IL-4 selectively inhibits IL-2-triggered Stat5 activation, but not proliferation, in human T cells

Journal of Immunology

Volumn 162, Issue 3, 1999, Pages 1261-1269

  Castro, Aaron ^a   Sengupta, Tapas K ^a   Ruiz, Donna C ^a   Yang, Edward ^b   Ivashkiv, Lionel B ^a,b,c  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Weill Cornell Medical Center   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D3; CYCLIN DEPENDENT KINASE INHIBITOR; DNA; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 7; MITOGEN ACTIVATED PROTEIN KINASE; PROSTAGLANDIN E RECEPTOR; PROTEIN TYROSINE KINASE; STAT5 PROTEIN; TYROSINE;

ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSIVE ELEMENT; DNA BINDING; HELPER CELL; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; ONCOGENE C FOS; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

BASE SEQUENCE; CELL DIFFERENTIATION; CELL DIVISION; DNA PRIMERS; DNA-BINDING PROTEINS; HUMANS; INTERLEUKIN-2; INTERLEUKIN-4; LYMPHOCYTE ACTIVATION; MILK PROTEINS; PROTEIN CONFORMATION; RECEPTORS, INTERLEUKIN-2; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; T-LYMPHOCYTES; TH1 CELLS; TH2 CELLS; TRANS-ACTIVATORS;

EID: 0033083261     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (73)

1. Smith, K. A. 1988. Interleukin-2: inception, impact, and implications. Science 240:1169.
2. Karnitz, L. M., and R. T. Abraham. 1996. Interleukin-2 receptor signaling mechanisms. Adv. Immunol. 61:147.
3. Taniguchi, T., and Y. Minami. 1993. The IL-2/IL-2 receptor system: a current overview. Cell 73:5.
4. Taniguchi, T., T. Miyazaki, Y. Minami, A. Kawahara, H. Fujii, Y. Nakagawa, M. Hatakeyama, and Z. J. Liu. 1995. IL-2 signaling involves recruitment and activation of multiple protein tyrosine kinases by the IL-2 receptor. Ann. NY Acad. Sci. 766:235.
5. Frank, D. A., M. J. Robertson, A. Bonni, J. Ritz, and M. E. Greenberg. 1995. Interleukin 2 signaling involves the phosphorylation of Stat proteins. Proc. Natl. Acad. Sci. USA 92:7779.
6. Gaffen, S. L., S. Y. Lai, W. Xu, F. Gouilleux, B. Groner, M. A. Goldsmith, and W. C. Greene. 1995. Signaling through the interleukin 2 receptor β chain activates a STAT-5-like DNA-binding activity. Proc. Natl. Acad. Sci. USA 92:7192.
7. Fujii, H., Y. Nakagawa, U. Schindler, A. Kawahara, H. Mori, F. Gouilleux, B. Groner, J. N. Ihle, Y. Minami, T. Miyazaki, and et al. 1995. Activation of Stat5 by interleukin 2 requires a carboxyl-terminal region of the interleukin 2 receptor β chain but is not essential for the proliferative signal transmission. Proc. Natl. Acad. Sci. USA 92:5482.
8. Beadling, C., D. Guschin, B. A. Witthuhn, A. Ziemiecki, J. N. Ihle, I. M. Kerr, and D. A. Cantrell. 1994. Activation of JAK kinases and STAT proteins by interleukin-2 and interferon α, but not the T cell antigen receptor, in human T lymphocytes. EMBO J. 13:5605.
9. Hou, J., U. Schindler, W. J. Henzel, S. C. Wong, and S. L. McKnight. 1995. Identification and purification of human Stat proteins activated in response to interleukin-2. Immunity 2:321.
10. Johnston, J. A., C. M. Bacon, D. S. Finbloom, R. C. Rees, D. Kaplan, K. Shibuya, J. R. Ortaldo, S. Gupta, Y. Q. Chen, J. D. Giri, et al. 1995. Tyrosine phosphorylation and activation of STAT5, STAT3, and Janus kinases by interleukins 2 and 15. Proc. Natl. Acad. Sci. USA. 92:8705.
