Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3

Genes and Development

Volumn 12, Issue 13, 1998, Pages 2048-2060

  Niwa, Hitoshi ^a,b   Burdon, Tom ^a   Chambers, Ian ^a   Smith, Austin ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

Cytokine receptor; Episome; ES cells; Leukemia inhibitory factor (LIF); Signaling; Tetracycline

Indexed keywords

CYTOKINE; CYTOKINE RECEPTOR; GLYCOPROTEIN GP 130; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 6 RECEPTOR; LEUKEMIA INHIBITORY FACTOR; STAT3 PROTEIN; TETRACYCLINE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL RENEWAL; CELL TYPE; CONTROLLED STUDY; EMBRYO; EPISOME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DNA BINDING; SIGNAL TRANSDUCTION; STEM CELL; TRANSGENE;

EID: 0032127977     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.13.2048     Document Type: Article

References (76)

1. Argetsinger, L.S., G.W. Hsu, M.G. Myers, N. Billestrup, M.F. White, and C. Carter-Su. 1995. Growth hormone, interferon-γ, and leukemia inhibitory factor promoted tyrosyl phosphorylation of insulin receptor substrate-1. J. Biol. Chem. 270: 14685-14692.
2. Baumann, H. and G.G. Wong. 1989. Hepatocyte-stimulating factor-111 shares structural and functional identity with leukemia-inhibitory factor. J. Immunol. 143: 1163-1167.
3. Baumann, H., D. Gearing, and S. Ziegler. 1994a. Signaling by the cytoplasmic domain of hematopoietin receptors involves two distinguishable mechanisms in hepatic cells. J. Biol. Chem. 269: 16297-16304.
4. Baumann, H., A.J. Symes, M.R. Comeau, K.K. Morella, Y. Wang, D. Friend, S.F. Ziegler, J.S. Fink, and D.P. Gearing. 1994b. Multiple regions within the cytoplasmic domains of the leukemia inhibitory factor receptor and gp130 cooperate in signal transduction in hepatic and neuronal cells. Mol. Cell. Biol. 14: 138-146.
5. Bernstine, E.G., M.L. Hooper, S. Grandchamp, and B. Ephrussi. 1973. Alkaline phosphatase activity in mouse teratoma. Proc. Natl. Acad. Sci. 70: 3899-3903.
6. Boccaccio, C., M. Ando, L. Tamagnone, A. Bardelli, P. Michieli, C. Battistini, and P. Comoglio. 1998. Induction of epithelial tubules by growth factor HGF depends on the STAT pathway. Nature 391: 285-288.
7. Boeuf, H., H. Hauss, F. De Graeve, N. Baran, and N. Kedinger. 1997. Leukemia inhibitory factor-dependent transcriptional activation in embryonic stem cells. J. Cell Biol. 138: 1207-1217.
8. Bonni, A., Y. Sun, M. Nadal-Vicens, A. Bhatt, D.A. Frank, I. Rozovsky, N. Stahl, G.D. Yancopoulos, and M.E. Greenberg. 1997. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278: 477-483.
9. Boulter, C.A., A. Aguzzi, R.L. Williams, E.F. Wagner, M.J. Evans, and R. Beddington. 1991. Expression of v-src induces aberrant development and twinning in chimaeric mice. Development 111: 357-366.
10. Boulton, T.G., N. Stahl, and G.D. Yancopoulos. 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.
11. Brook, F.A. and R.L. Gardner. 1997. The origin and efficient derivation of embryonic stem cells in the mouse. Proc. Natl. Acad. Sci. 94: 5709-5712.
12. Cao, X., A. Tay, G.R. Guy, and Y.H. Tan. 1996. Activation and association of stat3 with src in v-src-transformed cell lines. Mol. Cell. Biol. 16: 1595-1603.
