STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells

EMBO Journal

Volumn 18, Issue 17, 1999, Pages 4754-4765

  Nosaka, Tetsuya ^a   Kawashima, Toshiyuki ^a   Misawa, Kazuhide ^a   Ikuta, Koichi ^b   Mui, Alice L F ^c   Kitamura, Toshio ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Apoptosis; JAB; p21(WAF1 Cip1); pim 1; STAT5

Indexed keywords

GROWTH FACTOR; INTERLEUKIN 3; MESSENGER RNA; MUTANT PROTEIN; PROTEIN BCL X; PROTEIN P21; STAT5 PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; CELL FATE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; GENE INDUCTION; HEMATOPOIETIC CELL; LEUKEMIA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; APOPTOSIS; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA; DNA-BINDING PROTEINS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, LEUKEMIC; INTERLEUKIN-3; JANUS KINASE 2; MICE; MILK PROTEINS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-PIM-1; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TIME FACTORS; TRANS-ACTIVATORS; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 0033199236     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.17.4754     Document Type: Article

References (72)

1. Armstrong, D.K., Kaufmann, S.H., Ottaviano, Y.L., Furuya, Y., Buckley, J.A., Isaacs, J.T. and Davidson, N.E. (1994) Epidermal growth factor-mediated apoptosis of MDA-MB-468 human breast cancer cells. Cancer Res., 54, 5280-5283.
2. Boise, L.H., Gonzalez-Garcia, M., Postema, C.E., Ding, L., Lindsten, T., Turka, L.A., Mao, X., Nunez, G. and Thompson, C.B. (1993) bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell, 74, 597-608.
3. Breuer, M., Slebos, R., Verbeek, S., van Lohuizen, M., Wientjens, E. and Berns, A. (1989) Very high frequency of lymphoma induction by a chemical carcinogen in pim-1 transgenic mice. Nature, 340, 61-63.
4. Carlesso, N., Frank, D.A. and Griffin, J.D. (1996) Tyrosyl phosphorylation and DNA binding activity of signal transducers and activators of transcription (STAT) proteins in hematopoietic cell lines transformed by Bcr/Abl. J. Exp. Med. 183, 811-820.
5. Chin, Y.E., Kitagawa, M., Kuida, K., Flavell, R.A. and Fu, X.-Y. (1997) Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis. Mol. Cell. Biol., 17, 5328-5337.
6. 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.
7. Damell, J.E.,Jr, 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.
8. El-Deiry, W.S. et al. (1993) WAF1, a potential mediator of p53 tumor suppression. Cell, 75, 817-825.
9. Endo, T.A. et al. (1997) A new protein containing an SH2 domain that inhibits JAK kinases. Nature, 387, 921-924.
10. Evan, G.I., Wyllie, A.H., Gilbert, C.S., Littlewood, T.D., Land, H., Brooks, M., Waters, C.M., Penn, L.Z. and Hancock, D.C. (1992) Induction of apoptosis in fibroblasts by c-myc protein. Cell, 69, 119-128.
11. Fang, W., Rivard, J.J., Mueller, D.L. and Behrens, T.W. (1994) Cloning and molecular characterization of mouse bcl-x in B and T lymphocytes. J. Immunol., 153, 4388-4398.
12. Fujii, H. 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, 5482-5486.
13. Gill, G.N. and Lazar, C.S. (1981) Increased phosphotyrosine content and inhibition of proliferation in EGF-treated A431 cells. Nature, 293, 305-307.
14. Gouilleux-Gruart, V. et al. (1996) STAT-related transcription factors are constitutively activated in peripheral blood cells from acute leukemia patients. Blood, 87, 1692-1697.
15. 1 cyclin-dependent kinases. Cell, 75, 805-816.
16. Hilton, D.J. et al. (1998) Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc. Natl Acad. Sci. USA, 95, 114-119.
17. Ihle, J.N. (1995) Cytokine receptor signalling. Nature, 377, 591-594.
18. Ihle, J.N. (1996) STATs: signal transducers and activators of transcription. Cell, 84, 331-334.
19. Ishida, Y., Agata, Y., Shibahara, K. and Honjo, T. (1992) Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J., 11, 3887-3895.
20. Kaplan, M.H., Schindler, U., Smiley, S.T. and Grusby, M.J. (1996) Stat6 is required for mediating responses to IL-4 and for the development of Th2 cells. Immunity, 4, 313-319.
21. 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.
