A membrane-proximal region of the interleukin-2 receptor γc chain sufficient for Jak kinase activation and induction of proliferation in T cells

Molecular and Cellular Biology

Volumn 16, Issue 1, 1996, Pages 309-317

  Nelson, Brad H ^a   Lord, James D ^b   Greenberg, Philip D ^b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; RECEPTOR SUBUNIT;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MEMBRANE STRUCTURE; MITOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE ACTIVATION;

AMINO ACID SEQUENCE; ANIMAL; ENZYME ACTIVATION; GENES, FOS; GENES, MYC; HUMAN; LIGANDS; LYMPHOCYTE ACTIVATION; MICE; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN-TYROSINE KINASE; RECEPTORS, GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; RECEPTORS, INTERLEUKIN-2; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, NON-P.H.S.; SUPPORT, U.S. GOV'T, P.H.S.; T-LYMPHOCYTES;

EID: 0029655803     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.1.309     Document Type: Article

References (57)

1. Arima, N., M. Kamio, K. Imada, T. Hori, T. Hattori, M. Tsudo, M. Okuma, and T. Uchiyama. 1992. Pseudo-high affinity interleukin 2 (IL-2) receptor lacks the third component that is essential for functional IL-2 binding and signaling. J. Exp. Med. 176:1265-1272.
2. Asao, H., T. Takeshita, N. Ishii, S. Kumaki, M. Nakamura, and K. Sugamura. 1993. Reconstitution of functional interleukin 2 receptor complexes on fibroblastoid cells: involvement of the cytoplasmic domain of the gamma chain in two distinct signaling pathways. Proc. Natl Acad Sci. USA 90:4127-4131.
3. Asao, H., N. Tanaka, N. Ishii, M. Higuchi, T. Takeshita, M. Nakamura, T. Shirasawa, and K. Sugamura. 1994. Interleukin 2-induced activation of JAK3: possible involvement in signal transduction for c-myc induction and cell proliferation FEBS Lett 351:201-206.
4. Boussiotis, V. A., D. L. Barber, T. Nakarai, G. J. Freeman, J. G. Gribben, G. M. Bernstein, A. D. D'Andrea, J. Ritz, and L. M. Nadler. 1994 Prevention of T cell anergy by signaling through the gamma c chain of the IL-2 receptor. Science 266:1039-1042.
5. Cao, X., C. A. Kozak, Y.-J. Liu, M. Noguchi, E. O'Connell, and W. J. Leonard. 1993. Characterization of cDNAs encoding the murine interleukin 2 receptor (IL-2R) gamma chain chromosomal mapping and tissue specificity of IL-2R gamma chain expression. Immunology 90:8464-8468
6. 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, W. E. Paul, S. I. Katz, P. E. Love, and W. J. Leonard. 1995. Defective lymphoid development in mise lacking expression of the common cytokine receptor gamma chain. Immunity 2:223-238
7. Claesson-Welsh, L. 1994. Platelet-derived growth factor receptor signals J. Biol. Chem. 269:32023-32026.
8. Cornelis, S., I. Fache, J. Van der Heyden, Y. Guisez, J. Tavernier, R. Devos, W. Fiers, and G. Plaetinck. 1995. Characterization of critical residues in the cytoplasmic domain of the human interleukin-5 receptor alpha chain required for growth signal transduction. Eur. J. Immunol 25:1857-1864.
9. Crosier, K. E., G. G. Wong, B. Mathey-Prevot, D. G. Nathan, and C. A. Sieff. 1991 A functional isoform of the human granulocyte/macrophage colony-stimulating factor receptor has an unusual cytoplasmic domain. Proc Natl. Acad. Sci. USA 88:7744-7748
