SOCS1 is essential for regulatory T cell functions by preventing loss of Foxp3 expression as well as IFN-γ and IL-17A production

Journal of Experimental Medicine

Volumn 208, Issue 10, 2011, Pages 2055-2067

  Takahashi, Reiko ^a,b   Nishimoto, Shuhei ^a   Muto, Go ^a   Sekiya, Takashi ^a   Tamiya, Taiga ^a   Kimura, Akihiro ^a   Morita, Rimpei ^a   Asakawa, Mayako ^a   Chinen, Takatoshi ^a   Yoshimura, Akihiko ^a,b  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 2 RECEPTOR ALPHA; L SELECTIN; STAT1 PROTEIN; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; TRANSCRIPTION FACTOR FOXP3; TUBULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEMETHYLATION; ENHANCER REGION; GENE; HOMEOSTASIS; IMMUNOMODULATION; IN VITRO STUDY; INFLAMMATION; INTERFERON GAMMA GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAG2 GENE; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SOCS1 GENE; TH1 CELL; TH17 CELL;

ANIMALS; AUTOIMMUNITY; CELL DIFFERENTIATION; CYTOKINES; DNA-BINDING PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; INTERFERON-GAMMA; INTERLEUKIN-17; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; SKIN; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY;

EID: 80555154007     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20110428     Document Type: Article

References (47)

