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Mol Cell Biol, May 1998, p. 2545-2552, Vol. 18, No. 5
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Stat3 Activation by Src Induces Specific Gene Regulation and Is Required for Cell Transformation

James Turkson,1 Tammy Bowman,1 Roy Garcia,1 Eric Caldenhoven,2 Rolf P. De Groot,2 and Richard Jove1,*

Molecular Oncology Program, H. Lee Moffitt Cancer Center and Research Institute, and Department of Biochemistry and Molecular Biology, University of South Florida College of Medicine, Tampa, Florida 33612,1 and Department of Pulmonary Diseases, University Hospital Utrecht, Heidelberglaan, 3584 CX Utrecht, The Netherlands2

Received 16 September 1997/Returned for modification 13 November 1997/Accepted 30 January 1998

While signal transducers and activators of transcription (STATs) were originally discovered as intracellular effectors of normal signaling by cytokines, increasing evidence also points to a role for STAT transcription factors in oncogenesis. Previous studies have demonstrated that one STAT family member, Stat3, possesses constitutively elevated tyrosine phosphorylation and DNA-binding activity in fibroblasts stably transformed by the Src oncoprotein. To determine if this Stat3 activation by Src could induce Stat3-mediated gene expression, luciferase reporter constructs based on synthetic and authentic promoters were transfected into NIH 3T3 cells. Activation of endogenous cellular Stat3 by the Src oncoprotein induced gene expression through a Stat3-specific binding element (TTCCCGAA) of the C-reactive protein gene promoter. A naturally occurring splice variant of human Stat3 protein, Stat3beta , with a deletion in the C-terminal transactivation domain abolished this gene induction in a dominant negative manner. Expression of Stat3beta did not have any effect on a reporter construct based on the c-fos serum response element, which is not dependent on Stat3 signaling, indicating that Stat3beta does not nonspecifically inhibit other signaling pathways or Src function. Transfection of vectors expressing Stat3beta together with Src blocked cell transformation by Src as measured in a quantitative focus formation assay using NIH 3T3 cells. By contrast, Stat3beta had a much less pronounced effect on focus formation induced by the Ras oncoprotein, which does not activate Stat3 signaling. In addition, three independent clones of NIH 3T3 cells stably overexpressing Stat3beta were generated and characterized, demonstrating that Stat3beta overexpression does not have a toxic effect on cell viability. These Stat3beta -overexpressing clones were shown to be deficient in Stat3-mediated signaling and refractory to Src-induced cell transformation. We conclude that Stat3 activation by the Src oncoprotein leads to specific gene regulation and that Stat3 is one of the critical signaling pathways involved in Src oncogenesis. Our findings provide evidence that oncogenesis-associated activation of Stat3 signaling is part of the process of malignant transformation.

* Corresponding author. Mailing address: Molecular Oncology Program, Moffitt Cancer Center and Research Institute, 12902 Magnolia Dr., Tampa, FL 33612. Phone: (813) 979-6725. Fax: (813) 979-6700. E-mail: richjove{at}moffitt.usf.edu.

Mol Cell Biol, May 1998, p. 2545-2552, Vol. 18, No. 5
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


