Gfi1 negatively regulates Th17 differentiation by inhibiting RORγt activity

International Immunology

Volumn 21, Issue 7, 2009, Pages 881-889

  Ichiyama, Kenji ^a   Hashimoto, Masayuki ^a   Sekiya, Takashi ^a   Nakagawa, Ryusuke ^a   Wakabayashi, Yu ^a,c   Sugiyama, Yuki ^a,c   Komai, Kyoko ^a   Saba, Ingrid ^b   Möröy, Tarik ^b   Yoshimura, Akihiko ^a,c  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

IL; Smad; STAT; Transcription factor

Indexed keywords

CELL NUCLEUS RECEPTOR; GAMMA INTERFERON; GENE PRODUCT; GROWTH FACTOR INDEPENDENT 1; INTERLEUKIN 17; INTERLEUKIN 4; RETINOID RELATED ORPHAN RECEPTOR GAMMA T; STAT1 PROTEIN; STAT6 PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRAIN; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; TRANSCRIPTION REGULATION; UPREGULATION; WILD TYPE;

EID: 67649857192     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxp054     Document Type: Article

References (48)

1. Mosmann, T. R. and Coffman, R. L. 1989. TH1 and TH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7:145.
2. Murphy, K. M. and Reiner, S. L. 2002. The lineage decisions of helper T cells. Nat. Rev. Immunol. 2:933.
3. Flavell, R. A. 1999. The molecular basis of T cell differentiation. Immunol. Res. 19:159.
4. Abbas, A. K., Murphy, K. M. and Sher, A. 1996. Functional diversity of helper T lymphocytes. Nature 383:787.
5. Kottke, T., Sanchez-Perez, L., Diaz, R. M. et al. 2007. Induction of hsp70-mediated Th17 autoimmunity can be exploited as immunotherapy for metastatic prostate cancer. Cancer Res. 67:11970.
6. Aujla, S. J., Dubin, P. J. and Kolls, J. K. 2007. Th17 cells and mucosal host defense. Semin. Immunol. 19:377.
7. Kikly, K., Liu, L., Na, S. and Sedgwick, J. D. 2006. The IL-23/Th(17) axis: Therapeutic targets for autoimmune inflammation. Curr. Opin. Immunol. 18:670.
8. Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M. and Stockinger, B. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24:179.
9. Mangan, P. R., Harrington, L. E., O'Quinn, D. B. et al. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441:231.
10. Bettelli, E., Carrier, Y., Gao, W. et al. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441:235.
11. Korn, T., Bettelli, E., Gao, W. et al. 2007. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448:484.
12. Nurieva, R., Yang, X. O., Martinez, G. et al. 2007. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448:480.
13. McKenzie, B. S., Kastelein, R. A. and Cua, D. J. 2006. Understanding the IL-23-IL-17 immune pathway. Trends Immunol. 27:17.
14. Ivanov, I. I., McKenzie, B. S., Zhou, L. et al. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126:1121.
15. Ichiyama, K., Yoshida, H., Wakabayashi, Y. et al. 2008. Foxp3 inhibits RORgammat-mediated IL-17A mRNA transcription through direct interaction with RORgammat. J. Biol. Chem. 283:17003.
16. Hori, S. and Sakaguchi, S. 2004. Foxp3: A critical regulator of the development and function of regulatory T cells. Microbes Infect. 6:745.
17. Chen, W., Jin, W., Hardegen, N. et al. 2003. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198:1875.
18. You, S., Leforban, B., Garcia, C., Bach, J. F., Bluestone, J. A. and Chatenoud, L. 2007. Adaptive TGF-beta-dependent regulatory T cells control autoimmune diabetes and are a privileged target of anti-CD3 antibody treatment. Proc. Natl Acad. Sci. USA 104:6335.
19. Wei, J., Duramad, O., Perng, O. A., Reiner, S. L., Liu, Y. J. and Qin, F. X. 2007. Antagonistic nature of T helper 1/2 developmental programs in opposing peripheral induction of Foxp3+ regulatory T cells. Proc. Natl Acad. Sci. USA 104:18169.
20. Davidson, T. S., DiPaolo, R. J., Andersson, J. and Shevach, E. M. 2007. Cutting Edge: IL-2 is essential for TGF-beta-mediated induction of Foxp3+ T regulatory cells. J. Immunol. 178:4022.
21. Yao, Z., Kanno, Y., Kerenyi, M. et al. 2007. Nonredundant roles for Stat5a/b in directly regulating Foxp3. Blood 109:4368.
22. Takaki, H., Ichiyama, K., Koga, K. et al. 2008. STAT6 Inhibits TGF-beta1-mediated Foxp3 induction through direct binding to the Foxp3 promoter, which is reverted by retinoic acid receptor. J. Biol. Chem. 283:14955.
