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Molecular and Cellular Biology, November 1999, p. 7519-7528, Vol. 19, No. 11
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Requirement for Ras/Rac1-Mediated p38 and c-Jun N-Terminal Kinase Signaling in Stat3 Transcriptional Activity Induced by the Src Oncoprotein

James Turkson,1,2 Tammy Bowman,1,2 Jalila Adnane,2,3 Yi Zhang,1,2 Julie Y. Djeu,2,4 Madhavi Sekharam,1,5 David A. Frank,6 Lawrence B. Holzman,7 Jie Wu,1,2,5 Said Sebti,2,3 and Richard Jove1,2,*

Molecular Oncology,1 Drug Discovery,3 and Immunology4 Programs, Moffitt Cancer Center and Research Institute, Department of Biochemistry and Molecular Biology,2 and Department of Medical Microbiology and Immunology,5 University of South Florida College of Medicine, Tampa, Florida 33612; Department of Adult Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts 021156; and Department of Internal Medicine, University of Michigan Medical School, Ann Arbor, Michigan 481097

Received 19 February 1999/Returned for modification 20 April 1999/Accepted 5 August 1999

Signal transducers and activators of transcription (STATs) are transcription factors that mediate normal biologic responses to cytokines and growth factors. However, abnormal activation of certain STAT family members, including Stat3, is increasingly associated with oncogenesis. In fibroblasts expressing the Src oncoprotein, activation of Stat3 induces specific gene expression and is required for cell transformation. Although the Src tyrosine kinase induces constitutive Stat3 phosphorylation on tyrosine, activation of Stat3-mediated gene regulation requires both tyrosine and serine phosphorylation of Stat3. We investigated the signaling pathways underlying the constitutive Stat3 activation in Src oncogenesis. Expression of Ras or Rac1 dominant negative protein blocks Stat3-mediated gene regulation induced by Src in a manner consistent with dependence on p38 and c-Jun N-terminal kinase (JNK). Both of these serine/threonine kinases and Stat3 serine phosphorylation are constitutively induced in Src-transformed fibroblasts. Furthermore, inhibition of p38 and JNK activities suppresses constitutive Stat3 serine phosphorylation and Stat3-mediated gene regulation. In vitro kinase assays with purified full-length Stat3 as the substrate show that both JNK and p38 can phosphorylate Stat3 on serine. Moreover, inhibition of p38 activity and thus of Stat3 serine phosphorylation results in suppression of transformation by v-Src but not v-Ras, consistent with a requirement for Stat3 serine phosphorylation in Src transformation. Our results demonstrate that Ras- and Rac1-mediated p38 and JNK signals are required for Stat3 transcriptional activity induced by the Src oncoprotein. These findings delineate a network of tyrosine and serine/threonine kinase signaling pathways that converge on Stat3 in the context of oncogenesis.

* Corresponding author. Mailing address: Molecular Oncology Program, Moffitt Cancer Center, 12902 Magnolia Dr., Tampa, FL 33612. Phone: (813) 979-6725. Fax: (813) 632-1436. E-mail: richjove{at}moffitt.usf.edu.

Molecular and Cellular Biology, November 1999, p. 7519-7528, Vol. 19, No. 11
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


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