10. DiSanto, J. P., W. Muller, D. Guy-Grand, A. Fischer, and K. Rajewsky. 1995 Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain. Proc. Natl. Acad. Sci USA 92:377-381.
11. Fujii, H., Y. Nakagawa, U. Schindler, A. Kawahara, H. Mori, F. Gouilleuv, B. Groner, J. Ihle, Y. Minami, T. Miyazaki, and T. Taniguchi. 1995. Activation of stat5 by interleukin 2 requires a carboxyl-terminal region of the interleukin 2 receptor beta chain but is not essential for the proliferative signal transmission. Proc Natl. Acad Sci. USA 92:5482-5486.
12. Gearing, D. P., J. A. King, N. M. Gough, and N. A. Nicola. 1989. Expression cloning of a receptor for human granulocyte-macrophage colony-stimulating factor. EMBO J 8:3667-3676.
13. Giri, J. G., M. Ahdieh, J. Eisenman, K. Shanebeck, K. Grabstein, S. Kumaki, A. Namen, L. S. Park, D. Cosman, and K. Anderson. 1994. Utilization of the beta and gamma chains of the IL-2 receptor by the novel cytokine IL-15 EMBO J. 13:2822-2830.
14. Gunning, P., J. Leavitt, G. Muscat, S. Ng, and L. Kedes. 1987. A human beta-actin expression vector system directs high-level accumulation of antisense transcripts. Proc. Natl Acad Sci. USA 84:4831-4835.
15. Hara, T., and A. Miyajima. 1992. Two distinct functional high affinity receptors for mouse interleukin-3 (IL-3) EMBO J 11:1875-1884.
16. Harada, N., and B. H. Nelson. Unpublished data.
17. Hatakeyama, M., T. Kono, N. Kobayashi, A. Kawahara, S. D. Levin, R. M. Perlmutter, and T. Taniguchi. 1991. Interaction of the IL-2 receptor with the src-family kinase p56lck identification of novel intermolecular association. Science 252:1523-1528.
18. Hatakeyama, M., H. Mori, T. Doi, and T. Taniguchi. 1989. A restricted cytoplasmic region of IL-2 receptor beta chain is essential for growth signal transduction but not for ligand binding and internalization. Cell 59:837-845
19. Hatakeyama, M., M. Tsudo, S. Minamoto, T. Kono, T. Doi, T. Miyata, M. Miyasaka, and T. Taniguchi. 1989. Interleukin-2 receptor beta chain gene: generation of three receptor forms by cloned human alpha and beta chain cDNA's. Science 244:551-556
20. Hayashida, K., T. Kitamura, D. M. Gorman, K.-I. Arai, T. Yokota, and A. Miyajima. 1990 Molecular cloning of a second subunit of the receptor for human granulocyte-macrophage colony-stimulating factor (GM-CSF): reconstitution of a high-affinity GM-CSF receptor Proc Natl Acad. Sci USA 87:9655-9659.
21. Ho, S., H. Hunt, R. Horton, J. Pullen, and L. Pease. 1989 Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
22. Ishii, N., H. Asao, Y. Kimura, T. Takeshita, M. Nakamura, S. Tsuchiya, T. Konno, M. Maeda, T. Uchiyama, and K. Sugamura. 1994. Impairment of ligand binding and growth signaling of mutant IL-2 receptor gamma chains in patients with X-linked severe combined immunodeficiency. J. Immunol. 153:1310-1317.
23. Kitamura, T., N. Sato, K. Arai, and A. Miyajima. 1991. Expression cloning of the human IL-3 receptor cDNA reveals a shared beta subunit for the human IL-3 and GM-CSF receptors Cell 66:1165-1174.
24. Koch, C. A., D. Anderson, M. F. Moran, C. Ellis, and T. Pawson. 1991. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins Science 252:668-674.
25. Kondo, M., T. Takeshita, M. Higuchi, M. Nakamura, T. Sudo, S. Nishikawa, and K. Sugamura. 1994. Functional participation of the IL-2 receptor gamma chain in IL-7 receptor complexes. Science 263:1453-1454.
