Signaling through Gp130: Toward a general scenario of cytokine action

Growth Factors

Volumn 17, Issue 2, 1999, Pages 81-91

  Fukada, Toshiyuki ^a   Yoshida, Yuichi ^a   Nishida, Keigo ^a   Ohtani, Takuya ^a   Shirogane, Takahiro ^a   Hibi, Masahiko ^a   Hirano, Toshio ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Cytokine; Gab family; Gp130; Interleukin 6; JAK; SHP 2; STAT

Indexed keywords

CYTOKINE; GLYCOPROTEIN GP 130; INTERLEUKIN 6; RECEPTOR SUBUNIT;

ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL SURVIVAL; HEMATOPOIESIS; IMMUNE RESPONSE; INFLAMMATION; PLEIOTROPY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0033431790     PISSN: 08977194     EISSN: None     Source Type: Journal    
DOI: 10.3109/08977199909103518     Document Type: Article

References (82)

1. 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 beta-casein promoter activation. EMBO. J. 15, 135-142.
2. Bennett, A.M., Hausdorff, S.F., O'Reilly, A.M., Freeman, R.M. and Neel, B.G. (1996) Multiple requirements for SHPTP2 in epidermal growth factor-mediated cell cycle progression. Mol. Cell Biol. 16, 1189-1202.
3. Besser, D., Bromberg, J.F., Darnell, J.J.E. and Hanafusa, H. (1999) A single amino acid substitution in the v-Eyk intracellular domain results in activation of STAT3 and enhances cellular transformation. Molecular and Cellular Biology 19, 1401-1409.
4. Boeuf, H., Hauss, C., Graeve, F.D., Baran, N. and Kedinger, C. (1997) Leukemia inhibitory factor-dependent transcriptional activation in embryonic stem cells. J. Cell Biol. 138, 1207-1217.
5. Bonni, A., Sun, Y., Nadal-Vicens, M., Bhatt, A., Frank, D.A., Rozovsky, I., Stahl, N., Yancopoulos, G.D. and Greenberg, M.E. (1997) Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278, 477-483.
6. 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.
7. Bromberg, J.F., Horvath, C.M., Besser, D., Lathem, W.W. and Darnell, J.E.J. (1998) Stat3 activation is required for cellular transformation by v-src. Mol. Cell Biol. 18, 2553-2558.
8. Carpenter, L.R., Farruggella, T.J., Symes, A., Karow, M.L., Yancopoulos, G.D. and Stahl, N. (1998) Enhancing leptin response by preventing SH2-containing phosphatase 2 interaction with Ob receptor. Proc. Natl. Acad. Sci. USA 95, 6061-6066.
9. Catlett-Falcone, R., Landowski, T., Oshiro, M., Turkson, J., Levitzki, A., Savino, R., Ciliberto, G., Moscinski, L., Fernandez-Luna, J., Nunez, G., Dalton, W. and Jove, R. (1999) Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1, 105-115.
10. Chung, C.D., Liao, J., Liu, B., Rao, X., Jay, P., Berta, P. and Shuai, K. (1997) Specific inhibition of Stat3 signal transduction by PIAS3. Science 278, 1803-1805.
11. Darnell Jr., J.E. (1997) STATs and gene regulation. Science 277, 1630-1635.
12. Endo, T.A., Masuhara, M., Yokouchi, M., Suzuki, R., Sakamoto, H., Mitsui, K., Matsumoto, A., Tanimura, S., Ohtsubo, M., Misawa, H., Miyazaki, T., Leonor, N., Taniguchi, T., Fujita, T., Kanakura, Y., Komiya, S. and Yoshimura, A. (1997) A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387, 921-924.
13. Fujitani, Y., Hibi, M., Fukada, T., Takahashi Tezuka, M., Yoshida, H., Yamaguchi, T., Sugiyama, K., Yamanaka, Y., Nakajima, K. and Hirano, T. (1997) An alternative pathway for STAT activation that is mediated by the direct interaction between JAK and STAT. Oncogene 14, 751-761.
