Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: Involvement of STAT3 in anti-apoptosis

Immunity

Volumn 5, Issue 5, 1996, Pages 449-460

  Fukada, Toshiyuki ^a   Hibi, Masahiko ^a   Yamanaka, Yojiro ^a   Takahashi Tezuka, Mariko ^a   Fujitani, Yoshio ^a   Yamaguchi, Takuya ^a   Nakajima, Koichi ^a   Hirano, Toshio ^a  

^a OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; DNA FRAGMENT; GLYCOPROTEIN GP 130; GRANULOCYTE COLONY STIMULATING FACTOR; STAT3 PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL CYCLE; CELL GROWTH; CELL LINE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 0030292721     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80501-4     Document Type: Article

References (71)

1. Adachi, M., Fischer, E.H., Ihle, J., Imai, K., Jirik, F., Neel, B., Pawson, T., Shen, S.-H., Thomas, M., Ullrich, A., and Zhao, Z. (1996). Mammalian SH2-containing protein tyrosine phosphatases. Cell 85, 15.
2. Akira, S., Nishio, Y., Inoue, M., Wang, X.J., Wei, S., Matsusaka, T., Yoshida, K., Sudo, T., Naruto, M., and Kishimoto, T. (1994). Molecular cloning of APRF, a novel IFN-stimulated gene factor 3 p91-related transcription factor involved in the gp130-mediated signaling pathway. Cell 77, 63-71.
3. Ali, S., Chen, Z., Lebrun, J.-J., Vogel, W., Kharitonenkov, A., Kelly, P.A., and Ullrich, A. (1996). PTP1D is a positive regulator of the prolactin signal leading to β-casein promoter activation. EMBO J. 15, 135-142.
4. Bazan, J.F. (1990). Structural design and molecular evolution of a cytokine receptor superfamily. Proc. Natl. Acad. Sci. USA 87, 6934-6938.
5. Bennett, A.M., Tang, T.L., Sugimoto, S., Walsh, C.T., and Neel, B.G. (1994). Protein-tyrosine-phosphatase SHPTP2 couples platelet-derived growth factor receptor β to Ras. Proc. Natl. Acad. Sci. USA 91, 7335-7339.
6. Bennett, A.M., Housdorff, S.F., O'Reilly, A.M., Freeman, R.O., Jr., and Neel, B.G. (1996). Multiple requirements for SHPTP2 in epidermal growth factor-mediated cell cycle progression. Mol. Cell. Biol. 16, 1189-1202.
7. Boulton, T.G., Stahl, N., and Yancopoulos, G.D. (1994). Ciliary neurotrophic factor/leukemia inhibitory factor/interleukin 6/oncostatin M family of cytokines induces tyrosine phosphorylation of a common set of proteins overlapping those induced by other cytokines and growth factors. J. Biol. Chem. 269, 11648-11655.
8. Damen, J.E., Wakao, H., Miyajima, A., Krosl, J., Humphries, R.K., Cutler, R.L., and Krystal, G. (1995). Tyrosine 343 in the erythropoietin receptor positively regulates erythropoietin-induced cell proliferation and Stat5 activation. EMBO J. 14, 5557-5568.
9. Daniel, N.N., Pernis, A., and Rothman, P.B. (1995). Jak-STAT signaling induced by the v-abl oncogene. Science 269, 1875-1877.
10. Darnell, J.J., Kerr, I.M., and Stark, G.R. (1994). Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264, 1415-1421.
11. Durbin, J.E., Hachenmiller, R., Simon, M.C., and Levy, D.E. (1996). Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84, 443-450.
12. Freeman, R.M., Jr., Plutzky, J., and Neel, B.G. (1992). Identification of a human src homology 2-containing protein-tyrosine-phosphatase: a putative homolog of Drosophila corkscrew. Proc. Natl. Acad. Sci. USA 89, 11239-11243.
13. Friedmann, M.C., Migone, T.S., Russel, S.M., and Leonard, W.J. (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, 2077-2082.
