Stat3 is required for full neoplastic transformation by the Simian Virus 40 Large Tumor antigen

Molecular Biology of the Cell

Volumn 16, Issue 8, 2005, Pages 3832-3846

  Vultur, Adina ^a   Arulanandam, Rozanne ^a   Turkson, James ^b   Niu, Guilian ^b   Jove, Richard ^b   Raptis, Leda ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; JANUS KINASE; PROTEIN TYROSINE KINASE; RETINOBLASTOMA PROTEIN; SMALL INTERFERING RNA; SOMATOMEDIN RECEPTOR; STAT3 PROTEIN; VIRUS LARGE T ANTIGEN;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL ADHESION; CELL TRANSFORMATION; ENZYME INACTIVATION; FIBROBLAST; GENE DISRUPTION; GENETIC RECOMBINATION; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; SIMIAN VIRUS 40;

ANIMALS; ANTIGENS, VIRAL, TUMOR; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; PHOSPHOTYROSINE; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; RETINOBLASTOMA PROTEIN; RNA, SMALL INTERFERING; SIMIAN VIRUS 40; UP-REGULATION;

MURINAE; SIMIAN VIRUS 40;

EID: 23044447001     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-12-1104     Document Type: Article

References (61)

1. Akira, S. (2000). Roles of STAT3 defined by tissue-specific gene targeting. Oncogene 19, 2607-2611.
2. Angers-Loustau, A., Hering, R., Werbowetski, T. E., Kaplan, D. R., and Del Maestro, R. F. (2004). SRC regulates actin dynamics and invasion of malignant glial cells in three dimensions. Mol. Cancer Res. 2, 595-605.
3. Arulanandam, R., Vultur, A., and Raptis, L. (2005). Transfection techniques affecting Stat3 activity levels. Anal. Biochem. 338, 83-89.
4. Bromberg, J. F., Horvath, C. M., Besser, D., Lathem, W. W., and Darnell, J. E., Jr. (1998). Stat3 activation is required for cellular transformation by v-src. Mol. Cell. Biol. 18, 2553-2558.
5. Bromberg, J. F., Wrzeszczynska, M. H., Devgan, G., Zhao, Y., Pestell, R. G., Albanese, C., and Darnell, J. E., Jr. (1999). Stat3 as an oncogene. Cell 98, 295-303.
6. Calalb, M. B., Zhang, X., Polte, T. R., and Hanks, S. K. (1996). Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem. Biophys. Res. Commun. 228, 662-668.
7. Catlett-Falcone, R. et al. (1999). Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 10, 105-115.
8. Chau, B. N., and Wang, J. Y. (2003). Coordinated regulation of life and death by RB. Nat. Rev. Cancer 3, 130-138.
9. Ciardiello, F., Valverius, E. M., Colucci-D'Amato, G. L., Kim, N., Bassin, R. H., and Salomon, D. S. (1990). Differential growth factor expression in transformed mouse NIH-3T3 cells. J. Cell Biochem. 42, 45-57.
10. Cirri, P., Chiarugi, P., Marra, F., Raugei, G., Camici, G., Manao, G., and Ramponi, G. (1997). c-Src activates both STAT1 and STAT3 in PDGF-stimulated NIH3T3 cells. Biochem. Biophys. Res. Commun. 239, 493-497.
11. Classon, M., and Dyson, N. (2001). p107 and p130, versatile proteins with interesting pockets. Exp. Cell Res. 264, 135-147.
12. Daniels, C. E., Wilkes, M. C., Edens, M., Kottom, T. J., Murphy, S. J., Limper, A. H., and Leof, E. B. (2004). Imatinib mesylate inhibits the profibrogenic activity of TGF-beta and prevents bleomycin-mediated lung fibrosis. J. Clin. Invest. 114, 1308-1316.
13. Epling-Burnette, P. K. et al. (2001). Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl1 expression. J. Clin. Invest. 107, 351-362.
14. Fei, Z. L., D'Ambrosio, C., Li, S., Surmacz, E., and Baserga, R. (1995). Association of insulin receptor substrate 1 with simian virus 40 large T antigen. Mol. Cell. Biol. 15, 4232-4239.
15. Gabarra-Niecko, V., Schaller, M. D., and Dunty, J. M. (2003). FAK regulates biological processes important for the pathogenesis of cancer. Cancer Metastasis Rev. 22, 359-374.
16. Garcia, R. 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.
17. Grammatikakis, N. et al. (2001). Simian Virus 40 large Tumor antigen modulates the Raf signaling pathway. J. Biol. Chem. 276, 27840-27845.
18. Grammatikakis, N., Vultur, A., Ramana, C. V., Siganou, A., Schweinfest, C. W., and Raptis, L. (2002). The role of Hsp90N, a new member of the Hsp90 family, in signal transduction and neoplastic transformation. J. Biol. Chem. 277, 8312-8320.
19. Grandis, J. R., Drenning, S. D., Zeng, Q., Watkins, S. C., Melhem, M. F., Endo, S., Johnson, D. E., Huang, L., He, Y., Kim, J. D. (2000). Constitutive activation of Stat3 signaling abrogates apoptosis in squamous cell carcinogenesis in vivo. Proc. Natl. Acad. Sci. USA 97, 4227-4232.
