A preferential role for STAT5, not constitutively active STAT3, in promoting survival of a human lymphoid tumor

Journal of Immunology

Volumn 177, Issue 8, 2006, Pages 5032-5040

  Nagy, Zsuzsanna S ^a   Rui, Hallgeir ^b   Stepkowski, Stanislaw M ^c   Karras, James ^d   Kirken, Robert A ^a  

^a UNIVERSITY OF TEXAS AT EL PASO   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d ISIS PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL LEUKEMIA 10; GENE PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; JANUS KINASE; STAT PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 5; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL FUNCTION; CELL SURVIVAL; CELL VIABILITY; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; KINETICS; LYMPHATIC SYSTEM TUMOR; MICROARRAY ANALYSIS; NICK END LABELING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RECEPTOR AFFINITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR MODEL; VALIDATION PROCESS;

EID: 33749529310     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.8.5032     Document Type: Article

References (67)

1. Nagy, Z. S., J. Ross, H. Cheng, S. M. Stepkowski, and R. A. Kirken. 2004. Regulation of lymphoid cell apoptosis by Jaks and Stats. Crit. Rev. Immunol. 24: 87-110.
2. Chai, S. K., G. L. Nichols, and P. Rothman. 1997. Constitutive activation of JAKs and STATs in BCR-Abl-expressing cell lines and peripheral blood cells derived from leukemic patients. J. Immunol. 159: 4720-4728.
3. Bromberg, J. F., C. M. Horvath, D. Besser, W. W. Lathem, and J. E. Darnell, Jr. 1998. Stat3 activation is required for cellular transformation by v-src. Mol. Cell. Biol. 18: 2553-2558.
4. 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.
5. Murakami, Y., S. Nakano, Y. Niho, N. Hamasaki, and K. Izuhara. 1998. Constitutive activation of Jak-2 and Tyk-2 in a v-Src-transformed human gallbladder adenocarcinoma cell line. J. Cell. Physiol. 175: 220-228.
6. Turkson, J., T. Bowman, R. Garcia, E. Caldenhoven, R. P. De Groot, and R. Jove. 1998. Stat3 activation by Src induces specific gene regulation and is required for cell transformation. Mol. Cell. Biol. 18: 2545-2552.
7. Yu, C. L., D. J. Meyer, G. S. Campbell, A. C. Larner, C. Carter-Su, J. Schwartz, and R. Jove. 1995. Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 269: 81-83.
8. Kirken, R. A., R. A. Erwin, L. Wang, Y. Wang, H. Rui, and W. L. Farrar. 2000. Functional uncoupling of the Janus kinase 3-Stat5 pathway in malignant growth of human T cell leukemia virus type 1-transformed human T cells. J. Immunol. 165: 5097-5104.
9. Weber-Nordt, R. M., C. Egen, J. Wehinger, W. Ludwig, V. Gouilleux-Gruart, R. Mertelsmann, and J. Finke. 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.
10. Akira, S., Y. Nishio, M. Inoue, X. J. Wang, S. Wei, T. Matsusaka, K. Yoshida, T. Sudo, M. Naruto, and T. Kishimoto. 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.
11. Narimatsu, M., H. Maeda, S. Itoh, T. Atsumi, T. Ohtani, K. Nishida, M. Itoh, D. Kamimura, S. J. Park, K. Mizuno, et al. 2001. Tissue-specific autoregulation of the stat3 gene and its role in interleukin-6-induced survival signals in T cells. Mol. Cell. Biol. 21: 6615-6625.
12. Takeda, K., T. Kaisho, N. Yoshida, J. Takeda, T. Kishimoto, and S. Akira. 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.
13. Akaishi, H., K. Takeda, T. Kaisho, R. Shineha, S. Satomi, J. Takeda, and S. Akira. 1998. Defective IL-2-mediated IL-2 receptor α chain expression in Stat3-deficient T lymphocytes. Int. Immunol. 10: 1747-1751.
14. Catlett-Falcone, R., T. H. Landowski, M. M. Oshiro, J. Turkson, A. Levitzki, R. Savino, G. Ciliberto, L. Moscinski, J. L. Fernandez-Luna, G. Nunez, et al. 1999. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 10: 105-115.