23. Mucida, D., Park, Y., Kim, G. et al. 2007. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317:256.
24. Veldhoen, M., Hirota, K., Westendorf, A. M. et al. 2008. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453:106.
25. Kimura, A., Naka, T., Nohara, K., Fujii-Kuriyama, Y. and Kishimoto, T. 2008. Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc. Natl Acad. Sci. USA 105:9721.
26. Harrington, L. E., Hatton, R. D., Mangan, P. R. et al. 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.
27. Park, H., Li, Z., Yang, X. O. et al. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6:1133.
28. Kryczek, I., Wei, S., Vatan, L. et al. 2007. Cutting edge: opposite effects of IL-1 and IL-2 on the regulation of IL-17+ T cell pool IL-1 subverts IL-2-mediated suppression. J. Immunol. 179:1423.
29. Laurence, A., Tato, C. M., Davidson, T. S. et al. 2007. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26:371.
30. Batten, M., Li, J., Yi, S. et al. 2006. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7:929.
31. Stumhofer, J. S., Laurence, A., Wilson, E. H. et al. 2006. 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.
32. Moroy, T. 2005. The zinc finger transcription factor Growth factor independence 1 (Gfi1). Int. J. Biochem. Cell Biol. 37:541.
33. Shinnakasu, R., Yamashita, M., Kuwahara, M. et al. 2008. Gfi1-mediated stabilization of GATA3 protein is required for Th2 cell differentiation. J. Biol. Chem. 283:28216.
34. Zhu, J., Guo, L., Min, B. et al. 2002. Growth factor independent-1 induced by IL-4 regulates Th2 cell proliferation. Immunity 16:733.
35. Karsunky, H., Zeng, H., Schmidt, T. et al. 2002. Inflammatory reactions and severe neutropenia in mice lacking the transcriptional repressor Gfi1. Nat. Genet. 30:295.
36. Flanders, K. C., Sullivan, C. D., Fujii, M. et al. 2002. Mice lacking Smad3 are protected against cutaneous injury induced by ionizing radiation. Am. J. Pathol. 160:1057.
37. Takaki, H., Minoda, Y., Koga, K., Takaesu, G., Yoshimura, A. and Kobayashi, T. 2006. TGF-beta1 suppresses IFN-gamma-induced NO production in macrophages by suppressing STAT1 activation and accelerating iNOS protein degradation. Genes Cells 11:871.
38. Rodel, B., Tavassoli, K., Karsunky, H. et al. 2000. The zinc finger protein Gfi-1 can enhance STAT3 signaling by interacting with the STAT3 inhibitor PIAS3. EMBO J. 19:5845.
39. Boussif, O., Lezoualc'h, F., Zanta, M. A. et al. 1995. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: Polyethylenimine. Proc. Natl Acad. Sci. USA 92:7297.
40. Matsumura, Y., Kobayashi, T., Ichiyama, K. et al. 2007. Selective expansion of foxp3-positive regulatory T cells and immunosuppression by suppressors of cytokine signaling 3-deficient dendritic cells. J. Immunol. 179:2170.
41. Tanaka, K., Ichiyama, K., Hashimoto, M. 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.
42. Yang, X. O., Nurieva, R., Martinez, G. J. et al. 2008. Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 29:44.
43. Zweidler-Mckay, P. A., Grimes, H. L., Flubacher, M. M. and Tsichlis, P. N. 1996. Gfi-1 encodes a nuclear zinc finger protein that binds DNA and functions as a transcriptional repressor. Mol. Cell. Biol. 16:4024.
44. Duan, Z., Zarebski, A., Montoya-Durango, D., Grimes, H. L. and Horwitz, M. 2005. Gfi1 coordinates epigenetic repression of p21Cip/WAF1 by recruitment of histone lysine methyltransferase G9a and histone deacetylase 1. Mol. Cell. Biol. 25:10338.
45. Grimes, H. L., Chan, T. O., Zweidler-McKay, P. A., Tong, B. and Tsichlis, P. N. 1996. The Gfi-1 proto-oncoprotein contains a novel transcriptional repressor domain, SNAG, and inhibits G1 arrest induced by interleukin-2 withdrawal. Mol. Cell. Biol. 16:6263.
46. Moisan, J., Grenningloh, R., Bettelli, E., Oukka, M. and Ho, I. C. 2007. Ets-1 is a negative regulator of Th17 differentiation. J. Exp. Med. 204:2825.
47. Nakazawa, Y., Suzuki, M., Manabe, N. et al. 2007. Cooperative interaction between ETS1 and GFI1 transcription factors in the repression of Bax gene expression. Oncogene 26:3541.
48. Zhu, J., Davidson, T. S., Wei, G. et al. 2009. Down-regulation of Gfi-1 expression by TGF-beta is important for differentiation of Th17 and CD103+ inducible regulatory T cells. J. Exp. Med. 206:329.