Stat5a inhibits IL-12-induced Th1 cell differentiation through the induction of suppressor of cytokine signaling expression

Journal of Immunology

Volumn 174, Issue 7, 2005, Pages 4105-4112

  Takatori, Hiroaki ^a   Nakajima, Hiroshi ^a   Kagami, Shin Ichiro ^a   Hirose, Koichi ^a   Suto, Akira ^a   Suzuki, Kotaro ^a   Kubo, Masato ^b   Yoshimura, Akihiko ^c   Saito, Yasushi ^a   Iwamoto, Itsuo ^a  

^a CHIBA UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 4; STAT4 PROTEIN; STAT5A PROTEIN; STAT6 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; MALE; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RAT; RETROVIRUS; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

EID: 20144372087     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.7.4105     Document Type: Article

References (44)

1. O'Garra, A., and N. Arei. 2000. The molecular basis of T helper 1 and T helper 2 cell differentiation. Trends Cell Biol. 10:542.
2. Glimcher, L. H., and K. M. Murphy. 2000. Lineage commitment in the immune system: the T helper lymphocyte grows up. Gene Dev. 14:1693.
3. Murphy, K. M., and S. L. Reiner. 2002. The lineage decisions of helper T cells. Nat. Rev. Immunol. 2:933.
4. Takeda, K., T. Tanaka, W. Shi, M. Matsumoto, M. Minami, S. Kashiwamura, K. Nakanishi, N. Yoshida, T. Kishimoto, and S. Akira. 1996. Essential role of Stat6 in IL-4 signaling. Nature 380:627.
5. Shimoda, K., J. van Deursen, M. Y. Sangster, S. R. Sarawar, R. T. Carson, R. A. Tripp, C. Chu, F. W. Quelle, T. Nosaka, D. A. Vignali, et al. 1996. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 380:630.
6. Kaplan, M. H., U. Schindler, S. T. Smiley, and M. J. Grusby. 1996. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4:313.
7. + lymphocytes with a Th2 cytokine profile. J. Immunol. 164:3047.
8. Kuperman, D., B. Schofield, M. Wills-Karp, and M. J. Grusby. 1998. Signal transducer and activator of transcription factor 6 (Stat6)-deficient mice are protected from antigen-induced airway hyperresponsiveness and mucus production. J. Exp. Med. 187:939.
9. Trifilieff, A., A. El-Hasim, R. Corteling, and C. E. Owen. 2000. Abrogation of lung inflammation in sensitized Stat6-deficient mice is dependent on the allergen inhalation procedure. Br. J. Pharmacol. 130:1581.
10. Kagami, S., H. Nakajima, K. Kumano, K. Suzuki, A. Suto, K. Imada, H. W. Davey, Y. Saito, K. Takatsu, W. J. Leonard, and I. Iwamoto. 2000. Both Stat5a and Stat5b are required for antigen-induced eosinophil and T cell recruitment into the tissue. Blood 95:1370.
11. Kagami, S., H. Nakajima, A. Suto, K. Hirose, K. Suzuki, S. Morita, I. Kato, Y. Saito, T. Kitamura, and I. Iwamoto. 2001. Stat5a regulates T helper cell differentiation by several distinct mechanisms. Blood 97:2358.
12. Zhu, J., J. Cote-Sierra, L. Guo, and W. E. Paul. 2003. Stat5 activation plays a critical role in Th2 differentiation. Immunity 19:739.
13. Egwuagu, C. E., C. R. Yu, M. Zhang, R. M. Mahdi, S. J. Kim, and I. Gery. 2002. Suppressors of cytokine signaling proteins are differentially expressed in Th1 and Th2 cells: implications for Th cell lineage commitment and maintenance. J. Immunol. 168:3181.
14. H2-mediated allergic responses. Nat. Med. 9:1047.
15. Liu, X., G. W. Robinson, K.-U. Wagner, L. Garrett, A. Wynshaw-Boris, and L. Hennighausen. 1997. Stat5a is mandatory for adult mammary gland development and lactogenesis. Gene Dev. 11:179.
16. Uzel, G., D. M. Frucht, T. A. Fleisher, and S. M. Holland. 2001. Detection of intracellular phosphorylated STAT-4 by flow cytometry. Clin. Immunol. 100:270.
17. Suto, A., H. Nakajima, K. Hirose, K. Suzuki, S.-I. Kagami, Y. Seto, A. Hoshimoto, Y. Saito, D. C. Foster, and I. Iwamoto. 2002. Interleukin-21 prevents antigen-induced IgE production by inhibiting germline Cε transcription of IL-4-stimulated B cells. Blood 100:4565.
18. Suzuki, K., H. Nakajima, K. Ikeda, Y. Maezawa, A. Suto, H. Takatori, Y. Saito, and I. Iwamoto. 2003. IL-4-Stat6 signaling induces tristetraprolin expression and inhibits TNF-α production in mast cells. J. Exp. Med. 198:1717.
19. Moon, J. J., E. D. Rubio, A. Martino, A. Krumm, and B. H. Nelson. 2004. A permissive role for phosphatidylinositol 3-kinase in the Stat5-mediated expression of cyclin D2 by the interleukin-2 receptor. J. Biol. Chem. 279:5520.
