The IL-2 receptor promotes lymphocyte proliferation and induction of the c-myc, bcl-2, and bcl-x genes through the trans-activation domain of Stat5

Journal of Immunology

Volumn 164, Issue 5, 2000, Pages 2533-2541

  Lord, James D ^a,b,c   McIntosh, Bryan C ^a   Greenberg, Philip D ^b,c   Nelson, Brad H ^a,c  

^a BENAROYA RESEARCH INSTITUTE   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2 RECEPTOR; MUTANT PROTEIN; RECEPTOR SUBTYPE; STAT5 PROTEIN; TYROSINE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE INDUCTION; LYMPHOCYTE PROLIFERATION; MITOGENESIS; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTO ONCOGENE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSACTIVATION;

EID: 0034163579     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.164.5.2533     Document Type: Article

References (68)

1. Takeshita, T., K. Ohtani, H. Asao, S. Kumaki, M. Nakamura, and K. Sugamura. 1992. An associated molecule, p64 with IL-2 receptor β chain: its possible involvement in the formation of the functional intermediate-affinity IL-2 receptor complex. J. Immunol. 148:2154.
2. Nelson, B. H., J. D. Lord, and P. D. Greenberg. 1994. Cytoplasmic domains of the interleukin-2 receptor β and γ chains mediate the signal for T-cell proliferation. Nature 369:333.
3. Nakamura, Y., S. Russell, S. Mess, M. Friedmann, M. Erdos, C. Francois, Y. Jacques, S. Adelstein, and W. Leonard. 1994. Heterodimerization of the IL-2 receptor β- and γ-chain cytoplasmic domains is required for signalling. Nature 369:330.
4. Russell, S., J. Johnston, M. Noguchi, M. Kawamura, C. Bacon, M. Friedmann, M. Berg, D. McVicar, B. Witthuhn, and O. Silvennoinen. 1994. Interaction of 1L-2R β and γ c chains with Jak1 and Jak3: implications for XSCID and XCID. Science 266:1042.
5. Miyazaki, T., A. Kawahara, H. Fujii, Y. Nakagawa, Y. Minami, Z. Liu, I. Oishi, O. Silvennoinen, B. Witthuhn, J. Ihle. et al. 1994. Functional activation of Jak1 and Jak3 by selective association with IL-2 receptor subunits. Science 266:1045.
6. 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.
7. Park, S. Y., K. Saijo, K. Takahashi, M. Osawa, H. Arase, N. Hirayama, K. Miyake, H. Nakauchi, T. Shirasawa, and T. Saito. 1995. Developmental defects of lymphoid cells in Jak3 kinase-deficient mice. Immunity 3:771.
8. 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.
9. Nelson, B. H., B. C. McIntosh, L. L. Rosencrans, and P. D. Greenberg. 1997. Requirement for an initial signal from lhe membrane-proximal region of the interleukin 2 receptor γ c chain for Janus kinase activation leading to T cell proliferation. Proc. Natl. Acad. Sci. USA 94:1878.
10. Witthuhn, B. A., O. Silvennoinen, O. Miura, K. S. Lai, C. Cwik, E. T. Liu, and J. N. Ihle. 1994. Involvement of the Jak-3 janus kinase in signalling by interleukins 2 and 4 in lymphoid and myeloid cells. Nature 370:153.
11. Friedmann, M. C., T. S. Migone, S. M. Russell, and W. J. Leonard. 1996. Different interleukin 2 receptor beta-chain tyrosines couple to at least two signaling pathways and synergistically mediate interleukin 2-induced proliferation. Proc. Natl. Acad. Sci. USA 93:2077.
12. Goldsmith, M. A., S. Y. Lai, W. Xu, M. C. Amaral, E. S. Kuczek, L. J. Parent, G. B. Mills, K. L. Tarr, G. D. Longmore, and W. C. Greene. 1995. Growth signal transduction by the human interleukin-2 receptor requires cytoplasmic tyrosines of the β chain and non-tyrosine residues of the γ c chain. J. Biol Chem 270: 21729.