14. Fukada, T., Hibi, M., Yamanaka, Y., Takahashi-Tezuka, M., Fujitani, Y., Yamaguchi, T., Nakajima, K. and Hirano, T. (1996) Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: involvement of STAT3 in anti-apoptosis. Immunity 5, 449-460.
15. Fukada, T., Ohtani, T., Yoshida, Y., Shirogane, T., Nishida, K., Nakajima, K., Hibi, M. and Hirano, T. (1998) STAT3 orchestrates contradictory signals in cytokine-induced G1 to S cell-cycle transititon. EMBO. J. 17, 6670-6677.
16. Gerhartz, C., Heesel, B., Sasse, J., Hemmann, U., Landgraf, C., Schneider-Mergener, J., Horn, F., Heinrich, P.C. and Graeve, L. (1996) Differential activation of acute phase response factor/STAT3 and STAT1 via the cytoplasmic domain of the interleukin 6 signal transducer gp130. I. Definition of a novel phosphotyrosine motif mediating STAT1 activation. J. Biol. Chem. 271, 12991-12998.
17. Gu, H., Pratt, J.C., Burakoff, S.J. and Neel, B.G. (1998) Cloning of p97/Gab2, the major SHP2-binding protein in hematopoietic cells, reveals a novel pathway for cytokine-induced gene activation. Molecular Cell 2, 729-740.
18. Guschin, D., Rogers, N., Briscoe, J., Witthuhn, B., Watling, D., Horn, F., Pellegrini, S., Yasukawa, K., Heinrich, P., Stark, G.R. et al. (1995) A major role for the protein tyrosine kinase JAK1 in the JAK/STAT signal transduction pathway in response to interleukin-6. EMBO. L. 14, 1421-1429.
19. Hemmann, U., Gerhartz, C., Heesel, B., Sasse, J., Kurapkat, G., Grotzinger, J., Wollmer, A., Zhong, Z., Darnell Jr., J.E., Graeve, L., Heinrich, P.C. and Horn, F. (1996) Differential activation of acute phase response factor/Stat3 and Stal1 via the cytoplasmic domain of the interleukin 6 signal transducer gp130. II. Src homology SH2 domains define the specificity of stat factor activation. J. Biol. Chem. 271, 12999-13007.
20. Herbst, R., Carroll, P.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.
21. Hibi, M. and Hirano, T. (1998) Signal transduction through cytokine receptors (In Process Citation). Int. Rev. Immunol. 17, 75-102.
22. Hirano, T. (1998) Interleukin 6 and its receptor: Ten years later. Intern. Rev. Immunol. 16, 249-284.
23. Hirano, T., Nakajima, K. and Hibi, M. (1997) Signaling mechanisms through gp130: A model for the cytokine system. Cytokine & Growth Factor Reviews 8, 241-252.
24. Holgado-Madruga, M., Emlet, D.R., Moscatello, D.K., Godwin, A.K. and Wong, A.J. (1996) A Grb2-associated docking protein in EGF-and insulin-receptor signalling. Nature 379, 560-564.
25. Ichiba, M., Nakajima, K., Yamanaka, Y., Kiuchi, N. and Hirano, T. (1998) Autoregulation of the Stat3 gene through cooperation with a cAMP-responsive element-binding protein. J. Biol. Chem. 273, 6132-6138.
26. Ihara, S., Nakajima, K., Fukada, T., Hibi, M., Nagata, S., Hirano, T. and Fukui, Y. (1997) Dual control of neurite out-growth by STAT3 and MAP kinase in PC12 cells stimulated with interleukin-6. EMBO. J. 16, 5345-5352.