20. Mikita, T., D. Campbell, P. Wu, K. Williamson, and U. Schindler. 1996. Requirements for interleukin-4-induced gene expression and functional characterization of Stat6. Mol. Cell. Biol. 16:5811.
21. Wakao, H., F. Gouilleux, and B. Groner. 1994. Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J. 13:2182.
22. Auernhammer, C. J., C. Bousquet, and S. Melmed. 1999. Autoregulation of pituitary corticotroph SOCS-3 expression: characterization of the murine SOCS-3 promoter. Proc. Natl. Acad. Sci. USA 96:6964.
23. Nosaka, T., T. Kawashima, K. Misawa, K. Ikuta, A. L. Mui, and T. Kitamura. 1999. Stat5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J. 18:4754.
24. Daniel, C., A. Salvekar, and U. Schindler. 2000. A gain-of-function mutation in STAT6. J. Biol. Chem. 275:14255.
25. Morita, S., T. Kojima, and T. Kitamura. 2000. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 7:1063.
26. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3:133.
27. Szabo, S. J., A. S. Dighe, U. Gubler, and K. M. Murphy. 1997. Regulation of the interleukin (IL)-12Rβ2 subunit expression in developing T helper 1 (Th1) and Th2 cells. J. Exp. Med. 185:817.
28. Yasukawa, H., A. Sasaki, and A. Yoshimura. 2000. Negative regulation of cytokine signaling pathways. Annu. Rev. Immunol. 18:143.
29. Greenhalgh, C. J., and D. J. Hilton. 2001. Negative regulation of cytokine signaling. J. Leukocyte Biol. 70:348.
30. Kubo. M., T. Hanada, and A. Yoshimura. 2003. Suppressors of cytokine signaling and immunity. Nat. Immunol. 4:1169.
31. Ehret, G. B., P. Reichenbach, U. Schindler, C. M. Horvath, S. Fritz, M. Nabholz, and P. Bucher. 2001. DNA binding specificity of different STAT proteins: comparison of in vitro specificity with natural target sites. J. Biol. Chem. 276:6675.
32. Alexander, W. S., R. Starr, J. E. Fenner, C. L. Scott, E. Handman, N. S. Sprigg, J. E. Corbin, A. L. Cornish, R. Darwiche, C. M. Owczarek, et al. 1999. SOCS1 is a critical inhibitor of interferon γ signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell 98:597.
33. Marine, J.-C., D. J. Topham, C. McKay, D. Wang, E. Parganas, D. Stravopodis, A. Yoshimura, and J. N. Ihle. 1999. SOCS1 deficiency causes a lymphocytedependent perinatal lethality. Cell 98:609.
34. Ben-Sasson, S. Z., G. Le Gros, D. H. Conrad, F. D. Finkelman, and W. E. Paul. 1990. IL-4 production by T cells from naive donors: IL-2 is required for IL-4 production. J. Immunol. 145:1127.
35. Hwang, E. S., I. A. White, and I. C. Ho. 2002. An IL-4-independent and CD25-mediated function of c-maf in promoting the production of Th2 cytokines. Proc. Natl. Acad Sci. USA 99:13026.
36. Nakajima, H., X. W. Liu, A. Wynshaw-Boris, L. A. Rosenthal, K. Imada, D.S. Finbloom, L. Hennighausen, and W. J. Leonard. 1997. An indirect effect of Stat5a in IL-2-induced proliferation: a critical role for Stat5a in IL-2-mediated IL-2 receptor α chain induction. Immunity 7:691.
37. Cote-Sierra, L, G. Foucras, L. Guo, L. Chiodetti, H. A. Young, J. Hu-Li, J. Zhu, and W. E. Paul. 2004. Interleukin 2 plays a central role in Th2 differentiation. Proc. Natl. Acad. Sci. USA 101:3880.
38. Y and a GATA family protein. EMBO J. 15:5627.
39. Lecine, P., M. Algarte, P. Rameil, C. Beadling, P. Bucher, M. Nabholz, and J. Imbert. 1996. Elf-1 and Stat5 bind to a critical element in a new enhancer of the human interleukin-2 receptor a gene. Mol. Cell. Biol. 16:6829.
40. Lin, J.-X., and W. J. Leonard. 2000. The role of Stat5a and Stat5b in signaling by IL-2 family cytokines. Oncogene 19:2566.
41. Moriggl, R., D. J. Topham, S. Teglund, V. Sexl, C. McKay, D. Wang, A. Hoffmeyer, J. van Deursen, M. Y. Sangster, K. D. Bunting, et al. 1999. Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity 10:249.
42. Imada, K., E. T. Bloom, H. Nakajima, J. A. Horvath-Arcidiacono, G. B. Udy, H. W. Davey, and W. J. Leonard. 1998. Stat5b is essential for natural killer cell-mediated proliferation and cytolytic activity. J. Exp. Med. 188:2067.
43. Bream, J. H., D. L. Hodge, R. Gonsky, R. Spolski, W. J. Leonard, S. Krebs, S. Targan, A. Morinobu, J. J. O'Shea, and H. A. Young. 2004. A distal region in the interferon-γ gene is a site of epigenetic remodeling and transcriptional regulation by interleukin-2. J. Biol. Chem. 279:41249.
44. Takatori, H., H. Nakajima, K. Hirose, S-i. Kagami, T. Tamachi, A. Suto, K. Suzuki, Y. Saito, and I. Iwamoto. Indispensable role of Stat5a in Stat6-independent Th2 cell differentiation and allergic airway inflammation. J. Immunol. In press.