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Volume 271, Number 32, Issue of August 9, 1996 pp. 19443-19450
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.

Role of c-Src Tyrosine Kinase in G Protein-coupled Receptorand Gbeta gamma Subunit-mediated Activation of Mitogen-activated Protein Kinases

(Received for publication, March 1, 1996, and in revised form, May 10, 1996)

Louis M. Luttrell Dagger , Brian E. Hawes Dagger , Tim van Biesen Dagger , Deirdre K. Luttrell , Timothy J. Lansing and Robert J. Lefkowitz Dagger

From the Dagger  The Howard Hughes Medical Institute and the Departments of Medicine and Biochemistry, Duke University Medical Center, Durham, North Carolina 27710 and the  Department of Molecular Cell Biology, Glaxo Wellcome Inc., Research Triangle Park, North Carolina 27709

Several G protein-coupled receptors that interact with pertussis toxin-sensitive heterotrimeric G proteins mediate Ras-dependent activation of mitogen-activated protein (MAP) kinases. The mechanism involves Gbeta gamma subunit-mediated increases in tyrosine phosphorylation of the Shc adapter protein, Shc·Grb2 complex formation, and recruitment of Ras guanine nucleotide exchange factor activity. We have investigated the role of the ubiquitous nonreceptor tyrosine kinase c-Src in activation of the MAP kinase pathway via endogenous G protein-coupled lysophosphatidic acid (LPA) receptors or by transient expression of Gbeta gamma subunits in COS-7 cells. In vitro kinase assays of Shc immunoprecipitates following LPA stimulation demonstrated rapid, transient recruitment of tyrosine kinase activity into Shc immune complexes. Recruitment of tyrosine kinase activity was pertussis toxin-sensitive and mimicked by cellular expression of Gbeta gamma subunits. Immunoblots for coprecipitated proteins in Shc immunoprecipitates revealed a transient association of Shc and c-Src following LPA stimulation, which coincided with increases in Shc-associated tyrosine kinase activity and Shc tyrosine phosphorylation. LPA stimulation or expression of Gbeta gamma subunits resulted in c-Src activation, as assessed by increased c-Src autophosphorylation. Overexpression of wild-type or constitutively active mutant c-Src, but not kinase inactive mutant c-Src, lead to increased tyrosine kinase activity in Shc immunoprecipitates, increased Shc tyrosine phosphorylation, and Shc·Grb2 complex formation. MAP kinase activation resulting from LPA receptor stimulation, expression of Gbeta gamma subunits, or expression of c-Src was sensitive to dominant negatives of mSos, Ras, and Raf. Coexpression of Csk, which inactivates Src family kinases by phosphorylating the regulatory C-terminal tyrosine residue, inhibited LPA stimulation of Shc tyrosine phosphorylation, Shc·Grb2 complex formation, and MAP kinase activation. These data suggest that Gbeta gamma subunit-mediated formation of Shc·c-Src complexes and c-Src kinase activation are early events in Ras-dependent activation of MAP kinase via pertussis toxin-sensitive G protein-coupled receptors.


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