11. Lin, J. X., T. S. Migone, M. Tsang, M. Friedmann, J. A. Weatherbee, L. Zhou, A. Yamauchi, E. T. Bloom, J. Mietz, S. John, et al. 1995. The role of shared receptor motifs and common Stat proteins in the generation of cytokine pleiotropy and redundancy by IL-2, IL-4, IL-7, IL-13, and IL-15. Immunity 2:331.
12. Kawahara, A., Y. Minami, T. Miyazaki, J. N. Ihle, and T. Taniguchi. 1995. Critical role of the interleukin 2 (IL-2) receptor γ-chain-associated Jak3 in the IL-2-induced c-fos and c-myc, but not bcl-2, gene induction. Proc. Natl. Acad. Sci. USA 92:8724.
13. Miyazaki, T., Z. J. Liu, A. Kawahara, Y. Minami, K. Yamada, Y. Tsujimoto, E. L. Barsoumian, R. M. Permutter, and T. Taniguchi. 1995. Three distinct IL-2 signaling pathways mediated by bcl-2, c-myc, and lck cooperate in hematopoietic cell proliferation. Cell 81:223.
14. S) gene expression. Eur. J. Immunol. 26:294.
15. Takeshita, T., T. Arita, M. Higuchi, H Asao, K. Endo, H. Kuroda, N. Tanaka, K. Murata, N. Ishii, and K. Sugamura. 1997. STAM, signal transducing adaptor molecule, is associated with Janus kinases and involved in signaling for cell growth and c-myc induction. Immunity 6:449.
16. Izquierdo, M., and D. A. Cantrell. 1993. Protein tyrosine kinases couple the interleukin-2 receptor to p21ras. Eur. J. Immunol. 23:131.
17. Reif, K., B. M. T. Burgering, and D. A. Cantrell. 1997. Phosphatidylinositol 3-kinase links the interleukin-2 receptor to protein kinase B and p70 S6 kinase. J. Biol. Chem. 272:14426.
18. Beadling, C., J. Ng, J. W. Babbage, and D. A. Cantrell. 1996. Interleukin-2 activation of STAT5 requires the convergent action of tyrosine kinases and a serine/threonine kinase pathway distinct from the Raf1/ERK2 MAP kinase pathway. EMBO J. 15:1902.
19. Friedmann, M. C., T. S. Migone, S. M. Russell, and W. J. Leonard. 1996. Different interleukin 2 receptor β-chain tyrosines couple to at least two signaling pathways and synergistically mediate interleukin 2-induced proliferation. Proc. Natl. Acad. Sci. USA 93:2077.
20. Gaffen, S. L., S. Y. Lai, M. Ha, X. Liu, L. Hennighausen, W. C. Greene, and M. A. Goldsmith. 1996. Distinct tyrosine residues within the interleukin-2 receptor β chain drive signal transduction specificity, redundancy, and diversity. J. Biol. Chem. 271:21381.
21. Ihle, J. N., B. A. Witthuhn, F. W. Quelle, K. Yamamoto, and O. Silvennoinen. 1995. Signaling through the hematopoietic cytokine receptors. Annu. Rev. Immunol. 13:369.
22. Nelson, B. H., J. D. Lord, and P. D. Greenberg. 1996. A membrane-proximal region of the interleukin-2 receptor γ c chain sufficient for Jak kinase activation and induction of proliferation in T cells. Mol. Cell. Biol. 16:309.
23. Oakes, S. A., F. Candotti, J. A. Johnston, Y. Q. Chen, J. J. Ryan, N. Taylor, X. Liu, L. Hennighausen, L. D. Notarangelo, W. E. Paul, R. M. Blaese, and J. J. O'Shea. 1996. Signaling via IL-2 and IL-4 in JAK3-deficient severe combined immunodeficiency lymphocytes: JAK3-dependent and independent pathways. Immunity 5:605.
