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Subunit-mediated Activation of Mitogen-activated
Protein Kinases
(Received for publication, March 1, 1996, and in revised form, May 10, 1996)
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From the 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 G
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
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 G 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 G 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 G 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 G 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 G 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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