22. Kitamura, T. et al. (1989) Establishment and characterization of a unique human cell line that proliferates dependently on GM-CSF, IL-3, or erythropoietin. J. Cell. Physiol., 140, 323-334.
23. Kitamura, T., Onishi, M., Kinoshita, S., Shibuya, A., Miyajima, A. and Nolan, G.P. (1995) Efficient screening of retroviral cDNA expression libraries. Proc. Natl Acad. Sci. USA, 92, 9146-9150.
24. Kramer, M.H.H., Kluin, P.M., Wijburg, E.R., Fibbe, W.E. and Kluin-Nelemans, H.C., (1995) Differentiation of follicular lymphoma cells after autologous bone marrow transplantation and haematopoietic growth factor treatment. Lancet, 345, 488-490.
25. Lacronique, V. et al. (1997) A TEL-JAK2 fusion protein with constitutive kinase activity in human leukemia. Science, 278, 1309-1312.
26. Lenardo, M.J. (1991) Interleukin-2 programs mouse αβ T lymphocytes for apoptosis. Nature, 353, 858-861.
27. Leverson, J.D., Koskinen, P.J., Orrico, F.C., Rainio, E.-M., Jalkanen, K.J., Dash, A.B., Eisenman, R.N. and Ness, S.A. (1998) Pim-1 kinase and p100 cooperate to enhance c-Myb activity. Mol. Cell, 2, 417-425.
28. r 33000 Pim-1 kinase enhances factor-independent survival and inhibits apoptosis in murine myeloid cells. Cancer Res., 57, 5348-5355.
29. Liu, R.Y., Fan, C., Garcia, R., Jove, R. and Zuckerman, K.S. (1999) Constitutive activation of the JAK2/STAT5 signal transduction pathway correlates with growth factor independence of megakaryocytic leukemic cell lines. Blood, 93, 2369-2379.
30. Liu, X., Robinson, G.W., Wagner, K.-U., Garrett, L., Wynshaw-Boris, A. and Hennighausen, L. (1997) Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev., 11, 179-186.
31. Manabe, A., Coustan-Smith, E., Kumagai, M., Behm, F.G., Raimondi, S.C., Pui, C.H. and Campana, D. (1994) Interleukin-4 induces programmed cell death (apoptosis) in cases of high-risk acute lymphoblastic leukemia. Blood, 83, 1731-1737.
32. Masuhara, M. et al. (1997) Cloning and characterization of novel CIS family genes. Biochem. Biophys. Res. Commun., 239, 439-446.
33. WAF1/Cip1 by STAT5. Mol. Cell. Biol., 17, 2933-2943.
34. Meraz, M.A. et al. (1996) Targeted disruption of the Stat1 gene in mice reveales unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell, 84, 431-442.
35. 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.
36. 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.
37. Moriggl, R. et al. (1999) Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity, 10, 249-259.
38. Mui, A.L.-F., 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.
39. Naka, T. et al. (1997) Structure and function of a new STAT-induced STAT inhibitor. Nature, 387, 924-929.
40. Nakajima, H., Liu, X.-W., Wynshaw-Boris, A., Rosenthal, L.A., Imada, K., Finbloom, D.S., Hennighausen, L. and Leonard, W.J. (1997) An indirect effect of Stat5a in IL-2-induced proliferation: A critical role for Stat5a in IL-2-mediated IL-2 receptor α chain induction. Immunity, 7, 691-701.
41. Neubauer, H., Cumano, A., Muller, M., Wu, H., Huffstadt, U. and Pfeffer, K. (1998) Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell, 93, 397-409.
42. Nosaka, T., van Deursen, J.M.A., Tripp, R.A., Thierfelder, W.E., Witthuhn, B.A., McMickle, A.P., Doherty, P.C., Grosveld, G.C. and Ihle, J.N. (1995) Defective lymphoid development in mice lacking Jak3. Science, 270, 800-802.
43. Onishi, M. et al. (1996) Applications of retrovirus-mediated expression cloning. Exp. Hematol., 24, 324-329.
44. Onishi, M., Nosaka, T., Misawa, K.,. Mui, A.L.-F, Gorman, D., McMahon, M., Miyajima, A. and Kitamura, T. (1998) Identification and characterization of a constitutively active STAT5 mutant that promotes cell proliferation. Mol. Cell. Biol., 18, 3871-3879.
45. O'Shea, J.J. (1997) Jaks, STATs, cytokine signal transduction and immunoregulation: Are we there yet? Immunity, 7, 1-11.
46. Parganas, E. et al. (1998) Jak2 is essential for signaling through a variety of cytokine receptors. Cell, 93, 385-395.
47. Park, S.Y. et al. (1995) Developmental defects of lymphoid cells in Jak3 kinase-deficient mice. Immunity, 3, 771-782.
48. Pear, W.S., Nolan, G.P., Scott, M.L. and Baltimore, D. (1993) Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl Acad. Sci. USA, 90, 8392-8396.