15. Watson, C. J., and W. R. Miller. 1995. Elevated levels of members of the STAT family of transcription factors in breast carcinoma nuclear extracts. Br. J. Cancer 71: 840-844.
16. Cattaneo, E., L. Magrassi, C. De-Fraja, L. Conti, I. Di Gennaro, G. Butti, and S. Govoni. 1998. Variations in the levels of the JAK/STAT and ShcA proteins in human brain tumors. Anticancer Res. 18: 2381-2387.
17. Epling-Burnette, P. K., J. H. Liu, R. Catlett-Falcone, J. Turkson, M. Oshiro, R. Kothapalli, Y. Li, J. M. Wang, H. F. Yang-Yen, J. Karras, et al. 2001. Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression. J. Clin. Invest. 107: 351-362.
18. Fernandas, A., A. W. Hamburger, and B. I. Gerwin. 1999. ErbB-2 kinase is required for constitutive stat 3 activation in malignant human lung epithelial cells. Int. J. Cancer 83: 564-570.
19. Grandis, J. R., S. D. Drenning, Q. Zeng, S. C. Watkins, M. F. Melhem, S. Endo, D. E. Johnson, L. Huang, Y. He, and J. D. Kim. 2000. Constitutive activation of Stat3 signaling abrogates apoptosis in squamous cell carcinogenesis in vivo. Proc. Natl. Acad. Sci. USA 97: 4227-4232.
20. Ni, Z., W. Lou, E. S. Leman, and A. C. Gao. 2000. Inhibition of constitutively activated Stat3 signaling pathway suppresses growth of prostate cancer cells. Cancer Res. 60: 1225-1228.
21. Battle, T. E., and D. A. Frank. 2002. The role of STATs in apoptosis. Curr. Mol. Med. 2: 381-392.
22. Buettner, R., L. B. Mora, and R. Jove. 2002. Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin. Cancer Res. 8: 945-954.
23. Mora, L. B., R. Buettner, J. Seigne, J. Diaz, N. Ahmad, R. Garcia, T. Bowman, R. Falcone, R. Fairclough, A. Cantor, et al. 2002. Constitutive activation of Stat3 in human prostate tumors and cell lines: direct inhibition of Stat3 signaling induces apoptosis of prostate cancer cells. Cancer Res. 62: 6659-6666.
24. Nam, S., R. Buettner, J. Turkson, D. Kim, J. Q. Cheng, S. Muehlbeyer, F. Hippe, S. Vatter, K. H. Merz, G. Eisenbrand, and R. Jove. 2005. Indirubin derivatives inhibit Stat3 signaling and induce apoptosis in human cancer cells. Proc. Natl. Acad. Sci. USA 102: 5998-6003.
25. Turkson, J., J. S. Kim, S. Zhang, J. Yuan, M. Huang, M. Glenn, E. Haura, S. Sebti, A. D. Hamilton, and R. Jove. 2004. Novel peptidomimetic inhibitors of signal transducer and activator of transcription 3 dimerization and biological activity. Mol. Cancer Ther. 3: 261-269.
26. Turkson, J., S. Zhang, L. B. Mora, A. Burns, S. Sebti, and R. Jove. 2005. A novel platinum compound inhibits constitutive Stat3 signaling and induces cell cycle arrest and apoptosis of malignant cells. J. Biol. Chem. 280: 32979-32988.
27. Moriggl, R., D. J. Topham, S. Teglund, V. Sexl, C. McKay, D. Wang, A. Hoffmeyer, J. van Deursen, M. Y. Sangster, K. D. Bunting, et al. 1999. Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity 10: 249-259.
28. Hoover, R. R., M. J. Gerlach, E. Y. Koh, and G. Q. Daley. 2001. Cooperative and redundant effects of STAT5 and Ras signaling in BCR/ABL transformed hematopoietic cells. Oncogene 20: 5826-5835.
29. L. J. Exp. Med. 191: 977-984.
30. Behbod, F., Z. S. Nagy, S. M. Stepkowski, J. Karras, C. R. Johnson, W. D. Jarvis, and R. A. Kirken. 2003. Specific inhibition of Stat5a/b promotes apoptosis of IL-2-responsive primary and tumor-derived lymphoid cells. J. Immunol. 171: 3919-3927.
31. Kirken, R. A., R. A. Erwin, D. Taub, W. J. Murphy, F. Behbod, L. Wang, F. Pericle, and W. L. Farrar. 1999. Tyrphostin AG-490 inhibits cytokine-mediated JAK3/STAT5a/b signal transduction and cellular proliferation of antigen-activated human T cells. J. Leukocyte Biol. 65: 891-899.
32. Nagy, Z. S., Y. Wang, R. A. Erwin-Cohen, J. Aradi, B. Monia, L. H. Wang, S. M. Stepkowski, H. Rui, and R. A. Kirken. 2002. Interleukin-2 family cytokines stimulate phosphorylation of the Pro-Ser-Pro motif of Stat5 transcription factors in human T cells: resistance to suppression of multiple serine kinase pathways. J. Leukocyte Biol. 72: 819-828.