20. Greer, P. (2002). Closing in on the biological functions of Fps/Fes and Fer. Nat. Rev. Mol. Cell Biol. 3, 278-289.
21. He, T. C., Zhou, S., da Costa, L. T., Yu, J., Kinzler, K. W., and Vogelstein, B. (1998). A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95, 2509-2514.
22. Huang, M. et al. (2002). Inhibition of Bcr-Abl kinase activity by PD180970 blocks constitutive activation of Stat5 and growth of CML cells. Oncogene 21, 8804-8816.
23. Hung, W., and Elliott, B. (2001). Co-operative effect of c-Src tyrosine kinase and Stat3 in activation of hepatocyte growth factor expression in mammary carcinoma cells. J. Biol. Chem. 276, 12395-12403.
24. Johnston, J. A., Kawamura, M., Kirken, R. A., Chen, Y. Q., Blake, T. B., Shibuya, K., Ortaldo, J. R., McVicar, D. W., and O'Shea, J. J. (1994). Phosphorylation and activation of the Jak-3 Janus kinase in response to interleukin-2. Nature 370, 151-153.
25. Kaplan, P. L., and Ozanne, B. (1982). Polyoma virus transformed cells produce transforming growth factors and grow in serum-free medium. Virology 123, 372-380.
26. Levy, D. E., and Darnell, J. E., Jr. (2002). Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 3, 651-662.
27. Lin, J., Jin, X., Rothman, K., Lin, H. J., Tang, H., and Burke, W. (2002a). Modulation of signal transducer and activator of transcription 3 activities by p53 tumor suppressor in breast cancer cells. Cancer Res. 62, 376-380.
28. Lin, J., Tang, H., Jin, X., Jia, G., and Hsieh, J. T. (2002b). p53 regulates Stat3 phosphorylation and DNA binding activity in human prostate cancer cells expressing constitutively active Stat3. Oncogene 21, 3082-3088.
29. Mauro, L., Salerno, M., Morelli, C., Boterberg, T., Bracke, M. E., and Surmacz, E. (2003). Role of the IGF-1 receptor in the regulation of cell-cell adhesion: implications in cancer development and progression. J. Cell Physiol. 194, 108-116.
30. McLemore, M. L., Grewal, S., Liu, F., Archambault, A., Poursine-Laurent, J., Haug, J., and Link, D. C. (2001). STAT-3 activation is required for normal G-CSF-dependent proliferation and granulocytic differentiation. Immunity 14, 193-204.
31. Narimatsu, M. 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.
32. Nimmanapalli, R., O'Bryan, E., Huang, M., Bali, P., Burnette, P. K., Loughran, T., Tepperberg, J., Jove, R., Bhalla, K. (2002). Molecular characterization and sensitivity of STI-571 (imatinib mesylate, Gleevec)-resistant, Bcr-Abl-positive, human acute leukemia cells to SRC kinase inhibitor PD180970 and 17-allylamino-17-demethoxygeldanamycin. Cancer Res. 62, 5761-5769.
33. Okada, M., Nada, S., Yamanashi, Y., Yamamoto, T., and Nakagawa, H. (1991). CSK: a protein-tyrosine kinase involved in regulation of src family kinases. J. Biol. Chem. 266, 24249-24252.
34. Olayioye, M. A., Beuvink, I., Horsch, K., Daly, J. M., and Hynes, N. E. (1999). ErbB receptor-induced activation of stat transcription factors is mediated by Src tyrosine kinases. J. Biol. Chem. 274, 17209-17218.
35. Porcu, P., Grana, X., Li, S., Swantek, J., De Luca, A., Giordano, A., Baserga, R. (1994). An E2F binding sequence negatively regulates the response of the insulin-like growth factor 1 (IGF-I) promoter to simian virus 40T antigen and to serum. Oncogene 9, 2125-2134.
36. Radna, R. L., Canton, Y., Jha, K. K., Kaplan, P., Li, G., Tranganos, R., and Ozer, H. L. (1989). Growth of immortalized Simian Virus 40 tsA-transformed human fibroblasts is temperature dependent. Mol. Cell. Biol. 9, 3093-3096.
37. Raptis, L., Brownell, H. L., Vultur, A. M., Ross, G., Tremblay, E., and Elliott, B. E. (2000). Specific inhibition of growth factor-stimulated ERK1/2 activation in intact cells by electroporation of a Grb2-SH2 binding peptide. Cell Growth Differ. 11, 293-303.
38. Raptis, L., Brownell, H. L., Wood, K., Corbley, M., Wang, D., and Haliotis, T. (1997a). Cellular ras gene activity is required for full neoplastic transformation by Simian Virus 40. Cell Growth Differ. 8, 891-901.
39. Raptis, L., Lamfrom, H., and Benjamin, T. L. (1985). Regulation of cellular phenotype and expression of polyomavirus middle T antigen in rat fibroblasts. Mol. Cell. Biol. 5, 2476-2486.