13. Chambers, I., A. Cozens, J. Broadbent, M. Robertson, M. Lee, M. Li, and A. Smith. 1997. Structure of the mouse leukaemia inhibitory factor receptor gene: Regulated expression of mRNA encoding a soluble receptor isoform from an alternative 5′ untranslated region. Biochem. J. 328: 879-888.
14. Chomczynski, P. and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159.
15. Conover, J.C., N.Y. Ip, W.T. Poueymirou, B. Bates, M.P. Goldfarb, T.M. DeChiara, and G.D. Yancopoulos. 1993. Ciliary neurotrophic factor maintains the pluripotentiality of embryonic stem cells. Development 119: 559-565.
16. Davis, S., T.H. Aldrich, N. Stahl, L. Pan, T. Taga, T. Kishimoto, N.Y. Ip, and G.D. Yancopoulos. 1993. LIFRβ and gp130 as heterodimerizing signal transducers of the tripartite CNTF receptor. Science 260: 1805-1808.
17. Dittrich, E., C.H. Haft, L. Muys, P.C. Heinrich, and L. Graeve. 1996. A di-leucine motif and an upstream serine in the interleukin-6 (IL-6) signal transducer gp130 mediate ligand-induced endocytosis and down-regulation of the IL-6 receptor. J. Biol. Chem. 271: 5487-5494.
18. Dudley, D.T., L. Pang, S.J. Decker, A.J. Bridges, and A.R. Saltiel. 1995. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. 92: 7686-7689.
19. Durbin, J.E., R. Hackenmiller, M.C. Simon, and D.E. Levy. 1996. Targeted disruption of the mouse stat1 gene results in compromised innate immunity to viral disease. Cell 84: 443-450.
20. Ernst, M., D.P. Gearing, and A.R. Dunn. 1994. Functional and biochemical association of Hck with the LIF/IL-6 receptor signal transducing subunit gp130 in embryonic stem cells. EMBO J. 13: 1574-1584.
21. Ernst, M., A. Oates, and A.R. Dunn. 1996. Gp130-mediated signal transduction in embryonic stem cells involves activation of Jak and Ras/mitogen activated protein kinase pathways. J. Biol. Chem. 271: 30136-30143.
22. Evans, M.J. and M. Kaufman. 1981. Establishment in culture or pluripotential cells from mouse embryos. Nature 292: 154-156.
23. Fukada, T., M. Hibi, Y. Yamanaka, M. Takahashi-Tezuka, Y. Fujitani, T. Yamaguchi, K. Nakajima, and T. Hirano. 1996. Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: Involvement of STAT3 in anti-apoptosis. Immunity 5: 449-460.
24. Fukunaga, R., E. Ishizaka-Ikeda, Y. Seto, and S. Nagata. 1990. Expression cloning of a receptor for murine granulocyte colony-stimulating factor. Cell 61: 341-350.
25. Gassmann, M., G. Donoho, and P. Berg. 1995. Maintenance of an extrachromosomal plasmid vector in mouse embryonic stem cells. Proc. Natl. Acad. Sci. 92: 1292-1296.
26. Gearing, D.P. and G.A. Bruce. 1992. Oncostatin M binds the high-affinity leukemia inhibitory factor receptor. New Biol. 4: 61-65.
27. Gearing, D.P., C.J. Thut, T. VandenBos, S.D. Gimpel, P.B. Delaney, J. King, V. Price, D. Cosman, and M.P. Beckman. 1991. Leukemia inhibitory factor receptor is structurally related to the Il-6 signal transducer, gp130. EMBO J. 10: 2839-2848.
28. Gobert, S., S. Chretien, F. Gouilleux, O. Muller, C. Pallard, I. Dusanter-Fourt, B. Groner, C. Lacombe, S. Gisselbrecht, and P. Mayeux. 1996. Identification of tyrosine residues within the intracellular domain of the erythropoietin receptor crucial for STAT5 activation. EMBO J. 15: 2434-2441.
29. Gossen, M. and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. 89: 5547-5551.