33. 1 B cell lymphoma through control of cell cycle progression. Cell. Immunol. 202: 124-135.
34. Kanegane, H., A. Yachie, T. Miyawaki, and G. Tosato. 1998. EBV-NK cells interactions and lymphoproliferative disorders. Leuk. Lymphoma 29: 491-498.
35. Knecht, H., C. Berger, S. Rothenberger, B. F. Odermatt, and P. Brousset. 2001. The role of Epstein-Barr virus in neoplastic transformation. Oncology 60: 289-302.
36. Zhang, Y., J. Turkson, C. Carter-Su, T. Smithgall, A. Levitzki, A. Kraker, J. J. Krolewski, P. Medveczky, and R. Jove. 2000. Activation of Stat3 in v-Src-transformed fibroblasts requires cooperation of Jak1 kinase activity. J. Biol. Chem. 275: 24935-24944.
37. Darnell, J. E., Jr., I. M. Kerr, and G. R. Stark. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264: 1415-1421.
38. Ihle, J. N., B. A. Witthuhn, F. W. Quelle, K. Yamamoto, and O. Silvennoinen. 1995. Signaling through the hematopoietic cytokine receptors. Annu. Rev. Immunol. 13: 369-398.
39. Rui, H., J. J. Lebrun, R. A. Kirken, P. A. Kelly, and W. L. Farrar. 1994. JAK2 activation and cell proliferation induced by antibody-mediated prolactin receptor dimerization. Endocrinology 135: 1299-1306.
40. Watowich, S. S., A. Yoshimura, G. D. Longmore, D. J. Hilton, Y. Yoshimura, and H. F. Lodish. 1992. Homodimerization and constitutive activation of the erythropoietin receptor. Proc. Natl. Acad. Sci. USA 89: 2140-2144.
41. Longmore, G., S. Watowich, P. Pharr, D. Neumann, and H. Lodish. 1993. Activation of the erythropoietin receptor and leukemia induction in mice. Leukemia 7(Suppl. 2): S113-S116.
42. Robb, R. J., C. M. Rusk, J. Yodoi, and W. C. Greene. 1987. Interleukin 2 binding molecule distinct from the Tac protein: analysis of its role in formation of high-affinity receptors. Proc. Natl. Acad. Sci. USA 84: 2002-2006.
43. Teshigawara, K., H. M. Wang, K. Kato, and K. A. Smith. 1987. Interleukin 2 high-affinity receptor expression requires two distinct binding proteins. J. Exp. Med. 165: 223-238.
44. + natural killer cells after in vivo IL-2 therapy: p70 expression does not alone predict the level of intermediate affinity IL-2 binding. J. Exp. Med. 172: 1101-1114.
45. Kirken, R. A., M. G. Malabarba, J. Xu, X. Liu, W. L. Farrar, L. Hennighausen, A. C. Larner, P. M. Grimley, and H. Rui. 1997. Prolactin stimulates serine/tyrosine phosphorylation and formation of heterocomplexes of multiple Stat5 isoforms in Nb2 lymphocytes. J. Biol. Chem. 272: 14098-14103.
46. Tian, S. S., P. Lamb, H. M. Seidel, R. B. Stein, and J. Rosen. 1994. Rapid activation of the STAT3 transcription factor by granulocyte colony-stimulating factor. Blood 84: 1760-1764.
47. Qureshi, S. A., M. Salditt-Georgieff, and J. E. Darnell, Jr. 1995. Tyrosine-phosphorylated Stat1 and Stat2 plus a 48-kDa protein all contact DNA in forming interferon-stimulated-gene factor 3. Proc. Natl. Acad. Sci. USA 92: 3829-3833.
48. Bromberg, J. F., M. H. Wrzeszczynska, G. Devgan, Y. Zhao, R. G. Pestell, C. Albanese, and J. E. Darnell, Jr. 1999. Stat3 as an oncogene. Cell 98: 295-303.
49. Ellery, J. M., and P. J. Nicholls. 2002. Alternate signalling pathways from the interleukin-2 receptor. Cytokine Growth Factor Rev. 13: 27-40.
50. Lord, J. D., B. C. McIntosh, P. D. Greenberg, and B. H. Nelson. 2000. The IL-2 receptor promotes lymphocyte proliferation and induction of the c-myc, bcl-2, and bcl-x genes through the trans-activation domain of Stat5. J. Immunol. 164: 2533-2541.
51. Matikainen, S., T. Sareneva, T. Ronni, A. Lehtonen, P. J. Koskinen, and I. Julkunen. 1999. Interferon-α activates multiple STAT proteins and up-regulates proliferation-associated IL-2Rα, c-myc, and pim-1 genes in human T cells. Blood 93: 1980-1991.