13. Ravichandran, K. S., V. Igras, S. E. Shoelson, S. W. Fesik, and S. J. Burakoff. 1996. Evidence for a role for the phosphotyrosine binding domain of She in interleukin-2 signalling. Proc. Natl. Acad. Sci. USA 93:5275.
14. Lord, J. D., B. C. McIntosh, P. D. Greenberg, and B. H. Nelson. 1998. The IL-2 receptor promotes proliferation, bcl-2 and bcl-x induction, but not cell viability through the adapter molecule She. J. Immunol. 161:4627.
15. Claesson-Welsh, L. 1994. Platelet derived growth factor receptor signals. J. Biol. Chem. 269:32023.
16. Mui, A. L.-F., H. Wakao, A.-M. O'Farrell, N. Harada, and A. Miyajima. 1995. Interleukin-3, granulocyte-macrophage colony stimulating factor and interleukin-5 transduce signals through two STAT5 homologs. 1995 14:1166.
17. Lin, J.-X., J. Mietz, W. S. Modi, S. John, and W. J. Leonard. 1996. Cloning of human Stat5B. J. Biol. Chem. 271:10738.
18. 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.
19. Heim, M. H., I. M. Kerr, G. R. Stark, and J. E. Darnell, Jr. 1995. Contribution of STAT SH2 groups to specific interferon signaling by the Jak-STAT pathway. Science 267:1347.
20. Lin, J.-X., T.-S. Migone, M. Tsang, M. Friedmann, J. A. Weatherbee, L. Zhou, A. Yamaguchi, 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 pleotropy and redundancy by IL-2, IL-4, IL-7, IL-13, and IL-15. Immunity 2:331.
21. Greenlund, A. C., M. O. Morales, B. L. Viviane, H. Yan, J. Krolewski, and R. D. Schreiber, 1995. Stat recruitment by tyrosine-phosphorylated cytokine receptors: an ordered reversible affinity-driven process. Immunity 2:677.
22. Schindler, U., P. Wu, M. Rothe, M. Brasseur, and S. L. McKnight. 1995. Components of a Stat recognition code: evidence for two layers of molecular selectivity. Immunity 2:689.
23. Darnell, J. E. 1997. STATs and gene regulation. Science 277:1630.
24. Ihle, J. N. 1996. STATs: signal transducers and activators of transcription. Cell 84:331.
25. Yoshimura, A., M. Ichihara, I. Kinjyo, M. Moriyama, N. G. Copeland, D. J. Gilbert, N. A. Jenkins. T. Hara, and A. Miyajima. 1996. Mouse oncostatin M: an immediate early gene induced by multiple cytokines through the JAK-STAT5 pathway. EMBO J. 15:1055.
26. Matsumoto, A., M. Masuhara, K. Misui, M. Yokouchi, M. Ohtsubo, H. Mitsawa, 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 89:48.
27. John, S., C. M. Robbins, and W. J. Leonard. 1996. An IL-2 response element in the human IL-2 receptor alpha chain promoter is a composite element that binds Stat5, Elf-1, HMG-1(Y) and a GATA family protein. EMBO J. 15:5627.
28. Minami, M., M. Inoue, S. Wei, K. Takeda, M. Matsumoto, T. Kishimoto, and S. Akira. 1996. STAT3 activation is a critical step in gp130-mediated terminal differentiation and growth arrest of a myeloid cell line. Proc. Natl. Acad. Sci. USA 93:3963.
29. Wang, D., D. Stravdopodis, S. Teglund, J. Kitazawa, and J. N. Ihle. 1996. Naturally occurring dominant negative variants of Stat5. Mol. Cell. Biol. 16:6141.
30. Azam, M., C. Lee, I. Strehlow, and C. Schindler. 1997. Functionally distinct isoforms of STAT5 are generated by protein processing. Immunity 6:691.
31. Moriggl, R., V. Gouilleux-Gruart, R. Jahne, S. Berchtold, C. Gartmann, X. Liu, L. Hennighausen, A. Sotiropoulos, B. Groner, and F. Gouilleux. 1996. Deletion of the carboxy-terminal transactivation domain of MGF-Stat5 results in sustained DNA binding and a dominant negative phenotype. Mol. Cell. Biol. 16:5691.
