Aiolos promotes T H17 differentiation by directly silencing Il2 expression

Nature Immunology

Volumn 13, Issue 8, 2012, Pages 770-777

  Quintana, Francisco J ^a   Jin, Hulin ^a   Burns, Evan J ^a   Nadeau, Meghan ^a   Yeste, Ada ^a   Kumar, Deepak ^a   Rangachari, Manu ^a   Zhu, Chen ^a   Xiao, Sheng ^a   Seavitt, John ^b   Georgopoulos, Katia ^b   Kuchroo, Vijay K ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2; STAT3 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AIOLOS; UNCLASSIFIED DRUG; AHR PROTEIN, MOUSE; AROMATIC HYDROCARBON RECEPTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GAMMA INTERFERON; IKZF3 PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TH17 CELL; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; COLITIS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELLS, CULTURED; COLITIS; GENE EXPRESSION REGULATION; INTERFERON-GAMMA; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, ARYL HYDROCARBON; STAT3 TRANSCRIPTION FACTOR; TH17 CELLS; TRANS-ACTIVATORS;

EID: 84864146433     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2363     Document Type: Article

References (45)

1. Korn, T., Bettelli, E., Oukka, M. & Kuchroo, V.K. IL-17 and Th17 cells. Annu. Rev. Immunol. 27, 485-517 (2009).
2. Bettelli, E. et al. Reciprocal developmental pathways for the generation of pathogenic effector th17 and regulatory T cells. Nature 441, 235-238 (2006).
3. Korn, T. et al. IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells. Nature 448, 484-487 (2007). (Pubitemid 47123515)
4. Yang, X.O. et al. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 282, 9358-9363 (2007). (Pubitemid 47104613)
5. McGeachy, M.J. et al. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 10, 314-324 (2009).
6. + T helper cells. Cell 126, 1121-1133 (2006). (Pubitemid 44380299)
7. Yang, X.O. et al. T helper 17 lineage differentiation is programmed by orphan nuclear receptors RORα and RORγ. Immunity 28, 29-39 (2008).
8. Kimura, A., Naka, T., Nohara, K., Fujii-Kuriyama, Y. & Kishimoto, T. Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc. Natl. Acad. Sci. USA 105, 9721-9726 (2008). (Pubitemid 352031367)
9. Quintana, F.J. et al. Control of Treg and TH17 cell differentiation by the aryl hydrocarbon receptor. Nature 453, 65-71 (2008). (Pubitemid 351630328)
10. Veldhoen, M. et al. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453, 106-109 (2008). (Pubitemid 351630329)
11. + regulatory T cells promote T helper 17 cell development in vivo through regulation of interleukin-2. Immunity 34, 409-421 (2011).
12. Laurence, A. et al. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26, 371-381 (2007). (Pubitemid 46413906)
13. Liao, W., Lin, J.X., Wang, L., Li, P. & Leonard, W.J. Modulation of cytokine receptors by IL-2 broadly regulates differentiation into helper T cell lineages. Nat. Immunol. 12, 551-559 (2011).
14. + regulatory T cells promote Th17 cells in vitro and enhance host resistance in mouse Candida albicans Th17 cell infection model. Immunity 34, 422-434 (2011).
15. Yang, X.P. et al. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat. Immunol. 12, 247-254 (2011).
16. Georgopoulos, K. Haematopoietic cell-fate decisions, chromatin regulation and ikaros. Nat. Rev. Immunol. 2, 162-174 (2002). (Pubitemid 37328763)
17. + regulatory T cells. Nat. Immunol. 11, 846-853 (2010).
18. + regulatory T cells. Science 325, 1142-1146 (2009).
19. + T regulatory cells. J. Immunol. 184, 3433-3441 (2010).
20. + T cells. J. immunol. 183, 5518-5525 (2009).
21. Wang, J.H. et al. Aiolos regulates B cell activation and maturation to effector state. Immunity 9, 543-553 (1998).