14. Fujii, H., Nakagawa, Y., Schindler, U., Kawahara, A., Mori, H., Gouilleux, F.,Groner, B., Ihle, J.N., Minami, Y., Miyazaki, T., and Taniguchi, T. (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, 5482-5486.
15. Fujitani, Y., Nakajima, K., Kojima, H., Nakae, K., Takeda, T., and Hirano, T. (1994). Transcriptional activation of the IL-6 response element in the junB promoter is mediated by multiple Stat family proteins. Biochem. Biophys. Res. Commun. 202, 1181-1187.
16. Fukunaga, R., Ishizaka Ikeda, E., Pan, C.X., Seto, Y., and Nagata, S. (1991). Functional domains of the granulocyte colony-stimulating factor receptor. EMBO J. 10, 2855-2865.
17. Gobert, S., Chretein, S., Gouilleux, F., Muller, O., Pallard, C., Dusanter-Fourt, I., Groner, B., Lacombe, C., Gisselbrecht, S., and Mayeux, P. (1996). Identification of tyrosine residues within the intracellular domain of the erythropoietin receptor crucial for STAT5. EMBO J. 15, 2434-2441.
18. Haegeman, G., Content, J., Vorckaert, G., Derynck, R., Tavernier, J., and Fiers, W. (1986). Structural analysis of the sequence encoding for an inducible 26-kDa protein in human fibroblasts. Eur. J. Biochem. 159, 625-632.
19. Herbst, R., Carroll, R.M., Allard, J.D., Schilling, J., Raabe, T., and Simon, M.A. (1996). Daughter of Sevenless is a substrate of the phosphotyrosine phosphatase Corkscrew and functions during Sevenless signaling. Cell 85, 899-909.
20. Hibi, M., Murakami, M., Saito, M., Hirano,T., Taga, T., and Kishimoto, T. (1990). Molecular cloning and expression of an IL-6 signal transducer, gp130. Cell 63, 1149-1157.
21. Hibi, M., Nakajima, K., and Hirano, T. (1996). II-6 cytokine family and signal transduction: a model of cytokine system. J. Mol. Med. 74, 11-12.
22. Hirano, T. (1994). Interleukin-6. In The Cytokine Handbook, A. Thomson, ed. (London: Academic Press), pp. 145-168.
23. Hirano, T., Yasukawa, K., Harada, H., Taga, T., Watanabe, Y., Matsuda, T., Kashiwamura, S., Nakajima, K., Koyama, K., Iwamatsu, A., Tsunasawa, S., Matsui, H., Takahara, Y., Taniguchi, T., and Kishimoto, T. (1986). Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature 324, 73-76.
24. Hirano, T., Matsuda, T., and Nakajima, K. (1994). Signal transduction through gp130 that is shared among the receptors for the interleukin 6 related cytokine subfamily. Stem Cells 12, 262-277.
25. Ihle, J.N. (1995). Cytokine receptor signaling. Nature 377, 591-594.
26. Ihle, J.N. (1996). STATs: signal transducers and activators of transcription. Cell 84, 331-334.
27. Ip, N.Y., Nye, S.H., Boulton, T.G., Davis, S., Taga, T., Li, Y., Birren, S.J., Yasukawa, K., Kishimoto, T., Anderson, D.J., Stahl, N., and Yancopoulos, G.D. (1992). CNTF and LIF act on neuronal cells via shared signaling pathways that involve the IL-6 signal transducing receptor component gp130. Cell 69, 1121-1132.
28. Kaplan, M.H., Schindler, U., Smiley, S.T., and Grusby, M.J. (1996a). Stat6 is required for mediating responses to IL-4 and for the development of Th2 cells. Immunity 4, 313-319.
29. Kaplan, M.H., Sun, Y.-L., Hoey, T., and Grusby, M.J. (1996b). Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 382, 174-177.
30. Kinoshita, T., Yokota, T., Arai, K., and Miyajima, A. (1995). Suppression of apoptotic death in hematopoietic cells by signaling through the IL-3/GM-CSF receptors. EMBO J. 14, 266-275.