30. Hibi, M., M. Murakami, M. Saito, T. Hirano, T. Taga, and T. Kishimoto. 1990. Molecular cloning and expression of an IL-6 signal transducer, gp130. Cell 63: 1149-1157.
31. Higuchi, R., B. Krummel, and R.K. Saiki. 1988. A general method of in vitro preparation and specific mutagenesis of DNA fragments: Study of protein and DNA interactions. Nucleic Acids Res. 15: 7351-7367.
32. Hirota, H., K. Yoshida, T. Kishimoto, and T. Taga. 1995. Continuous activation of gp130, a signal-transducing receptor component for interleukin 6-related cytokines, causes myocardial hypertrophy in mice. Proc. Natl. Acad. Sci. 92: 4862-4866.
33. Hocke, G.M., M.Z. Cui, and G.H. Fey. 1995. The LIF response element of the α2 macroglobulin gene confers LIF-induced transcriptional activation in embryonal stem cells. Cytokine 7: 491-502.
34. Ihara, S., K. Nakajima, T. Fukada, M. Hibi, S. Nagata, T. Hirano, and Y. Fukui. 1997. Dual control of neurite outgrowth by STAT3 and MAP kinase in PC12 cells stimulated with interleukin-6. EMBO J. 16: 5345-5352.
35. Ihle, J. 1996. STATs: Signal transducers and activators of transcription. Cell 84: 331-334.
36. Kishimoto, T., T. Taga, and S. Akira. 1994. Cytokine signal transduction. Cell 76: 253-262.
37. Koblar, S.A., A.M. Turnley, B.J. Classon, K.L. Reid, C.B. Ware, S.S. Cheema, M. Murphy, and P.F. Bartlett. 1998. Neural precursor differentiation into astrocytes requires signaling through the leukemia inhibitory factor receptor. Proc. Natl. Acad. Sci. 95: 3178-3181.
38. Li, M., M. Sendtner, and A. Smith. 1995. Essential function of LIF receptor in motor neurons. Nature 378: 724-727.
39. Lutticken, C., U.M. Wegenka, J. Yuan, J. Buschmann, C. Schindler, A. Ziemiecki, A.G. Harpur, A.F. Wilks, K. Yasukawa, T. Taga, T. Kishimoto, G. Barbieri, S. Pellegrini, M. Sendtner, P.C. Heinrich, and F. Horn. 1994. Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130. Science 263: 89-92.
40. Mansour, S.L., K.R. Thomas, and M.R. Capecchi. 1988. Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: A general strategy for targeting mutations to non-selectable genes. Nature 336: 348-352.
41. Martin, G.R. 1981. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by terato-carcinoma stem cells. Proc. Natl. Acad. Sci. 78: 7634-7638.
42. Matsuda, T., T. Fukada, M. TakahashiTezuka, Y. Okuyama, Y. Fujitani, Y. Hanazono, H. Hirai, and T. Hirano. 1995a. Activation of Fes tyrosine kinase by gp130, an interleukin-6 family cytokine signal transducer, and their association. J. Biol. Chem. 270: 11037-11039.
43. Matsuda, T., M. TakahashiTezuka, T. Fukada, Y. Okuyama, Y. Fujitani, S. Tsukada, H. Mano, H. Hirai, O.N. Witte, and T. Hirano. 1995b. Association and activation of Btk and Tec tyrosine kinases by gp130, a signal transducer of the interleukin-6 family of cytokines. Blood 85: 627-633.
44. Minami, M., M. Inoue, S. Wei, K. Takeda, M. Matsumoto, T. Kishimoto, and A. 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. 93: 3963-3966.
45. Mountford, P., B. Zevnik, A. Duwel, J. Nichols, M. Li, C. Dani, M. Robertson, I. Chambers, and A. Smith. 1994. Dicistronic targeting constructs: Reporters and modifiers of mammalian gene expression. Proc. Natl. Acad. Sci. 91: 4303-4307.