24. Miyazaki, T., A. Kawahara, H. Fujii, Y. Nakagawa, Y. Minami, Z. J. Liu, I. Oishi, O. Silvennoinen, B. A. Witthuhn, J. N. Ihle, et al. 1994. Functional activation of Jak1 and Jak3 by selective association with IL-2 receptor subunits. Science 266:1045.
25. Kirken, R. A., H. Rui, M. G. Malabarba, O. M. Howard, M. Kawamura, O. S. JJ, and W. L. Farrar. 1995. Activation of JAK3, but not JAK1, is critical for IL-2-induced proliferation and STAT5 recruitment by a COOH-terminal region of the IL-2 receptor β-chain. Cytokine 7:689.
26. Teglund, S., C. McKay, E. Schuetz, J. M. van Deursen, D. Stravopodis, D. Wang, M. Brown, S. Bodner, G. Grosveld, and J. N. Ihle. 1998. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 93:841.
27. Zamorano, J., H. Y. Wang, R. Wang, Y. Shi, G. D. Longmore, and A. D. Keegan. 1998. Regulation of cell growth by IL-2: role of STAT5 in protection from apoptosis but not in cell cycle progression. J. Immunol. 160:3502.
28. 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 a chain induction. Immunity 7:691.
29. + T cells. Annu. Rev. Immunol. 12:635.
30. Szabo, S. J., N. G. Jacobson, A. S. Dighe, U. Gubler, and K. M. Murphy. 1995. Developmental commitment to the Th2 lineage by extinction of IL-12 signaling. Immunity 2:665.
31. Szabo, S. J., A. S. Dighe, U. Gubler, and K. M. Murphy. 1997. Regulation of the interleukin (IL)-12R β 2 subunit expression in developing T helper 1 (Th1) and Th2 cells. J. Exp. Med. 185:817.
32. Sakatsume, M., and D. S. Finbloom. 1996. Modulation of the expression of the IFN-γ receptor β-chain controls responsiveness to IFN-gamma in human peripheral blood T cells. J. Immunol. 156:4160.
33. Bach, E. A., S. J. Szabo, A. S. Dighe, A. Ashkenazi, M. Aguet, K. M. Murphy, and R. D. Schreiber. 1995. Ligand-induced autoregulation of IFN-γ receptor β chain expression in T helper cell subsets. Science 270:1215.
34. Pernis, A., S. Gupta, K. J. Gollob, E. Garfein, R. L. Coffman, C. Schindler, and P. Rothman. 1995. Lack of interferon γ receptor β chain and the prevention of interferon γ signaling in TH1 cells. Science 269:245.
35. Yanagida, T., T. Kato, O. Igarashi, T. Inoue, and H. Nariuchi. 1994. Second signal activity of IL-12 on the proliferation and IL-2R expression of T helper cell-1 clone. J. Immunol. 152:4919.
36. Paul, W. E., and R. A. Seder. 1994. Lymphocyte responses and cytokines. Cell 76:241.
37. Heinzel, F. P., R. M. Rerko, F. Hatam, and R. M. Locksley. 1993. IL-2 is necessary for the progression of leishmaniasis in susceptible murine hosts. J. Immunol. 150:3924.
38. Le Gros, G., S. Z. Ben-Sasson, R. Seder, F. D. Finkelman, and W. E. Paul. 1990. Generation of interleukin 4 (IL-4)-producing cells in vivo and in vitro: IL-2 and IL-4 are required for in vitro generation of IL-4-producing cells. J. Exp. Med. 172:921.
39. O'Garra, A., and K. Murphy. 1994. Role of cytokines in determining T-lymphocyte function. Curr. Opin. Immunol. 6:458.
40. Cantrell, D. A., and K. A. Smith. 1984. The interleukin-2 T-cell system: a new cell growth model. Science 224:1312.
41. Stern, J. B., and K. A. Smith. 1986 Interleukin-2 induction of T-cell G1 progression and c-myb expression. Science 233:203.