31. Klingmuller, U., Lorenz, U., Cantley, L.C., Neel, B.G., and Lodish, H.F. (1995). Specific recruitment of SH-PTP1 to the erythropoietin receptor causes inactivation of JAK2 and termination of proliferative signals. Cell 80, 729-738.
32. Kumar, G., Gupta, S., Wang, S., and Nel, A.E. (1994). Involvement of Janus kinases, p52shc, Raf-1, and MEK-1 in the IL-6-induced mitogen-activated protein kinase cascade of a growth-responsive B cell line. J. Immunol. 153, 4436-4447.
33. Li, W., Nishimura, R., Kashishian, A., Batzer, A.G., Kim, W.J., Cooper, J.A., and Schlessinger, J. (1994). A new function for a phosphotyrosine phosphatase: linking GRB2-Sos to a receptor tyrosine kinase. Mol. Cell. Biol. 14, 509-517.
34. Lowenstein, E.J., Daly, R.J., Batzer, A.G., Li, W., Margolis, B., Lammers, R., Ullrich, A., Skolnik, E.Y., Bar-Sagi, D., and Schlessinger, J. (1992). The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70, 431-442.
35. Lutticken, C., Wegenka, U.M., Yuan, J., Buschmann, J., Schindler, C., Ziemiecki, A., Harpur, A.G., Wilks, A.F., Yasukawa, K., Taga, T., Kishimoto, T., Barbirri, G., Pellegrini, S., Sendtner, M., Heinrich, P.C., and Horn, F. (1994). Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130. Science 263, 89-92.
36. Matsuda, T., Yamanaka, Y., and Hirano, T. (1994). Interleukin-6-induced tyrosine phosphorylation of multiple proteins in murine hematopoietic lineage cells. Biochem. Biophys. Res. Commun. 200, 821-828.
37. Matthews, R.J., Bowne, D.B., Flores, E., and Thomas, M.L. (1992). Characterization of hematopoietic intracellular protein tyrosine phosphatases: description of a phosphatase containing an SH2 domain and another enriched in proline-, glutamic acid-, serine-, and threonine-rich sequences. Mol. Cell. Biol. 12, 2396-2405.
38. Meraz, M.A., White, J.M., Sheedhan, K.C.F., Bach, E.A., Rodig, S.J., Dighe, A.S., Kaplan, D.H., Riley, J.K., Gleenlund, A.C., Campbell, D., Carver-Moore, K., DuBois, R.N., Clark, R., Aguet, M., and Schreiber R.D. (1996). Targeted disruption of the mouse Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84, 431-442.
39. Migone, T.S., Lin, J.X., Cereseto, A., Mulloy, J.C., O'Shea, J.J., Franchini, G., and Leonard, W.J. (1995). Constitutively activated Jak-STAT pathway in T cells transformed with HTLV-I. Science 269, 79-81.
40. Miyazaki, T., Liu, Z.J., Kawahara, A., Minami, Y., Yamada, K., Tsujimoto, Y., Barsoumian, E.L., Permutter, R.M., and Taniguchi, T. (1995). Three distinct IL-2 signaling pathways mediated by bcl-2, c-myc, and lck cooperate in hematopoietic cell proliferation. Cell 81, 223-231.
41. Mui, A.L., Wakao, H., Kinoshita, T., Kitamura, T., and Miyajima, A. (1996). Suppression of interleukin-3-induced gene expression by a C-terminal truncated Stat5: role of Stat5 in proliferation. EMBO J. 15, 2425-2433.
42. Murakami, M., Narazaki, M., Hibi, M., Yawata, H., Yasukawa, K., Hamaguchi, M., Taga, T., and Kishimoto, T. (1991). Critical cytoplasmic region of the interleukin 6 signal transducer gp130 is conserved in the cytokine receptor family. Proc. Natl. Acad. Sci. USA 88, 11349-11353.