40. leu61 blocks differentiation of transformable 3T3 L1 and C3HT1/2derived preadipocytes in a dose- and time-dependent manner. Cell Growth Differ. 8, 11-21.
41. Rothen-Rutishauser, B., Riesen, F. K., Braun, A., Gunthert, M., and Wunderli-Allenspach, H. (2002). Dynamics of tight and adherens junctions under EGTA treatment. J. Membr. Biol. 188, 151-162.
42. Sage, J., Mulligan, G. J., Attardi, L. D., Miller, A., Chen, S., Williams, B., Theodorou, E., and Jacks, T. (2000). Targeted disruption of the three Rb-related genes leads to loss of G(1) control and immortalization. Genes Dev. 14, 3037-3050.
43. Sears, R. C., and Nevins, J. R. (2002). Signaling networks that link cell proliferation and cell fate. J. Biol. Chem. 277, 11617-11620.
44. Sell, C., Dumenil, G., Deveaud, C., Miura, M., Coppola, D., DeAngelis, T., Rubin, R., Efstratiadis, A., and Baserga, R. (1994). Effect of a null mutation of the insulin-like growth factor I receptor gene on growth and transformation of mouse embryo fibroblasts. Mol. Cell. Biol. 14, 3604-3612.
45. Sullivan, C. S., and Pipas, J. M. (2002). T antigens of simian virus 40, molecular chaperones for viral replication and tumorigenesis. Microbiol. Mol. Biol. Rev. 66, 179-202.
46. Tedesco, D., Fischer-Fantuzzi, L., and Vesco, C. (1993). Limits of transforming competence of SV40 nuclear and cytoplasmic large T mutants with altered Rb binding sequences. Oncogene 8, 549-557.
47. Trimarchi, J. M., and Lees, J. A. (2002). Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 3, 11-20.
48. 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.
49. Turkson, J., Kim, J. S., Zhang, S., Yuan, J., Huang, M., Glenn, M., Haura, E., Sebti, S., Hamilton, A. D., and Jove, R. (2004). Novel peptidomimetic inhibitors of signal transducer and activator of transcription 3 dimerization and biological activity. Mol. Cancer Ther. 3, 261-269.
50. Turkson, J., Ryan, D., Kim, J. S., Zhang, Y., Chen, Z., Haura, E., Laudano, A., Sebti, S., Hamilton, A. D., and Jove, R. (2001). Phosphotyrosyl peptides block Stat3-mediated DNA binding activity, gene regulation, and cell transformation. J. Biol. Chem. 276, 45443-45455.
51. Vignais, M. L., and Gilman, M. (1999). Distinct mechanisms of activation of Stat1 and Stat3 by PDGF receptor in a cell-free system. Mol. Cell. Biol. 19, 3727-3735.
52. Vignais, M. L., Sadowski, H. B., Watling, D., Rogers, N. C., and Gilman, M. (1996). PDGF induces phosphorylation of multiple JAK family kinases and STAT proteins. Mol. Cell. Biol. 16, 1759-1769.
53. Vultur, A., Cao, J., Arulanandam, R., Turkson, J., Jove, R., Greer, P., Craig, A., Elliott, B. E., and Raptis, L. (2004). Cell to cell adhesion modulates Stat3 activity in normal and breast carcinoma cells. Oncogene 23, 2600-2616.
54. Wagner, B. J., Hayes, T. E., Hoban, C. J., and Cochran, B. H. (1990). The SIF binding element confers sis/platelet-derived growth factor inducibility onto the c-fos promoter. EMBO J. 9, 4477-4484.
55. Wang, Y. Z., Wharton, W., Garcia, R., Kraker, A., Jove, R., and Pledger, W. J. (2000). Activation of Stat3 preassembled with PDGF beta receptors requires Src kinase activity. Oncogene 19, 2075-2085.
56. Witthuhn, B. A., Silvennoinen, O., Miura, O., Lai, K. S., Cwik, C., Liu, E. T., and Ihle, J. N. (1994). Involvement of the Jak-3 Janus kinase in signalling by interleukins 2 and 4 in lymphoid and myeloid cells. Nature 370, 153-157.
57. Young, A. P., Nagarajan, R., and Longmore, G. D. (2003). Mechanisms of transcriptional regulation by Rb-E2F segregate by biological pathway. Oncogene 22, 7209-7217.
58. Yu, C. L., Meyer, D. J., Campbell, G. S., Lamer, 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.
59. Yu, H., and Jove, R. (2004). The STATs of cancer-new molecular targets come of age. Nat. Rev. Cancer 4, 97-105.
60. Zalvide, J., Stubdal, H., and DeCaprio, J. A. (1998). The J domain of Simian Virus 40 Large Tumor antigen is required to functionally inactivate Rb family proteins. Mol. Cell. Biol. 18, 1408-1415.
61. Zhang, Y., Turkson, J., Carter-Su, C., Smithgall, T., Levitzki, A., Kraker, A., Krolewski, J. J., Medveczky, P., and Jove, R. (2000). Activation of Stat3 in v-Src transformed fibroblasts requires cooperation of Jak1 kinase activity. J. Biol. Chem. 275, 24935-24944.