32. Pfeffer, L. M., J. E. Mullersman, S. R. Pfeffer, A. Murti, W. Shi, and C. H. Yang. 1997. STAT3 as an adapter to couple phosphatidylinositol 3-kinase to the IF-NAR1 chair of the type I interferon receptor. Science 276:1418.
33. Kumar, A., M. Commane, T. W. Flickinger, C. M. Horvath, and G. R. Stark. 1997. Defective TNF-α-induced apoptosis in STAT1-null cells due to low constitutive levels of caspases. Science 278:1630.
34. Lechner, J., T. Welte, J. K. Tomasi, P. Bruno, C. Cairns, J.-A. Gustafsson, and W. Doppler. 1997. Promoter-dependent synergy between glucocorticoid receptor and Stat5 in the activation of β-casein gene transcription. J. Biol. Chem. 272: 20954.
35. Stoecklin, E., M. Wissler, R. Moriggl, and B. Groner. 1997. Specific DNA binding of Stat5, but not of glucocorticoid receptor, is required for their functional cooperation in the regulation of gene transcription. Mol. Cell. Biol. 17:6708.
36. Moriggl, R., C. 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.
37. Fujii, H., Y. Nakagawa, U. Schindler, A. Kawahara, H. Mori, F. Gouilleux, B. Groner, J. Ihle, Y. Minami, T. Miyazaki, 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.
38. 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.
39. Fujii, H., K. Ogasawara, H. Otsuka, M. Suzuki, K.-I. Yamamura, T. Yokochi, T. Miyazaki, H. Suzuki, T. W. Mak, S. Taki, et al. 1998. Functional dissection of the cytoplasmic subregions of the IL-2 receptor β c chain in primary lymphocyte populations. EMBO J. 17:6551.
40. Welte, T., D. Leitenberg, B. N. Dittel, B. K. al-Ramadi, B. Xie, Y. E. Chin, C. A. Janeway, Jr., A. L. M. Bothwell, K. Bottomly, and X.-Y. Fu. 1999. STAT5 interaction with the T cell receptor complex and stimulation of T cell proliferation. Science 283:222.
41. 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.
42. Ziegler, S. F., T. A. Bird, K. M. Morella, B. Mosley, D. P. Gearing, and H. Baumann. 1993. Distinct regions of the human granulocyte-colony-stimulating factor receptor are required for proliferation and gene induction. Mol. Cell. Biol. 13:2384.
43. 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.
44. Ascherman, D. P., T.-S. Migone, M. C. Friedmann, and W. J. Leonard. 1997. Interleukin-2 (IL-2)-mediated induction of the IL-2 receptor α chain gene. J. Biol. Chem. 272:8704.
45. Boucheron, C., S. Dumon, S. C. Santos, R. Moriggl, L. Hennighausen, S. Gisselbrecht, and F. Gouilleux. 1998. A single amino acid in the DNA-binding regions of STAT5A and STAT5B confer distinct DNA-binding specificities. J. Biol. Chem. 273:33936.
46. Verdier, F., R. Rabionet, F. Gouilleux, C. Beisenherz-Huss, P. Varlet, O. Muller, P. Mayeux, C. Lacombe, S. Gisselbrecht, and S. Chretien. 1998. A sequence of the CIS gene promoter interacts preferentially with two associated STAT5A dimers: a distinct biochemical difference between STAT5A and STAT5B. Mol. Cell. Biol. 18:5852.
47. Udy, G. B., R. P. Towers, R. G. Snell, R. W. Wilkins, S.-H. Park, P. A. Ram, D. J. Waxman, and H. W. Davey. 1997. Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc. Natl. Acad. Sci. USA 94:7239.
48. 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 alpha chain induction. Immunity 7:691.
49. 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 cytolylic activity. J. Exp. Med. 188:2067.
50. Teglund, S., C. McKay, E. Schuetz, J. M. v. 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.