46. Murakami, M., M. Hibi, N. Nakagawa, T. Nakagawa, K. Yasukawa, K. Yamanishi, T. Taga, and T. Kishimoto. 1993. IL-6-induced homodimerization of gp130 and associated activation of a tyrosine kinase. Science 260: 1808-1810.
47. Nakajima, K., Y. Yamanaka, K. Nakae, H. Kojima, M. Ichiba, N. Kiuchi, T. Kitaoka, T. Fukada, M. Hibi, and T. Hirano. 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., B.A. Witthuhn, K. Yoshida, O. Silvennoinen, K. Yasukawa, J.N. Ihle, T. Kishimoto, and T. Taga. 1994. Activation of JAK2 kinase mediated by the interleukin 6 signal transducer gp130. Proc. Natl. Acad. Sci. 91: 2285-2289.
49. Nichols, J., I. Chambers, and A. Smith. 1994. Derivation of germline competent embryonic stem cells with combination of interleukin-6 and soluble interleukin-6 receptor. Exp. Cell Res. 215: 237-239.
50. Okazawa, H., K. Okamoto, F. Ishino, T. IshinoKaneko, S. Takeda, Y.M.M. Toyoda, and H. Hamada. 1991. The oct3 gene, a gene for an embryonic transcription factor, is controlled by a retinoic acid repressible enhancer. EMBO J. 10: 2997-3006.
51. Pennica, D., K.L. King, K.J. Shaw, E. Luis, J. Rullamas, S.-M. Luoh, W.C. Darbinne, D.S. Knutzon, R. Yen, K.R. Chien, J.B. Baker, and W.L. Wood. 1995a. Expression cloning of cardiotrophin 1, a cytokine that induces cardiac myocyte hypertrophy. Proc. Natl. Acad. Sci. 92: 1142-1146.
52. Pennica, D., K.J. Shaw, T.A. Swanson, M.W. Moore, D.L. Shelton, K.A. Zioncheck, A. Rosenthal, T. Taga, N.F. Paoni, and W.I. Wood. 1995b. Cardiotrophin-1. Biological activities and binding to the leukemia inhibitory factor receptor/ gp130 signaling complex. J. Biol. Chem. 270: 10915-10922.
53. Rathjen, P.D., J. Nichols, S. Toth, D.R. Edwards, J.K. Heath, and A.G. Smith. 1990. Developmentally programmed induction of differentiation inhibiting activity and the control of stem cell populations. Genes & Dev. 4: 2308-2318.
54. Rose, T.M., D.M. Weiford, N.L. Gunderson, and A.G. Bruce. 1994. Oncostatin M (OSM) inhibits the differentiation of pluripotent embryonic stem cells in vitro. Cytokine 6: 48-54.
55. Sadowski, H.B., K. Shuai, J.E. Darnell, and M.Z. Gilman. 1993. A common nuclear signal transduction pathway activated by growth factor and cytokine receptors. Science 261: 1739-1744.
56. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
57. Schaefer, T.S., L.K. Sanders, and D. Nathans. 1995. Cooperative transcriptional activity of jun and Stat3β, a short form of Stat3. Proc. Natl. Acad. Sci. 92: 9097-9101.
58. Sheng, Z., K. Knowlton, J. Chen, M. Hoshijima, J.H. Brown, and K.R. Chien. 1997. Cardiotrophin 1 (CT-1) inhibition of cardiac myocyte apoptosis via a mitogen activated protein kinase-dependent pathway. J. Biol. Chem. 272:5783-5791.
59. Shimozaki, K., K. Nakajima, T. Hirano, and S. Nagata. 1997. Involvement of STAT3 in the granulocyte colony-stimulating factor-induced differentiation of myeloid cells. J. Biol. Chem. 272: 25184-25189.
60. Smith, A.G. 1991. Culture and differentiation of embryonic stem cells. J. Tiss. Cult. Meth. 13: 89-94.
61. Smith, A.G. and M.L. Hooper. 1987. Buffalo rat liver cells produce a diffusible activity which inhibits the differentiation of murine embryonal carcinoma and embryonic stem cells. Dev. Biol. 121: 1-9.
62. Smith, A.G., J.K. Heath, D.D. Donaldson, G.G. Wong, J. Moreau, M. Stahl, and D. Rogers. 1988. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 336: 688-690.