26. Kondo, M., T. Takeshita, N. Ishii, M. Nakamura, S. Watanabe, K. Arai, and K. Sugamura. 1993. Sharing of the interleukin-2 (IL-2) receptor gama chain between receptors for IL-2 and IL-4. Science 262:1874-1877.
27. Lin, J., T. Migone, M. Tsang, M. Friedmann, J. A. Wetherbee, L. Zhou, A. Yamauchi, E. T. Bloom, J. Mietz, S. John, and W. J. Leonard. 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 2:331-339.
28. Lord, J. D., B. H. Nelson, and P. D. Greenberg. Unpublished data
29. Merida, I., P. Williamson, W. A. Kuziel, W. C. Greene, and G. N. Gaulton. 1993. The serine-rich cytoplasmic domain of the interleukin-2 receptor beta chain is essential for interleukin-2-dependent tyrosine protein kinase and phosphatidylinositol-3-kinase activation. J. Biol. Chem. 268:6765-6770.
30. 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 2:89-100
31. Miyazaki, T., A. Kawahara, H. Fujii, Y. Nakagawa, Y. Minami, Z. Liu, I. Oishi, O. Silvennoinen, B. Witthuhn, and J. Ihle. 1994. Functional activation of Jak1 and Jak3 by selective association with IL-2 receptor subunits. Science 266:1045-1047
32. 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 81:223-231.
33. Murata, Y., S. Takaki, M. Migita, Y. Kikuchi, A. Tominaga, and K. Takatsu. 1992. Molecular cloning and expression of the human interleukin 5 receptor. J Exp Med. 175:341-351.
34. 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 beta- and gamma-chain cytoplasmic domains is required for signalling. Nature (London) 369:330-333.
35. Nelson, B. H., J. D. Lord, and P. D. Greenberg. 1994. Cytoplasmic domains of the interleukin-2 receptor beta and gamma chains mediate the signal for T-cell proliferation. Nature (London) 369:333-336.
36. Noguchi, M., Y. Nakamura, S. M. Russell, S. F. Ziegler, M. Tsang, X. Cao, and W. J. Leonard. 1993. Interleukin-2 receptor gamma chain: a functional component of the interleukin-7 receptor Science 262:1877-1880.
37. 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 gamma chain mutation results in X-linked severe combined immunodeficiency in humans. Cell 73:147-157.
38. Park, L. S., U. Martin, R. Sorensen, S. Luhr, P. J. Morrissey, D. Cosman, and A. Larsen. 1992. Cloning of the low-affinity murine granulocyte-macrophage colony-stimulating factor receptor and reconstitution of a high-affinity receptor complex. Proc. Natl. Acad. Sci. USA 89:4295-4299
39. Peschon, J. J., P. J. Morrissey, K. H. Grabstein, F. J. Ramsdell, E. Maraskovsky, B. C. Gliniak, L. S. Park, S. F. Ziegler, D. E. Williams, C. B. Ware, et al. 1994. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice J. Exp. Med. 180:1955-1960
40. Polutskaya, A., Y. Zhao, M. B. Lilly, and A. S. Kraft. 1994. Mapping the intracytoplasmic regions of the alpha granulocyte-macrophage colony-stimulating factor receptor necessary for cell growth regulation. J Biol. Chem. 269:14607-14613.
41. Puck, J. M., S. M. Deschenes, J. C. Porter, A. S. Dutra, C. J. Brown, H. F. Willard, and P. S. Henthorn, 1993. The interleukin-2 receptor gamma chain maps to Xq13.1 and is mutated in X-linked severe combined immunodeficiency, SCIDX1 Hum Mol. Genet. 2:1099-1104.
42. c chain of the receptor for granulocyte-macrophage colony-stimulating factor, and its activation requires the membrane-proximal region. Mol. Cell. Biol. 14:4335-4341