27. Ihle, J.N., Witthuhn, B.A., Quelle, F.W., Yamamoto, K., Thierfelder, W.E., Kreider, B. and Silvennoinen, O. (1994) Signaling by the cytokine receptor superfamily: JAKs and STATs. Trends Biochem. Sci. 19, 222-227.
28. Ingham, R.J., Holgado-Madruga, M., Siu, C., Wong, A.J. and Gold, M.R. (1998) The Gab1 protein is a docking site for multiple proteins involved in signaling by the B cell antigen receptor. J. Biol. Chem. 273, 30630-30637.
29. Jain, N., Zhang, T., Fong, S.L., Lim, C.P. and Cao, X. (1998) Repression of Stat3 activity by activation of mitogen-activated protein kinase (MAPK). Oncogene 17, 3157-3167.
30. Kaplan, M.H., Daniel, C., Schindler, U. and Grusby, M.J. (1998) Stat proteins control lymphocyte proliferation by regulating p27Kip1 expression. Mol. Cell Biol. 18, 1996-2003.
31. Kim, H., Hawley, T.S., Hawley, R.G. and Baumann, H. (1998) Protein tyrosine phosphatase 2 (SHP-2) moderates signaling by gp130 but is not required for the induction of acute-phase plasma protein genes in hepatic cells. Mol. Cell Biol. 18, 1525-1533.
32. Kiuchi, N., Nakajima, K., Ichiba, M., Fukada, T., Narimatsu, M., Mizuno, K., Hibi, M. and Hirano, T. (1999) STAT3 is required for the gp130-mediated full activation of the c-myc gene. J. Exp. Med. 189, 63-73.
33. 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.
34. 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.
35. Liu, Z.G., Hsu, H., Goeddel, D.V. and Karin, M. (1996) Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87, 565-576.
36. Liu, B., Liao, J., Rao, X., Kushner, S.A., Chung, C.D., Chang, D.D. and Shuai, K. (1998) Inhibition of Stal1-mediated gene activation by PIAS1. Proc. Natl. Acad. Sci. USA 95, 10626-10631.
37. Luo, H., Hanratty, W.P. and Dearolf, C.R. (1995) An amino acid substitution in the Drosophila hopTum-1 Jak kinase causes leukemia-like hematopoietic defects. EMBO. J. 14, 1412-1420.
38. Marengere, L.E., Waterhouse, P., Duncan, G.S., Mittrucker, H.W., Feng, G.S. and Mak, T.W. (1996) Regulation of T cell receptor signaling by tyrosine phosphatase SYP association with CTLA-4 (published errata appear in Science, 1996, December 6; 274 (5293) 1597, and 1997, April 4; 276 (5309) 21). Science 272, 1170-1173.
39. Matsumura, I., Ishikawa, J., Nakajima, K., Oritani, K., Tomiyama, Y., Miyagawa, J., Kato, T., Miyazaki, H., Matsuzawa, Y. and Kanakura, Y. (1997) Thrombopoietin-induced differentiation of a human megakaryoblastic leukemia cell line, CMK, involves transcriptional activation of p21(WAF1/Cip1) by STAT5. Mol. Cell Biol. 17, 2933-2943.
40. Metcalf, D. (1989) Actions and interactions of G-CSF, LIF, and IL-6 on normal and leukemic murine cells. Leukemia 3, 349-355.
41. Minami, M., Inoue, M., Wei, S., Takeda, K., Matsumoto, M., Kishimoto, T. and Akira, S. (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, 3963-3966.
42. Morigg, R., Topham, D.J., Teglund, S., Sexl, V., McKay, C., Wang, D., Hoffmeyer, A., van Deursen, J., Sangster, M.Y., Bunting, K.D., Grosveld, G.C. and Ihle, J.N. (1999) Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity 10, 249-259.
43. 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.
44. 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.
45. Naka, T., Narazaki, M., Hirata, M., Matsumoto, T., Minamoto, S., Aono, A., Nishimoto, N., Kajita, T., Taga, T., Yoshizaki, K., Akira, S. and Kishimoto, T. (1997) Structure and function of a new STAT-induced STAT inhibitor. Nature 387, 924-929.