52. Calo, V., M. Migliavacca, V. Bazan, M. Macaluso, M. Buscemi, N. Gebbia, and A. Russo. 2003. STAT proteins: from normal control of cellular events to tumorigenesis. J. Cell. Physiol. 197: 157-168.
53. Grandis, J. R., S. D. Drenning, A. Chakraborty, M. Y. Zhou, Q. Zeng, A. S. Pitt, and D. J. Tweardy. 1998. Requirement of Stat3 but not Stat1 activation for epidermal growth factor receptor-mediated cell growth in vitro. J. Clin. Invest. 102: 1385-1392.
54. Turkson, J., T. Bowman, J. Adnane, Y. Zhang, J. Y. Djeu, M. Sekharam, D. A. Frank, L. B. Holzman, J. Wu, S. Sebti, and R. Jove. 1999. Requirement for Ras/Rac1-mediated p38 and c-Jun N-terminal kinase signaling in Stat3 transcriptional activity induced by the Src oncoprotein. Mol. Cell. Biol. 19: 7519-7528.
55. Noguchi, T., K. Ikeda, K. Yamamoto, I. Yoshida, A. Ashiba, J. Tsuchiyama, K. Shinagawa, T. Yoshino, M. Takata, and M. Harada. 2001. Antisense oligodeoxynucleotides to latent membrane protein 1 induce growth inhibition, apoptosis and Bcl-2 suppression in Epstein-Barr virus (EBV)-transformed B-lymphoblastoid cells, but not in EBV-positive natural killer cell lymphoma cells. Br. J. Haematol. 114: 84-92.
56. Burke, W. M., X. Jin, H. J. Lin, M. Huang, R. Liu, R. K. Reynolds, and J. Lin. 2001. Inhibition of constitutively active Stat3 suppresses growth of human ovarian and breast cancer cells. Oncogene 20: 7925-7934.
57. Garcia, R., T. L. Bowman, G. Niu, H. Yu, S. Minton, C. A. Muro-Cacho, C. E. Cox, R. Falcone, R. Fairclough, S. Parsons, et al. 2001. Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 20: 2499-2513.
58. WAF1,CIP1,SDI1 gene by interleukin-6 type cytokines: a prerequisite for their pro-differentiating and anti-apoptotic effects on human osteoblastic cells. J. Biol. Chem. 273: 21137-21144.
59. Shishodia, S., and B. B. Aggarwal. 2002. Nuclear factor-κB activation: a question of life or death. J. Biochem. Mol. Biol. 35: 28-40.
60. Ruland, J., G. S. Duncan, A. Elia, I. del Barco Barrantesqq, L. Nguyen, S. Plyte, D. G. Millar, D. Bouchard, A. Wakeham, P. S. Ohashi, and T. W. Mak. 2001. Bcl10 is a positive regulator of antigen receptor-induced activation of NF-κB and neural tube closure. Cell 104: 33-42.
61. Thome, M. 2004. CARMA1, BCL-10 and MALT1 in lymphocyte development and activation. Nat. Rev. Immunol. 4: 348-359.
62. Yeh, W. C., A. Shahinian, D. Speiser, J. Kraunus, F. Billia, A. Wakeham, J. L. de la Pompa, D. Ferrick, B. Hum, N. Iscove, et al. 1997. Early lethality, functional NF-κB activation, and increased sensitivity to TNF-induced cell death in TRAF2-deficient mice. Immunity 7: 715-725.
63. Sun, L., L. Deng, C. K. Ea, Z. P. Xia, and Z. J. Chen. 2004. The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol. Cell 14: 289-301.
64. Nakano, H., S. Sakon, H. Koseki, T. Takemori, K. Tada, M. Matsumoto, E. Munechika, T. Sakai, T. Shirasawa, H. Akiba, et al. 1999. Targeted disruption of Traf5 gene causes defects in CD40- and CD27-mediated lymphocyte activation. Proc. Natl. Acad. Sci. USA 96: 9803-9808.
65. Chung, J. Y., Y. C. Park, H. Ye, and H. Wu. 2002. All TRAFs are not created equal: common and distinct molecular mechanisms of TRAF-mediated signal transduction. J. Cell Sci. 115: 679-688.
66. Hauer, J., S. Puschner, P. Ramakrishnan, U. Simon, M. Bongers, C. Federle, and H. Engelmann. 2005. TNF receptor (TNFR)-associated factor (TRAF) 3 serves as an inhibitor of TRAF2/5-mediated activation of the noncanonical NF-κB pathway by TRAF-binding TNFRs. Proc. Natl. Acad. Sci. USA 102: 2874-2879.
67. Lyss, G., T. J. Schmidt, I. Merfort, and H. L. Pahl. 1997. Helenalin, an antiinflammatory sesquiterpene lactone from Arnica, selectively inhibits transcription factor NF-κB. Biol. Chem. 378: 951-961.