63. Stahl, N., T.G. Boulton, T. Farruggella, N.Y. Ip, S. Davis, B.A. Witthuhn, F.W. Quelle, O. Silvennoinen, G. Barbieri, S. Pellegrini, J.N. Ihle, and G.D. Yancopoulos. 1994. Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6 beta receptor components. Science 263: 92-95.
64. Stahl, N., T.J. Farrugella, T.G. Boulton, Z. Zhong, J.E. Darnell, and G.D. Yancopoulos. 1995. Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 267: 1349-1353.
65. Starr, R., U. Novak, T.A. Willson, M. Inglese, V. Murphy, W.S. Alexander, D. Metcalf, N.A. Nicola, D.J. Hilton, and M. Ernst. 1997. Distinct roles for leukemia inhibitory factor receptor α-chain and gp130 in cell type-specific signal transduction. J. Biol. Chem. 272: 19982-19986.
66. Takeda, K., K. Noguchi, W. Shi, T. Tanaka, M. Matsumoto, N. Yoshida, T. Kishimoto, and S. Akira. 1997. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc. Natl. Acad. Sci. 94: 3801-3804.
67. Tomida, M., Y. Yamamoto-Yamaguchi, and M. Hozumi. 1984. Purification of a factor inducing differentiation of mouse myeloid leukemic M1 cells from conditioned medium of mouse fibroblast L929 cells. J. Biol. Chem. 259: 10978-10982.
68. Wen, Z., Z. Zhong, and J.E. Darnell. 1995. Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82: 241-250.
69. Williams, R.L., D.J. Hilton, S. Pease, T.A. Willson, C.L. Stewart, D.P. Gearing, E.F. Wagner, D. Metcalf, N.A. Nicola, and N.M. Gough. 1988. Myeloid leukemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 336: 684-687.
70. Wolf, E., R. Kramer, I. Polejaeva, H. Thoenen, and G. Brem. 1994. Efficient generation of chimeric mice using embryonic stem cells after long term culture in the presence of ciliary neurotrophic factor. Transgenic Res. 3: 152-158.
71. Yamamori, T., K. Fukada, R. Aebersold, S. Korsching, M.-J. Fann, and P.H. Patterson. 1989. The cholinergic neuronal differentiation factor from heart cells is identical to leukemia inhibitory factor. Science 246: 1412-1416.
72. Yamanaka, Y., K. Nakajima, T. Fukada, M. Hibi, and T. Hirano. 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.
73. Yasukawa, K., T. Saito, K. Futatsugi, T. Saito, Y. Sekimori, Y. Koishihara, H. Fukui, Y. Ohsugi, T. Matsuda, H. Yawata, T. Hitano, T. Taga, and T. Kishimoto. 1990. Purification and characterization of soluble human IL-6 receptor expressed in CHO cells. J. Biochem. 108: 673-676.
74. Yin, T. and Y.-C. Yang. 1994. Mitogen-activated protein kinases and ribosomal S6 protein kinases are involved in signaling pathways shared by interleukin-11, interleukin-6, leukemia inhibitory factor, and oncostatin M in mouse 3T3-L1 cells. J. Biol. Chem. 269: 3731-3738.
75. Yoshida, K., I. Chambers, J. Nichols, A. Smith, M. Saito, K. Yasukawa, M. Shoyab, T. Taga, and T. Kishimoto. 1994. Maintenance of the pluripotential phenotype of embryonic stem cells through direct activation of gp130 signalling pathways. Mech. Dev. 45: 163-171.
76. Yoshida, K., T. Taga, M. Saito, S. Suematsu, A. Kumanogoh, T. Tanaka, H. Fujiwara, M. Hirata, T. Yamagami, T. Nakahata, T. Hirabayashi, Y. Yoneda, K. Tanaka, W.-Z. Wang, C. Mori, K. Shiota, N. Yoshida, and T. Kishimoto. 1996. Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc. Natl. Acad. Sci. 93: 407-411.