46. 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.
47. Nakajima, K., Yamanaka, Y., Nakae, K., Kojima, H., Ichiba, M., Kiuchi, N., Kitaoka, T., Fukada, T., Hibi, M. and Hirano, T. (1996) A central role for Stat3 in IL-6-induced regulation of growth and differentiation in M1 leukemia cells. EMBO. J. 15, 3651-3658.
48. 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.
49. Neel, B.G. and Tonks, N.K. (1997) Protein tyrosine phosphatases in signal transduction. Curr. Opin. Cell Biol. 9, 193-204.
50. Nishida, K., Yoshida, Y., Itoh, M., Fukada, T., Ohtani, Y.T.S., Astumi, T., Takahashi-Tezuka, M., Hibi, M. and Hirano, T. (1999) Gab-family adaptor proteins act downstream of cytokine and growth factor receptors and T-and B-cell antigen receptors. Blood 93, 1809-1816.
51. Niwa, H., Burdon, T., Chambers, I. and Smith, A. (1998) Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev. 12, 2048-2060.
52. 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.
53. O'Reilly, A.M. and Neel, B.G. (1998) Structural determinants of SHP-2 function and specificity in Xenopus mesoderm induction. Mol. Cell Biol. 18, 161-177.
54. Ono, K., Suga, H., Iwabe, N., Kuma, K. and Miyata, T. (1999) Multiple protein tyrosine phosphatases in sponge and explosive gene duplication in the early evolution of animals before the Parazoan-Eumetazoan split. J. Mol. Evol. 48, 654-662.
55. Paul, W.E. and Seder, R.A. (1994) Lymphocyte responses and cytokines. Cell 76, 241-251.
56. Pei, D., Wang, J. and Walsh, C.T. (1996) Differential functions of the two Src homology 2 domains in protein tyrosine phosphatase SH-PTP1. Proc. Natl. Acad. Sci. USA 93, 1141-1145.
57. 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.
58. Pregel, M.J., Shen, S.H. and Storer, A.C. (1995) Regulation of protein tyrosine phosphatase 1C: opposing effects of the two src homology 2 domains. Protein Eng 8, 1309-1316.
59. Raabe, T., Riesgo-Escovar, J., Liu, X., Bausenwein, B.S., Deak, P., Maroy, 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.
60. Rodig, S.J., Meraz, M.A., White, J.M., Lampe, P.A., Riley, J.K., Arthur, C.D., King, K.L., Sheehan, K.C., Yin, L., Pennica, D., Johnson Jr., E.M. and Schreiber, R.D. (1998) Disruption of the Jak1 gene demonstrates obligatory and nonredundant roles of the Jaks in cytokine-induced biologic responses. Cell 93, 373-383.
61. Saxton, T.M., Henkemeyer, M., Gasca, S., Shen, R., Rossi, D.J., Shalaby, F., Feng, G.S. and Pawson, T. (1997) Abnormal mesoderm patterning in mouse embryos mutant for the SH2 tyrosine phosphatase Shp-2. EMBO. J. 16, 2352-2364.
62. Schreiber, M., Kolbus, A., Piu, F., Szabowski, A., U, M.h.-S., Tian, J., Karin, M., Angel, P. and Wagner, E.F. (1999) Control of cell cycle progression by c-Jun is p53 dependent. Genes Dev. 13, 607-619.
63. Sengupta, T.K., Talbot, E.S., Scherle, P.A. and Ivashkiv, L.B. (1998) Rapid inhibition of interleukin-6 signaling and Stat3 activation mediated by mitogen-activated protein kinases. Proc. Natl. Acad. Sci. USA 95, 11107-11112.