43. Murakami, M., Hibi, M., Nakagawa, N., Nakagawa, T., Yasukawa, K., Yamanishi, K., Taga, T., and Kishimoto, T. (1993). IL-6-induced homodimerization of gp130 and associated activation of a tyrosine kinase. Science 260, 1808-1810.
44. Nakajima, K., Matsuda, T., Fujitani, Y., Kojima, H., Yamanaka, Y., Nakae, K., Takeda, T., and Hirano, T. (1995). Signal transduction through IL-6 receptor: involvement of multiple protein kinases, stat factors, and a novel H7-sensitive pathway. Ann. NY Acad. Sci. 762, 55-70.
45. Nakajima, K., Yamanaka, Y., Nakae, K., Kojima, H., Ichiba, M., Kiuchi, N., Kitaoka, T., Fukada, T., Hibi, M., and Hirano, T. (1996). A central rolefor Stat3 in IL-6-induced regulation of growth and differentiation in M1 leukemia cells. EMBO J. 15, 3651-3658.
46. Narazaki, M., Witthuhn, B.A., Yoshida, K., Silvennoinen, O., Yasukawa, K., Ihle, J.N., Kishimoto, T., and Taga, T. (1994). Activation of JAK2 kinase mediated by the interleukin 6 signal transducer gp130. Proc. Natl. Acad. Sci. USA 91, 2285-2289.
47. Noguchi, T., Matozaki, T., Horita, K., Fujioka, Y., and Kasuga, M. (1994). Role of SH-PTP2, a protein-tyrosine phosphatase with Src homology 2 domains, in insulin-stimulated Ras activation. Mol. Cell. Biol. 14, 6674-6682.
48. Pennica, D., Shaw, K.J., Swanson, T.A., Moore, M.W., Shelton, D.L., Zioncheck, K.A., Rosenthal, A., Taga, T., Paoni, N.F., and Wood, W.I. (1995). Cardiotrophin-1: biological activities and binding to the leukemia inhibitory factor receptor/gp130 signaling complex. J. Biol. Chem. 270, 10915-10922.
49. Perkins, L.A., Larsen, I., and Perrimon, N. (1992). corkscrew encodes a putative protein tyrosine phosphatase that functions to transduce the terminal signal from the receptor tyrosine kinase torso. Cell 70, 225-236.
50. Plutzky, J., Neel, B.G., and Rosenberg, R.D. (1992). Isolation of a src homology 2-containing tyrosine phosphatase. Proc. Natl. Acad. Sci. USA 89, 1123-1127.
51. Raabe, T., Riesgo-Escovar, J., Liu, X., Bausenwein, B.S., Deak, P., Maröy, P., and Hafen, E. (1996). DOS, a novel pleckstrin homology domain-containing protein required for signal transduction between Sevenless and Ras1 in Drosophila. Cell 85, 911-920.
52. Sadowski, H.B., Shuai, K., Darnell, J.E., Jr., and Gilman, M.Z. (1993). A common nuclear signal transduction pathway activated by growth factor and cytokine receptors. Science 261, 1739-1744.
53. Sato, N., Sakamaki, K., Terada, N., Arai, K., and Miyajima, A. (1993). Signal transduction by the high-affinity GM-CSF receptor: two distinct cytoplasmic regions of the common β subunit responsible for different signaling. EMBO J. 12, 4181-4189.
54. Sehgal, P.B., Grieninger, G., and Tosato, G., eds. (1989). Regulation of the acute phase an immune responses: interleukin-6. Ann. NY Acad. Sci. 557, 1-580.
55. Shen, S.H., Bastien, L., Posner, B.I., and Chretien, P. (1991). A protein-tyrosine phosphatase with sequence similarity to the SH2 domain of the protein-tyrosine kinases Nature 352, 736-739. Erratum: Nature 353, 868.
56. Shibuya, H., Yoneyama, M., Ninomiya-Tsuji, J., Matsumoto, K., and Taniguchi, T. (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.