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  • Chen, H., Hutt-Fletcher, L., Cao, L., Hayward, S. D. (2003). A Positive Autoregulatory Loop of LMP1 Expression and STAT Activation in Epithelial Cells Latently Infected with Epstein-Barr Virus. J. Virol. 77: 4139-4148 [Abstract] [Full Text]  
  • Leong, P. L., Andrews, G. A., Johnson, D. E., Dyer, K. F., Xi, S., Mai, J. C., Robbins, P. D., Gadiparthi, S., Burke, N. A., Watkins, S. F., Grandis, J. R. (2003). Targeted inhibition of Stat3 with a decoy oligonucleotide abrogates head and neck cancer cell growth. Proc. Natl. Acad. Sci. USA 100: 4138-4143 [Abstract] [Full Text]  
  • Minoguchi, M., Minoguchi, S., Aki, D., Joo, A., Yamamoto, T., Yumioka, T., Matsuda, T., Yoshimura, A. (2003). STAP-2/BKS, an Adaptor/Docking Protein, Modulates STAT3 Activation in Acute-phase Response through Its YXXQ Motif. J. Biol. Chem. 278: 11182-11189 [Abstract] [Full Text]  
  • Ravandi, F., Talpaz, M., Estrov, Z. (2003). Modulation of Cellular Signaling Pathways: Prospects for Targeted Therapy in Hematological Malignancies. Clin. Cancer Res. 9: 535-550 [Abstract] [Full Text]  
  • Dolled-Filhart, M., Camp, R. L., Kowalski, D. P., Smith, B. L., Rimm, D. L. (2003). Tissue Microarray Analysis of Signal Transducers and Activators of Transcription 3 (Stat3) and Phospho-Stat3 (Tyr705) in Node-negative Breast Cancer Shows Nuclear Localization Is Associated with a Better Prognosis. Clin. Cancer Res. 9: 594-600 [Abstract] [Full Text]  
  • Kloth, M. T., Laughlin, K. K., Biscardi, J. S., Boerner, J. L., Parsons, S. J., Silva, C. M. (2003). STAT5b, a Mediator of Synergism between c-Src and the Epidermal Growth Factor Receptor. J. Biol. Chem. 278: 1671-1679 [Abstract] [Full Text]  
  • Glozak, M. A., Li, Y., Reuille, R., Kim, K. H., Vo, M.-N., Rogers, M. B. (2003). Trapping and Characterization of Novel Retinoid Response Elements. Mol. Endocrinol. 17: 27-41 [Abstract] [Full Text]  
  • Alas, S., Bonavida, B. (2003). Inhibition of Constitutive STAT3 Activity Sensitizes Resistant Non-Hodgkin's Lymphoma and Multiple Myeloma to Chemotherapeutic Drug-mediated Apoptosis. Clin. Cancer Res. 9: 316-326 [Abstract] [Full Text]  
  • Scoles, D. R., Nguyen, V. D., Qin, Y., Sun, C.-X., Morrison, H., Gutmann, D. H., Pulst, S.-M. (2002). Neurofibromatosis 2 (NF2) tumor suppressor schwannomin and its interacting protein HRS regulate STAT signaling. Hum Mol Genet 11: 3179-3189 [Abstract] [Full Text]  
  • Krause, A., Scaletta, N., Ji, J.-D., Ivashkiv, L. B. (2002). Rheumatoid Arthritis Synoviocyte Survival Is Dependent on Stat3. J. Immunol. 169: 6610-6616 [Abstract] [Full Text]  
  • Mora, L. B., Buettner, R., Seigne, J., Diaz, J., Ahmad, N., Garcia, R., Bowman, T., Falcone, R., Fairclough, R., Cantor, A., Muro-Cacho, C., Livingston, S., Karras, J., Pow-Sang, J., Jove, R. (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 [Abstract] [Full Text]  
  • Schreiner, S. J., Schiavone, A. P., Smithgall, T. E. (2002). Activation of STAT3 by the Src Family Kinase Hck Requires a Functional SH3 Domain. J. Biol. Chem. 277: 45680-45687 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Bjornstrom, L., Sjoberg, M. (2002). Signal Transducers and Activators of Transcription as Downstream Targets of Nongenomic Estrogen Receptor Actions. Mol. Endocrinol. 16: 2202-2214 [Abstract] [Full Text]  
  • Velichko, S., Wagner, T. C., Turkson, J., Jove, R., Croze, E. (2002). STAT3 Activation by Type I Interferons Is Dependent on Specific Tyrosines Located in the Cytoplasmic Domain of Interferon Receptor Chain 2c. ACTIVATION OF MULTIPLE STATS PROCEEDS THROUGH THE REDUNDANT USAGE OF TWO TYROSINE RESIDUES. J. Biol. Chem. 277: 35635-35641 [Abstract] [Full Text]  
  • Yoshida, T., Hanada, T., Tokuhisa, T., Kosai, K.-i., Sata, M., Kohara, M., Yoshimura, A. (2002). Activation of STAT3 by the Hepatitis C Virus Core Protein Leads to Cellular Transformation. JEM 196: 641-653 [Abstract] [Full Text]  
  • Tarn, C., Zou, L., Hullinger, R. L., Andrisani, O. M. (2002). Hepatitis B Virus X Protein Activates the p38 Mitogen-Activated Protein Kinase Pathway in Dedifferentiated Hepatocytes. J. Virol. 76: 9763-9772 [Abstract] [Full Text]  
  • Sato, K.-i., Nagao, T., Kakumoto, M., Kimoto, M., Otsuki, T., Iwasaki, T., Tokmakov, A. A., Owada, K., Fukami, Y. (2002). Adaptor Protein Shc Is an Isoform-specific Direct Activator of the Tyrosine Kinase c-Src. J. Biol. Chem. 277: 29568-29576 [Abstract] [Full Text]  
  • Shen, R., Kaplan, M. H. (2002). The Homeostasis But Not the Differentiation of T Cells Is Regulated by p27Kip1. J. Immunol. 169: 714-721 [Abstract] [Full Text]  
  • Abreu, M. T., Arnold, E. T., Thomas, L. S., Gonsky, R., Zhou, Y., Hu, B., Arditi, M. (2002). TLR4 and MD-2 Expression Is Regulated by Immune-mediated Signals in Human Intestinal Epithelial Cells. J. Biol. Chem. 277: 20431-20437 [Abstract] [Full Text]  
  • Li, L., Shaw, P. E. (2002). Autocrine-mediated Activation of STAT3 Correlates with Cell Proliferation in Breast Carcinoma Lines. J. Biol. Chem. 277: 17397-17405 [Abstract] [Full Text]  
  • Sachdev, P., Zeng, L., Wang, L. H. (2002). Distinct Role of Phosphatidylinositol 3-Kinase and Rho Family GTPases in Vav3-induced Cell Transformation, Cell Motility, and Morphological Changes. J. Biol. Chem. 277: 17638-17648 [Abstract] [Full Text]  
  • Haq, R., Halupa, A., Beattie, B. K., Mason, J. M., Zanke, B. W., Barber, D. L. (2002). Regulation of Erythropoietin-induced STAT Serine Phosphorylation by Distinct Mitogen-activated Protein Kinases. J. Biol. Chem. 277: 17359-17366 [Abstract] [Full Text]  


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