51. Mui, A. L., H. Wakao, T. Kinoshita, T. Kitamura, and A. Miyajima. 1996. Suppression of interleukin-3-induced gene expression by a C-terminal truncated Stat5: role of Stat5 in proliferation. EMBO J. 15:2425.
52. Zhang, Z., Z. Wen, and J. E. Darnell. 1994. Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264:95.
53. Shibuya, H., M. Yoneyama, J. Ninomiya-Tsuji, K. Matsumoto, and T. Taniguchi. 1992. IL-2 and EGF receptors stimulate the hematopoietic cell cycle via different signaling pathways: demonstration of a novel role for c-myc. Cell 70:57.
54. 1. Nature 328:445.
55. Akbar, A. N., N. J. Borthwick, R. G. Wickremasinghe, P. Panayiotidis, D. Pilling, M. Bofill, S. Krajewski, J. C. Reed, and M. Salmon. 1996. Interleukin-2 receptor common gamma chain signaling cytokines regulate activated T cell apoptosis in response to growth factor withdrawal: selective induction of anti-apoptotic (bcl-2, bcl-xL) but not pro-apoptotic (bax. bcl-xS) gene expression. Eur. J. Immunol. 26:294.
56. Deng, G., and E. R. Podack. 1993. Suppression of apoptosis in a cytotoxic T-cell line by interleukin-2-mediated gene transcription and deregulated expression of the protooncogene bcl-2. Proc. Natl. Acad. Sci. USA 90:2189.
57. Boise, L. H., A. J. Minn, P. J. Noel, C. H. June, M. A. Accavitti, T. Lindsten, and C. B. Thompson, 1995. CD28 costimulation can promote T cell survival by enhancing the expression of bcl-xL. Immunity 3:87.
58. Miyazaki, T., Z.-J. Liu, A. Kawahara, Y. Minami, K. Yamada, Y. Tsujimoto, E. L. Barsoumian, R. M. Perlmutter, 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.
59. Kelley, K., B. H. Cochran, S. C. D., and P. Leder. 1983. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell 35:603.
60. Dani, C., J. M. Blanchard, M. Piechaczyk, S. El Sabouty, L. Marty, and P. Jeanteur. 1984. Extreme instability of myc mRNA in normal and transformed human cells. Proc. Natl. Acad. Sci. USA 81:7046.
61. Gotoh, N., M. Toyoda, and M. Shibuya. 1997. Tyrosine phosphorylation sites at amino acids 239 and 240 of She are involved in epidermal growth factor-induced mitogenic signalling that is distinct from ras/mitogen-activated protein kinase activation. Mol. Cell. Biol. 17:1824.
62. Hatakeyama, M., H. Mori, T. Doi, and T. Taniguchi. 1989. A restricted cytoplasmic region of IL-2 receptor β chain is essential for growth signal transduction but not for ligand binding and internalization. Cell 59:837.
63. Fujio, Y., K. Kunisada, H. Hirota, K. Yamauchi-Takihara, and T. Kishimoto, 1997. Signals through gp130 upregulate bcl-x gene expression via Stat1-binding cis-element in cardiac myocytes. J. Clin. Invest. 99:2892.
64. Catlett-Falcone, R., T. H. Landowski, M. M. Oshiro, J. Turkson, A. Levitzski, S. R., G. Ciliberto, L. Moscinski, J. L. Fernandez-Luna, G. Nunez, W. S. Dalton, et al. 1999. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 10:105.
65. Kiuchi, N., K. Nakajima, M. Ichiba, T. Fukada, M. Narimatsu, K. Mizuno, M. Hibi, and T. Hirano. 1999. Stat3 is required for the gp130-mediated full activation of the c-myc gene. J. Exp. Med. 189:63.
66. ras requires two domains of interleukin 2 receptor β subunit, the essential region for growth stimulation and lck-binding domain. J. Biol Chem 267:25423
67. Hatakeyama, M., A. Kawahara, H. Mori, H. Shibuya, and T. Taniguchi. 1992. c-fos gene induction by interleukin 2: identification of the critical cytoplasmic regions within the interleukin 2 receptor β chain. Proc. Natl. Acad. Sci. USA 89:2022.
68. ras. Trends Biol. Sci. 21:257.