57. Shimoda, K., van Deursen, J., Sangster, M.Y., Sarwar, S.R., Carson, R.T., Tripp, R.A., Chu, C., Quelle, F.W., Nosaka, T., Vignali, D.A.A., Doherty, P.C., Grosveld, G., Paul, W., and Ihle, J.N. (1996). Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 380, 630-633.
58. Stahl, N., Boulton. T.G., Farruggella, T., Ip, N.Y., Davis, S., Witthuhn, B.A., Quelle, F.W., Silvennoinen, O., Barbieri, G., Pellegrini, S., Ihle, J.N., and Yancopoulos, G.D. (1994). Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6β receptor components. Science 263, 92-95.
59. Stahl, N., Farruggella, T.J., Boulton, T.G., Zhong, Z., Darnell, J.J., and Yancopoulos, G.D. (1995). Choice of STATs and other substrates specified by modular tyrosine based motifs in cytokine receptors. Science 267, 1349-1353.
60. Taga, T., Hibi, M., Hirata, Y., Yamasaki, K., Yasukawa, K., Matsuda, T., Hirano, T., and Kishimoto, T. (1989). Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130. Cell 58, 573-581.
61. Takeda, K., Tanaka, T., Shi, W., Matsumoto, M., Minami, M., Kashiwamura, S., Nakanishi, K., Yoshida, N., Kishimoto, T., and Akira, S. (1996). Essential role of Stat6 in IL-4 signaling. Nature 380, 627-630.
62. Tang, T.L., Freeman, R.M., Jr., O'Reilly, A.M., Neel, B.G., and Sokol, S.Y. (1995). The SH2-containing protein-tyrosine phosphatase SH-PTP2 is required upstream of MAP kinase for early Xenopus development. Cell 80, 473-483.
63. Thierfelder, W.E., van Deursen, J.M., Yamamoto, K., Tripp, R.A., Sarawar, S.R., Carson, R.T., Sangster, M.Y., Vignali, D.A.A., Doherty, P.C., Grosveld, G.G., and Ihle, J.N. (1996). Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells. Nature 382, 171-174.
64. Van Snick, J. (1990). Interleukin-6: an overview. Annu. Rev. Immunol. 8, 253-278.
65. Yamanaka, Y., Nakajima, K., Fukada, T., Hibi, M., and Hirano, T. (1996). Differentiation and growth arrest signals are generated through the cytoplasmic region of gp130 that is essential for Stat3 activation. EMBO J. 15, 1557-1565.
66. Yamasaki, K., Taga, T., Hirata, Y., Yawata, H., Kawanishi, Y., Seed, B., Taniguchi, T., Hirano, T., and Kishimoto, T. (1988). Cloning and expression of the human interleukin-6 (BSF-2/IFNβ2) receptor. Science 241, 825-828.
67. Yan, R., Small, S., Desplan, C., Dearolf, C.R., and Darnell, J.E. (1996). Identification of a Stat gene that functions in Drosophila development. Cell 84, 421-430.
68. Yi, T., Mui, A.L., Krystal, G., and Ihle, J.N. (1993). Hematopoietic cell phosphatase associates with the interleukin-3(IL-3) receptor β chain and down-regulates IL-3-induced tyrosine phosphorylation and mitogenesis. Mol. Cell. Biol. 13, 7577-7586.
69. Yin, T., Taga, T., Tsang, M.L., Yasukawa, K., Kishimoto, T., and Yang, Y.C. (1993). Involvement of IL-6 signal transducer gp130 in IL-11-mediated signal transduction. J. Immunol. 151, 2555-2561.
70. Yu, C.L., Meyer, D.J., Campbell, G.S., Larner, A.C., Carter-Su, C., Schwartz, J., and Jove, R. (1995). Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 269, 81-83.
71. Zilberstein, A., Ruggieri, R., Korn, J.H., and Revel, M. (1986). Structure and expression of cDNA and genes for human interferon-β2, a distinct species inducible by growth-stimulatory cytokines. EMBO J. 5, 2529-2537.