22. Bandyopadhyay, S. et al. Interleukin 2 gene transcription is regulated by Ikaros-induced changes in histone acetylation in anergic T cells. Blood 109, 2878-2886 (2007). (Pubitemid 46482084)
23. Depper, J.M. et al. Interleukin 2 (IL-2) augments transcription of the IL-2 receptor gene. Proc. Natl. Acad. Sci. USA 82, 4230-4234 (1985). (Pubitemid 15053616)
24. Kimura, A., Naka, T. & Kishimoto, T. IL-6-dependent and-independent pathways in the development of interleukin 17-producing T helper cells. Proc. Natl. Acad. Sci. USA 104, 12099-12104 (2007). (Pubitemid 47185636)
25. Villarino, A.V., Gallo, E. & Abbas, A.K. STAT1-activating cytokines limit Th17 responses through both T-bet-dependent and-independent mechanisms. J. immunol. 185, 6461-6471 (2010).
26. + T lymphocytes. J. Immunol. 179, 7305-7315 (2007).
27. Koipally, J., Renold, A., Kim, J. & Georgopoulos, K. Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. EMBO J. 18, 3090-3100 (1999). (Pubitemid 29255617)
28. Durant, L. et al. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 32, 605-615 (2010).
29. Wei, L., Laurence, A., Elias, K.M. & O'Shea, J.J. IL-21 is produced by Th17 cells and drives IL-17 production in a STAT3-dependent manner. J. Biol. Chem. 282, 34605-34610 (2007). (Pubitemid 350232469)
30. Wei, L. et al. Discrete roles of STAT4 and STAT6 transcription factors in tuning epigenetic modifications and transcription during T helper cell differentiation. Immunity 32, 840-851 (2010).
31. Quintana, F.J. et al. Antigen microarrays identify unique serum autoantibody signatures in clinical and pathologic subtypes of multiple sclerosis. Proc. Natl. Acad. Sci. USA 105, 18889-18894 (2008).
32. + T cell memory by promoting the generation of IL-7Rα-expressing cells. J. Exp. Med. 204, 547-557 (2007). (Pubitemid 46457078)
33. Kühn, R., Lohler, J., Rennick, D., Rajewsky, K. & Muller, W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274 (1993). (Pubitemid 23320290)
34. Ivanov, I.I. et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498 (2009).
35. O'Connor, W. Jr. et al. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat. Immunol. 10, 603-609 (2009).
36. + IL-7Rα high memory T cells in chronic colitis. Eur. J. Immunol. 40, 2423-2436 (2010).
37. Cox, J.H. et al. IL-27 promotes T cell-dependent colitis through multiple mechanisms. J. Exp. Med. 208, 115-123 (2011).
38. Villarino, A.V. et al. Helper T cell IL-2 production is limited by negative feedback and STAT-dependent cytokine signals. J. Exp. Med. 204, 65-71 (2007). (Pubitemid 46148757)
39. Oh, H.-M. et al. STAT3 promotes T cell survival and inhibits IL-2 production through up-regulation of class O forkhead transcription factors. J. Biol. Chem. 286, 30888-30897 (2011).
40. Yamanouchi, J. et al. Interleukin-2 gene variation impairs regulatory T cell function and causes autoimmunity. Nat. Genet. 39, 329-337 (2007). (Pubitemid 46328484)
41. Liu, S.M. et al. Differential IL-21 signaling in APCs leads to disparate Th17 differentiation in diabetes-susceptible NOD and diabetes-resistant NOD.Idd3 mice. J. Clin. Invest. 121, 4303-4310 (2011).
42. 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). (Pubitemid 41541792)
43. Wilson, C.B., Rowell, E. & Sekimata, M. Epigenetic control of T-helper-cell differentiation. Nat. Rev. Immunol. 9, 91-105 (2009).
44. Jeon, M.S. & Esser, C. The murine IL-2 promoter contains distal regulatory elements responsive to the Ah receptor, a member of the evolutionarily conserved bHLH-PAS transcription factor family. J. Immunol. 165, 6975-6983 (2000). (Pubitemid 32001169)
45. Apetoh, L. et al. The aryl hydrocarbon receptor interacts with c-maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat. Immunol. 11, 854-861 (2010).