64. Shimoda, K., van Deursen, J., Sangster, M.Y., Sarawar, S.R., Carson, R.T., Tripp, R.A., Chu, C., Quelle, F.W., Nosaka, T., Vignali, D.A., Doherty, P.C., Grosveld, G., Paul, W.E. and Ihle, J.N. (1996) Eack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 380, 630-633.
65. Stahl, N., Farruggella, T.J., Boulton, T.G., Zhong, Z., Darnell Jr., J.E. and Yancopoulos, G.D. (1995) Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 267, 1349-1353.
66. Starr, R., Willson, T.A., Viney, E.M., Murray, L.J., Rayner, J.R., Jenkins, B.J., Gonda, T.J., Alexander, W.S., Metcalf, D., Nicola, N.A. and Hilton, D.J. (1997) A family of cytokine-inducible inhibitors of signalling. Nature 387, 917-921.
67. Symes, A., Stahl, N., Reeves, S.A., Farruggella, T., Servidei, T., Gearan, T., Yancopoulos, G. and Fink, J.S. (1997) The protein tyrosine phosphatase SHP-2 negatively regulates ciliary neurotrophic factor induction of gene expression. Curr. Biol. 7, 697-700.
68. Takahashi-Tezuka, M., Hibi, M., Fujitani, Y., Fukada, T., Yamaguchi, T. and Hirano, T. (1997) Tec tyrosine kinase links the cytokine receptors to PI-3 kinase probably through JAK. Oncogene 14, 2273-2282.
69. Takahashi-Tezuka, M., Yoshida, Y., Fukada, T., Ohtani, T., Yamanaka, Y., Nishida, K., Nakajima, K., Hibi, M. and Hirano, T. (1998) Gabi acts as an adapter molecule linking the cytokine receptor gp130 to ERK mitogen-activated protein kinase. Mol. Cell Biol. 18, 4109-4117.
70. 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 State in IL-4 signalling. Nature 380, 627-630.
71. Takeda, K., Kaisho, T., Yoshida, N., Takeda, J., Kishimoto, T. and Akira, S. (1998) Stat3 activation is responsible for IL-6-dependent T-cell proliferation through preventing apoptosis: generation and characterization of T-cell-specific Stat3-deficient mice. J. Immunol. 161, 4652 4660.
72. Tang, T.L., Freeman Jr., R.M., 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.
73. Taniguchi, T. (1995) Cytokine signaling through nonreceptor protein tyrosine kinase. Science 268, 251-255.
74. Thierfelder, W.E., van Deursen, J.M., Yamamoto, K., Tripp, R.A., Sarawar, S.R., Carson, R.T., Sangster, M.Y., Vignali, D.A., Doherty, P.C., Grosveld, G.C. and Ihle, J.N. (1996) Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells. Nature 382, 171-174.
75. Thomson, A. W. (1998) The Cytokine Handbook. Academic Press, London.
76. Tonks, N.K and Neel, B.G. (1996) From form to function: signaling by protein tyrosine phosphatases (see comments). Cell 87, 365-368.
77. Turkson, J., Bowman, T., Garcia, R., Caldenhoven, E., De Groot, R.P. and Jove, R. (1998) Stat3 activation by Src induces specific gene regulation and is required for cell transformation. Mol. Cell Biol. 18, 2545-2552.
78. Weidner, K.M., Di Cesare, S., Sachs, M., Brinkmann, V., Behrens, J. and Birchmeier, W. (1996) Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis. Nature 384, 173-176.
79. Wen, Z., Zhong, Z. and Darnell, J.E. (1995) Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82, 241-250.
80. White, M.F. and Yenush, L. (1998) The IRS-signaling system: a network of docking proteins that mediate insulin and cytokine action. Curr. Top Microbiol Immunol. 228, 179-208.
81. 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.
82. Yoshimura, A., Ohkubo, T., Kiguchi, T., Jenkins, N.A., Gilbert, D.J., Copeland, N.G., Hara, T. and Miyajima, A. (1995) A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors. EMBO. J. 14, 2816-2826.