43. Russell, S., J. Johnston, M. Noguchi, M. Kawamura, C. Bacon, M. Friedmann, M. Berg, D. McVicar, B. Witthuhn, and O. Silvennoinen. 1994. Interaction of IL-2R beta and gamma c chains with Jak1 and Jak3 implications for XSCID and XCID. Science 266:1042-1045
44. Russell, S. M., A. D. Keegan, N. Harada, Y. Nakamura, M. Noguchi, P. Leland, M. C. Friedmann, A. Miyajima, R. K. Puri, W. E. Paul, and W. J. Leonard. 1993. Interleukin-2 receptor gamma chain: a functional component of the interleukin-4 receptor Science 262:1880-1883.
45. Satoh, T., Y. Minami, T. Kono, K. Yamada, A. Kawahara, T. Taniguchi, and Y. Kaziro. 1992. Interleukin 2-induced activation of ras requires two domains of interleukin 2 receptor beta subunit, the essential region for growth stimulation and lck-binding domain. J. Biol. Chem. 267:25423-25427.
46. Schorle, H., T. Holtschke, T. Hunig, A. Schimpl, and I. Horak. 1991. Development and function of T cells in mice rendered interleukin-2 deficient by gene targeting. Nature (London) 352:621-624.
47. 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 70:57-67.
48. Sugamura, K., T. Takeshita, H. Asao, S. Kumaki, K. Ohbo, K. Ohtani, and M. Nakamura. 1990. IL-2-induced signal transduction: involvement of tyrosine kinase and IL-2 receptor gamma chain Lymphokine Res. 9:539-542.
49. Takaki, S., H. Kanazawa, M. Shiiba, and K. Takatsu. 1994. A critical cytoplasmic domain of the interleukin-5 (IL-5) receptor alpha chain and its function in IL-5-mediated growth signal transduction Mol. Cell. Biol. 14: 7404-7413.
50. Takaki, S., A. Tominaga, Y. Hitoshi, S. Mita, E. Sonoda, N. Yamaguchi, and K. Takatsu. 1990 Molecular cloning and expression of the murine interleukin-5 receptor EMBO J. 9:4367-4374.
51. Takeshita, T., H. Asao, K. Ohtani, N. Ishii, S. Kumaki, N. Tanaka, H. Munakata, M. Nakamura, and K. Sugamura. 1992 Cloning of the gamma chain of the human IL-2 receptor Science 257:379-382.
52. Takeshita, T., H. Asao, J. Suzuki, and K. Sugamura. 1990. An associated molecule, p64, with high-affinity interleukin 2 receptor Int. Immunol. 2:477-480
53. Takeshita, T., K. Ohtani, H. Asao, S. Kumaki, M. Nakamura, and K. Sugamura. 1992. An associated molecule, p64 with IL-2 receptor beta chain. Its possible involvement in the formation of the functional intermediate-affinity IL-2 receptor complex. J. Immunol 148:2154-2158.
54. Tanaka, N., H. Asao, K. Ohbo, N. Ishii, T. Takeshita, M. Nakamura, H. Sasaki, and K. Sugamura. 1994. Physical association of Jak1 and Jak2 tyrosine kinases with the interleukin 2 receptor beta and gamma chains. Proc. Natl Acad. Sci. USA 91:7271-7275.
55. von Freeden-Jeffry, U., P. Vieira, L. A. Lucian, T. McNeil, S. E. Burdach, and R. Murray. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med 181:1519-1526.
56. Voss, S. D., P. M. Sondel, and R. J. Robb. 1992. Characterization of the interleukin 2 receptors (IL-2R) expressed on human natural killer cells activated in vivo by IL-2: association of the p64 IL-2R gamma chain with the IL-2R beta chain in functional intermediate-affinity IL-2R. J. Exp. Med. 176:531-541.
57. Yaseen, N. R., J. Park, T. Kerppola, T. Curran, and S. Sharma. 1994 A central role for Fos in human B- and T-cell NFAT (nuclear factor of activated T cells): an acidic region is required for in vitro assembly. Mol Cell. Biol. 14:6886-6895.