42. Sengupta, T. K., E. M. Schmitt, and L. B. Ivashkiv. 1996. Inhibition of cytokines and JAK-STAT activation by distinct signaling pathways. Proc. Natl. Acad. Sci. USA 93:9499.
43. Ivashkiv, L. B., E. M. Schmitt, and A. Castro. 1996. Inhibition of transcription factor Stat1 activity in mononuclear cell cultures and T cells by the cyclic AMP signaling pathway. J. Immunol. 157:1415.
44. Beadling, C., K. W. Johnson, and K. A. Smith. 1993. Isolation of interleukin 2-induced immediate-early genes. Proc. Natl. Acad. Sci. USA 90:2719.
45. Kaplan, M. H., C. Daniel, U. Schindler, and M. J. Grusby. 1998. Stat proteins control lymphocyte proliferation by regulating p27Kip1 expression. Mol. Cell. Biol. 18:1996.
46. Wang, F., T. K. Sengupta, Z. Zhong, and L. B. Ivashkiv. 1995. Regulation of the balance of cytokine production and the signal transducer and activator of transcription (STAT) transcription factor activity by cytokines and inflammatory synovial fluids. J. Exp. Med. 182:1825.
47. Henttinen, T., D. E. Levy, O. Silvennoinen, and M. Hurme. 1995. Activation of the signal transducer and transcription (STAT) signaling pathway in a primary T cell response: critical role for IL-6. J. Immunol. 155:4582.
48. Liu, K. D., S. Y. Lai, M. A. Goldsmith, and W. C. Greene. 1995. Identification of a variable region within the cytoplasmic tail of the IL-2 receptor β chain that is required for growth signal transduction. J. Biol. Chem. 270:22176.
49. John, S., C. M. Robbins, and W. J. Leonard. 1996. An IL-2 response element in the human IL-2 receptor a chain promoter is a composite element that binds Stat5, Elf-1, HMG-1(Y) and a GATA family protein. EMBO J. 15:5627.
50. 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 α gene. Mol. Cell. Biol. 16:6829.
51. Matsumoto, A., M. Masuhara, K. Mitsui, M. Yokouchi, M. Ohtsubo, H. Misawa, A. Miyajima, and A. Yoshimura. 1997. CIS, a cytokine inducible SH2 protein, is a target of the JAK-STAT5 pathway and modulates STAT5 activation. Blood 89:3148.
52. Breuer, M., R. Slebos, S. Verbeek, M. van Lohuizen, E. Wientjens, and A. Berns. 1989. Very high frequency of lymphoma induction by a chemical carcinogen in pim-1 transgenic mice. Nature 340:61.
53. 2. J. Immunol. 145:2616.
54. Dickinson, L. A., T. Joh, Y. Kohwi, and T. Kohwi-Shigematsu. 1992. A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell 70:631.
55. Hemar, A., A. Subtil, M. Lieb, E. Morelon, R. Hellio, and A. Dautry-Varsat. 1995. Endocytosis of intcrleukin 2 receptors in human T lymphocytes: distinct intracellular localization and fate of the receptor α, β, and γ chains. J. Cell. Biol. 129:55.
56. Nakarai, T., M. J. Robertson, M. Streuli, Z. Wu, T. L. Ciardelli, K. A. Smith, and J. Ritz. 1994. Interleukin 2 receptor γ chain expression on resting and activated lymphoid cells. J. Exp. Med. 180:241.
57. Fernandez-Botran, R., V. M. Sanders, and E. S. Vitetta. 1989. Interactions between receptors for interleukin 2 and interleukin 4 on lines of helper T cells (HT-2) and B lymphoma cells (BCL1). J. Exp. Med. 169:379.
58. Cantrell, D. A., M. Izquierdo, K. Reif, and M. Woodrow. 1993. Regulation of PtdIns-3-kinase and the guaninc nucleotide binding proteins p21ras during signal transduction by the T cell antigen receptor and the interleukin-2 receptor. Semin. Immunol. 5:319.
