4 regulates IL-17A promoter activity and controls RORγt-dependent Th17 colitis in vivo. Inflamm. Bowel Dis. 17: 1343-1358.
34. Powell, N., J. B. Canavan, T. T. MacDonald, and G. M. Lord. 2010. Transcriptional regulation of the mucosal immune system mediated by T-bet. Mucosal Immunol. 3: 567-577.
35. Lohoff, M., H. W. Mittrücker, S. Prechtl, S. Bischof, F. Sommer, S. Kock, D. A. Ferrick, G. S. Duncan, A. Gessner, and T. W. Mak. 2002. Dysregulated T helper cell differentiation in the absence of interferon regulatory factor 4. Proc. Natl. Acad. Sci. USA 99: 11808-11812.
36. Tominaga, N., K. Ohkusu-Tsukada, H. Udono, R. Abe, T. Matsuyama, and K. Yui. 2003. Development of Th1 and not Th2 immune responses in mice lacking IFN-regulatory factor-4. Int. Immunol. 15: 1-10.
37. Staudt, V., E. Bothur, M. Klein, K. Lingnau, S. Reuter, N. Grebe, B. Gerlitzki, M. Hoffmann, A. Ulges, C. Taube, et al. 2010. Interferon-regulatory factor 4 is essential for the developmental program of T helper 9 cells. Immunity 33: 192-202.
38. Goswami, R., R. Jabeen, R. Yagi, D. Pham, J. Zhu, S. Goenka, and M. H. Kaplan. 2012. STAT6-dependent regulation of Th9 development. J. Immunol. 188: 968-975.
39. Zheng, Y., A. Chaudhry, A. Kas, P. deRoos, J. M. Kim, T.-T. Chu, L. Corcoran, P. Treuting, U. Klein, and A. Y. Rudensky. 2009. Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature 458: 351-356.