49. Peeters, P. et al. (1997) Fusion of TEL, the ETS-variant gene 6 (ETV6), to the receptor-associated kinase JAK2 as a result of t(9;12) in a lymphoid and t(9;15;12) in a myeloid leukemia. Blood, 90, 2535-2540.
50. Polyak, K., Waldman, T., He, T.-C., Kinzler, K.W. and Vogelstein, B. (1996) Genetic determinants of p53-induced apoptosis and growth arrest. Genes Dev., 10, 1945-1952.
51. Quelle, F.W., Wang, D., Nosaka, T., Thierfelder, W.E., Stravopodis, D., Weinstein, Y. and Ihle, J.N. (1996) Erythropoietin induces activation of Stat5 through association with specific tyrosines on the receptor that are not required for a mitogenic response. Mol. Cell. Biol., 16, 1622-1631.
52. Rodig, S.J. et al. (1998) Disruption of the Jak1 gene demonstrates obligatory and nonredundant roles of the Jaks in cytokine-induced biologic responses. Cell, 93, 373-383.
53. Selten, G., Cuypers, H.T., Boelens, W., Robanus-Maandag, E., Verbeek, J., Domen, J., van Beveren, C. and Berns, A. (1986) The primary structure of the putative oncogene pim-1 shows extensive homology with protein kinases. Cell, 46, 603-611.
54. INK4a. Cell, 88, 593-602.
55. Shimoda, K. et al. (1996) Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature, 380, 630-633.
56. Staal, F.J., Bakker, A.Q., Verkuijlen, M., van Oort, E. and Spits, H. (1996) Use of bicistronic retroviral vectors encoding the LacZ gene together with a gene of interest: a mothod to select producer cells and follow transduced target cells. Cancer Gene Ther., 3, 345-351.
57. Starr, R. et al. (1997) A family of cytokine-inducible inhibitors of signalling. Nature, 387, 917-921.
58. Takeda, K. et al. (1996) Essential role of Stat6 in IL-4 signalling. Nature, 380, 627-630.
59. Takeda, K., Noguchi, K., Shi, W., Tanaka, T., Matsumoto, M., Yoshida, N., Kishimoto, T. and Akira, S. (1997) Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc. Natl Acad. Sci. USA, 94, 3801-3804.
60. Teglund, S. et al. (1998) Stat5a and stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell, 93, 841-850.
61. Thierfelder, W.E. et al. (1996) Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cell. Nature, 382, 171-174.
62. Thomis, D.C., Gurniak, C.B., Tivol, E., Sharpe, A.H. and Berg, L.J. (1995) Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3. Science, 270, 794-797.
63. Udy, G.B., Towers, R.P., Snell, R.G., Wilkins, R.J., Park, S.-H., Ram, P.A., Waxman, D.J. and Davey, H.W. (1997) Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc. Natl Acad. Sci. USA, 94, 7239-7244.
64. van der Houven van Oordt, C.W., Schouten, T.G., van Krieken, J.H., van Dierendonck, J.H., van der Eb,AJ. and Breuer,M.L. (1998) X-ray-induced lymphomagenesis in Em-pim-1 transgenic mice: an investigation of the co-operating molecular events. Carcinogenesis, 19, 847-853.
65. Van Lohuizen, M., Verbeek, S., Krimpenfort, P., Domen, J., Saris, C., Radaszkiewicz, T. and Berns, A. (1989) Predisposition to lymphomagenesis in pim-1 transgenic mice: cooperation with c-myc and N-myc in murine leukemia virus-induced tumors. Cell, 56. 673-682.
66. Wang, D., Stravopodis, D., Teglund, S., Kitazawa, J. and Ihle, J.N. (1996) Naturally occurring dominant negative variants of Stat5. Mol. Cell. Biol., 16, 6141-6148.
67. Weber-Nordt, R.M., Egen, C., Wehinger, J., Ludwig, W., Gouilleux-Gruart, V., Mertelsmann, R. and Finke, J. (1996) Constitutive activation of STAT proteins in primary lymphoid and myeloid leukemia cells and in Epstein-Barr virus (EBV)- related lymphoma cell lines. Blood, 88, 809-816.
68. Welte, T. et al. (1999) STAT5 interaction with the T cell receptor complex and stimulation of T cell proliferation. Science, 283, 222-225.
69. Cip1. Mol. Cell. Biol., 17, 5598-5611.
70. 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.
71. Yoshimura, A., Ichihara, M., Kinjyo, I., Moriyama, M., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., Hara, T. and Miyajima, A. (1996) Mouse oncostatin M: an immediate early gene induced by multiple cytokines through the JAK-STAT5 pathway. EMBO J., 15, 1055-1063.
72. Younes, A. et al. (1994) Growth inhibition of follicular small-cleaved-cell lymphoma cells in short-term culture by IL-3. Ann. Oncol., 5, 265-268.