1. Belkaid, Y., and K. Tarbell. 2009. Regulatory T cells in the control of hostmicroorganism interactions. Annu. Rev. Immunol. 27:551-589. http://dx.doi.org/10.1146/annurev.immunol.021908.132723
2. Bennett, C.L., and H.D. Ochs. 2001. IPEX is a unique X-linked syndrome characterized by immune dysfunction, polyendocrinopathy, enteropathy, and a variety of autoimmune phenomena. Curr. Opin. Pediatr. 13:533- 538. http://dx.doi.org/10.1097/00008480-200112000-00007
3. Bennett, C.L., J. Christie, F. Ramsdell, M.E. Brunkow, P.J. Ferguson, L. Whitesell, T.E. Kelly, F.T. Saulsbury, P.F. Chance, and H.D. Ochs. 2001. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat. Genet. 27:20- 21. http://dx.doi.org/10.1038/83713
4. Brunkow, M.E., E.W. Jeffery, K.A. Hjerrild, B. Paeper, L.B. Clark, S.A. Yasayko, J.E. Wilkinson, D. Galas, S.F. Ziegler, and F. Ramsdell. 2001. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27:68-73. http://dx.doi.org/10.1038/83784
5. Chan, H.C., L.Y. Ke, L.L. Chang, C.C. Liu, Y.H. Hung, C.H. Lin, R.N. Li, W.C. Tsai, H.W. Liu, and J.H. Yen. 2010. Suppressor of cytokine signaling 1 gene expression and polymorphisms in systemic lupus erythematosus. Lupus. 19:696-702. http://dx.doi.org/10.1177/0961203309357437
6. + regulatory T cells control TH17 responses in a Stat3-dependent manner. Science. 326:986-991. http://dx.doi.org/10.1126/science.1172702
7. Durant, L., W.T. Watford, H.L. Ramos, A. Laurence, G. Vahedi, L. Wei, H. Takahashi, H.W. Sun, Y. Kanno, F. Powrie, and J.J. O'Shea. 2010. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity. 32:605-615. http://dx.doi.org/10.1016/j.immuni.2010.05.003
8. Floess, S., J. Freyer, C. Siewert, U. Baron, S. Olek, J. Polansky, K. Schlawe, H.D. Chang, T. Bopp, E. Schmitt, et al. 2007. Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol. 5:e38. http://dx.doi.org/10.1371/journal.pbio.0050038
9. Fontenot, J.D., J.P. Rasmussen, L.M. Williams, J.L. Dooley, A.G. Farr, and A.Y. Rudensky. 2005. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity. 22:329-341. http://dx.doi.org/10.1016/j.immuni.2005.01.016
10. Hanada, T., H. Yoshida, S. Kato, K. Tanaka, K. Masutani, J. Tsukada, Y. Nomura, H. Mimata, M. Kubo, and A. Yoshimura. 2003. Suppressor of cytokine signaling-1 is essential for suppressing dendritic cell activation and systemic autoimmunity. Immunity. 19:437-450. http://dx.doi.org/10.1016/S1074-7613(03)00240-1
11. Hori, S. 2010. c-Rel: a pioneer in directing regulatory T-cell lineage commitment? Eur. J. Immunol. 40:664-667. http://dx.doi.org/10.1002/eji.201040372
12. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science. 299:1057-1061. http://dx.doi.org/10.1126/science.1079490
13. Inagaki-Ohara, K., T. Chinen, G. Matsuzaki, A. Sasaki, Y. Sakamoto, K. Hiromatsu, F. Nakamura-Uchiyama, Y. Nawa, and A. Yoshimura. 2004. Mucosal T cells bearing TCRgammadelta play a protective role in intestinal inflammation. J. Immunol. 173:1390-1398.
14. Isomäki, P., T. Alanärä, P. Isohanni, A. Lagerstedt, M. Korpela, T. Moilanen, T. Visakorpi, and O. Silvennoinen. 2007. The expression of SOCS is altered in rheumatoid arthritis. Rheumatology (Oxford). 46:1538-1546. http://dx.doi.org/10.1093/rheumatology/kem198
15. Kim, H.P., and W.J. Leonard. 2007. CREB/ATF-dependent T cell receptorinduced FoxP3 gene expression: a role for DNA methylation. J. Exp. Med. 204:1543-1551.
16. + regulatory T cells. Immunity. 31:609-620. http://dx.doi.org/10.1016/j.immuni.2009.09.003
17. Koch, M.A., G. Tucker-Heard, N.R. Perdue, J.R. Killebrew, K.B. Urdahl, and D.J. Campbell. 2009. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10:595-602. http://dx.doi.org/10.1038/ni.1731
18. + T cells: a committed regulatory T-cell lineage and an uncommitted minor population retaining plasticity. Proc. Natl. Acad. Sci. USA. 106:1903-1908. http://dx.doi.org/10.1073/pnas.0811556106
19. Lu, L.F., T.H. Thai, D.P. Calado, A. Chaudhry, M. Kubo, K. Tanaka, G.B. Loeb, H. Lee, A. Yoshimura, K. Rajewsky, and A.Y. Rudensky. 2009. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity. 30:80-91. http://dx.doi.org/10.1016/j.immuni.2008.11.010
20. Lu, L.F., M.P. Boldin, A. Chaudhry, L.L. Lin, K.D. Taganov, T. Hanada, A. Yoshimura, D. Baltimore, and A.Y. Rudensky. 2010. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell. 142:914-929. http://dx.doi.org/10.1016/j.cell.2010.08.012
21. R cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197:111-119. http://dx.doi.org/10.1084/jem.20021345
22. Murai, M., P. Krause, H. Cheroutre, and M. Kronenberg. 2010. Regulatory T-cell stability and plasticity in mucosal and systemic immune systems. Mucosal Immunol. 3:443-449. http://dx.doi.org/10.1038/mi.2010.27
23. Nakae, S., Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, I. Homma, K. Sekikawa, M. Asano, and Y. Iwakura. 2002. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity. 17:375-387. http://dx.doi.org/10.1016/S1074-7613(02)00391-6
24. + Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity. 31:772-786. http://dx.doi.org/10.1016/j.immuni.2009.10.001
25. + natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl. Acad. Sci. USA. 105:10113-10118. http://dx.doi.org/10.1073/pnas.0711106105
26. Rubtsov, Y.P., R.E. Niec, S. Josefowicz, L. Li, J. Darce, D. Mathis, C. Benoist, and A.Y. Rudensky. 2010. Stability of the regulatory T cell lineage in vivo. Science. 329:1667-1671. http://dx.doi.org/10.1126/science.1191996
27. Rudra, D., T. Egawa, M.M. Chong, P. Treuting, D.R. Littman, and A.Y. Rudensky. 2009. Runx-CBFbeta complexes control expression of the transcription factor Foxp3 in regulatory T cells. Nat. Immunol. 10:1170- 1177. http://dx.doi.org/10.1038/ni.1795
28. + regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22:531-562. http://dx.doi.org/10.1146/annurev.immunol.21.120601.141122
29. Sakaguchi, S., T. Yamaguchi, T. Nomura, and M. Ono. 2008. Regulatory T cells and immune tolerance. Cell. 133:775-787. http://dx.doi.org/10.1016/j.cell.2008.05.009
30. Scalapino, K.J., and D.I. Daikh. 2009. Suppression of glomerulonephritis in NZB/NZW lupus prone mice by adoptive transfer of ex vivo expanded regulatory T cells. PLoS ONE. 4:e6031. http://dx.doi.org/10.1371/journal.pone.0006031
31. Sharabi, A., Z.M. Sthoeger, K. Mahlab, S. Lapter, H. Zinger, and E. Mozes. 2009. A tolerogenic peptide that induces suppressor of cytokine signaling (SOCS)-1 restores the aberrant control of IFN-gamma signaling in lupus-affected (NZB x NZW)F1 mice. Clin. Immunol. 133:61-68. http://dx.doi.org/10.1016/j.clim.2009.06.010
32. Smith, E., M.A. Stark, A. Zarbock, T.L. Burcin, A.C. Bruce, D. Vaswani, P. Foley, and K. Ley. 2008. IL-17A inhibits the expansion of IL-17A-producing T cells in mice through "short-loop" inhibition via IL-17 receptor. J. Immunol. 181:1357-1364.
33. Sutton, C.E., S.J. Lalor, C.M. Sweeney, C.F. Brereton, E.C. Lavelle, and K.H. Mills. 2009. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity. 31:331-341. http://dx.doi.org/10.1016/j.immuni.2009.08.001
34. Suzue, K., T. Asai, T. Takeuchi, and S. Koyasu. 2003. In vivo role of IFNgamma produced by antigen-presenting cells in early host defense against intracellular pathogens. Eur. J. Immunol. 33:2666-2675. http://dx.doi.org/10.1002/eji.200323292
35. Takimoto, T., Y. Wakabayashi, T. Sekiya, N. Inoue, R. Morita, K. Ichiyama, R. Takahashi, M. Asakawa, G. Muto, T. Mori, et al. 2010. Smad2 and Smad3 are redundantly essential for the TGF-beta-mediated regulation of regulatory T plasticity and Th1 development. J. Immunol. 185:842-855. http://dx.doi.org/10.4049/jimmunol.0904100
36. Tanaka, K., K. Ichiyama, M. Hashimoto, H. Yoshida, T. Takimoto, G. Takaesu, T. Torisu, T. Hanada, H. Yasukawa, S. Fukuyama, et al. 2008. Loss of suppressor of cytokine signaling 1 in helper T cells leads to defective Th17 differentiation by enhancing antagonistic effects of IFN-gamma on STAT3 and Smads. J. Immunol. 180:3746-3756.
37. Tang, Q., J.Y. Adams, C. Penaranda, K. Melli, E. Piaggio, E. Sgouroudis, C.A. Piccirillo, B.L. Salomon, and J.A. Bluestone. 2008. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity. 28:687-697. http://dx.doi.org/10.1016/j.immuni.2008.03.016
38. + T cells in gut Peyer's patches. Science. 323:1488- 1492. http://dx.doi.org/10.1126/science.1169152
39. Wan, Y.Y., and R.A. Flavell. 2007. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature. 445:766- 770. http://dx.doi.org/10.1038/nature05479
40. + regulatory T cells. J. Immunol. 180:1565-1575.
41. + regulatory T cell function. Science. 322:271-275. http://dx.doi.org/10.1126/science.1160062
42. Yang, X.O., R. Nurieva, G.J. Martinez, H.S. Kang, Y. Chung, B.P. Pappu, B. Shah, S.H. Chang, K.S. Schluns, S.S. Watowich, et al. 2008. Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity. 29:44-56. http://dx.doi.org/10.1016/j.immuni.2008.05.007
43. Yao, Z., Y. Kanno, M. Kerenyi, G. Stephens, L. Durant, W.T. Watford, A. Laurence, G.W. Robinson, E.M. Shevach, R. Moriggl, et al. 2007. Nonredundant roles for Stat5a/b in directly regulating Foxp3. Blood. 109:4368-4375. http://dx.doi.org/10.1182/blood-2006-11-055756
44. Yoshimura, A., T. Naka, and M. Kubo. 2007. SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 7:454-465. http://dx.doi.org/10.1038/nri2093
45. Zhan, Y., G.M. Davey, K.L. Graham, H. Kiu, N.L. Dudek, T.W. Kay, and A.M. Lew. 2009. SOCS1 negatively regulates the production of Foxp3+ CD4+ T cells in the thymus. Immunol. Cell Biol. 87:473-480. http://dx.doi.org/10.1038/icb.2009.23
46. Zheng, Y., S. Josefowicz, A. Chaudhry, X.P. Peng, K. Forbush, and A.Y. Rudensky. 2010. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature. 463:808-812. http://dx.doi.org/10.1038/nature08750
47. Zhou, X., S.L. Bailey-Bucktrout, L.T. Jeker, C. Penaranda, M. Martínez-Llordella, M. Ashby, M. Nakayama, W. Rosenthal, and J.A. Bluestone. 2009. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat. Immunol. 10:1000-1007. http://dx.doi.org/10.1038/ni.1774