59. Keegan, A. D., K. Nelms, L. M. Wang, J. H. Pierce, and W. E. Paul. 1994. Interleukin 4 receptor: signaling mechanisms. Immunol. Today 15:423.
60. Minami, Y., Y. Nakagawa, A. Kawahara, T. Miyazaki, K. Sada, H. Yamamura, and T. Taniguchi. 1995. Protein tyrosine kinase Syk is associated with and activated by the IL-2 receptor: possible link with the c-myc induction pathway. Immunity 2:89.
61. Naka, T., M. Narazaki, M. Hirata, T. Matsumoto, S. Minamoto, A. Aono, N. Nishimoto, T. Kajita, T. Taga, K. Yoshizaki, S. Akira, and T. Kishimoto. 1997. Structure and function of a new STAT-induced STAT inhibitor. Nature 387:924.
62. Starr, R., T. A. Willson, E. M. Viney, L. J. Murray, J. R. Rayner, B. J. Jenkins, T. J. Gonda, W. S. Alexander, D. Metcalf, N. A. Nicola, and D. J. Hilton. 1997. A family of cytokine-inducible inhibitors of signalling. Nature 387:917.
63. Endo, T. A., M. Masuhara, M. Yokouchi, R. Suzuki, H. Sakamoto, K. Mitsui, A. Matsumoto, S. Tanimura, M. Ohtsubo, H. Misawa, et al. 1997. A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387:921.
64. Chung, C. D., J. Liao, B. Liu, X. Rao, P. Jay, P. Berta, and K. Shuai. 1997. Specific inhibition of Stat3 signal transduction by PIAS3. Science 278:1803.
65. Blanchard, D. A., M. T. Affredou, and A. Vazquez. 1997. Modulation of the p27kip1 cyclin-dependent kinase inhibitor expression during IL-4-mediated human B cell activation. J. Immunol. 158:3054.
66. Higuchi, M., H. Asao, N. Tanaka, K. Oda, T. Takeshita, M. Nakamura, J. Van Snick, and K. Sugamura. 1996. Dispensability of Jak1 tyrosine kinase for interleukin-2-induced cell growth signaling in a human T cell line. Eur. J. Immunol. 26:1322.
67. Rodig, S. J., M. A. Meraz, J. M. White, P. A. Lampe, J. K. Riley, C. D. Arthur, K. L. King, K. C. Sheehan, L. Yin, D. Pennica, et al. 1998. Disruption of the Jak1 gene demonstrates obligatory and nonredundart roles of the Jaks in cytokine-induced biologic responses. Cell 93:373.
68. Noguchi, M., H. Yi, H. M. Rosenblatt, A. H. Filipovich, S. Adelstein, W. S. Modi, O. W. McBride, and W. J. Leonard. 1993. Interleukin-2 receptor γ chain mutation results in X-linked severe combined immunodeficiency in humans. Cell 73:147.
69. Nosaka, T., J. M. van Deursen, R. A. Tripp, W. E. Thierfelder, B. A. Witthuhn, A. P. McMickle, P. C. Doherty, G. C. Grosveld, and J. N. Ihle. 1995. Defective lymphoid development in mice lacking Jak3. Science 270:800.
70. Thomis, D. C., C. B. Gurniak, E. Tivol, A. H. Sharpe, and L. J. Berg. 1995. Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3. Science 270:794.
71. Cao, X., E. W. Shores, J. Hu-Li, M. R. Anver, B. L. Kelsall, S. M. Russell, J. Drago, M. Noguchi, A. Grinberg, E. T. Bloom, et al. 1995. Defective lymphoid development in mice lacking expression of the common cytokine receptor γ chain. Immunity 2:223.
72. Nakajima, H., E. W. Shores, M. Noguchi, and W. J. Leonard. 1997. The common cytokine receptor γ chain plays an essential role in regulating lymphoid homeostasis. J. Exp. Med. 185:189.
73. Thomis, D. C., W. Lee, and L. J. Berg. 1997. T cells from Jak3-deficient mice have intact TCR signaling, but increased apoptosis. J. Immunol. 159:4708.