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(Received for publication, March 1, 1996, and in revised form, May 10, 1996)
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
Volume 271, Number 32,
Issue of August 9, 1996
pp. 19443-19450
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.
Subunit-mediated Activation of Mitogen-activated
Protein Kinases
,
,
,
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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 E. Shumay, X. Song, H.-y. Wang, and C. C. Malbon pp60Src Mediates Insulin-stimulated Sequestration of the beta 2-Adrenergic Receptor: Insulin Stimulates pp60Src Phosphorylation and Activation Mol. Biol. Cell, November 1, 2002; 13(11): 3943 - 3954. [Abstract] [Full Text] [PDF]
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 A. Sabri, J. Short, J. Guo, and S. F. Steinberg Protease-Activated Receptor-1-Mediated DNA Synthesis in Cardiac Fibroblast Is via Epidermal Growth Factor Receptor Transactivation: Distinct PAR-1 Signaling Pathways in Cardiac Fibroblasts and Cardiomyocytes Circ. Res., September 20, 2002; 91(6): 532 - 539. [Abstract] [Full Text] [PDF]
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 A. Ptasznik, E. Urbanowska, S. Chinta, M. A. Costa, B. A. Katz, M. A. Stanislaus, G. Demir, D. Linnekin, Z. K. Pan, and A. M. Gewirtz Crosstalk Between BCR/ABL Oncoprotein and CXCR4 Signaling through a Src Family Kinase in Human Leukemia Cells J. Exp. Med., September 2, 2002; 196(5): 667 - 678. [Abstract] [Full Text] [PDF]
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S. Dalle, T. Imamura, D. W. Rose, D. S. Worrall, S. Ugi, C. J. Hupfeld, and J. M. Olefsky Insulin Induces Heterologous Desensitization of G Protein-Coupled Receptor and Insulin-Like Growth Factor I Signaling by Downregulating {beta}-Arrestin-1 Mol. Cell. Biol., September 1, 2002; 22(17): 6272 - 6285. [Abstract] [Full Text] [PDF]
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J. Kim, A. D. Eckhart, S. Eguchi, and W. J. Koch beta -Adrenergic Receptor-mediated DNA Synthesis in Cardiac Fibroblasts Is Dependent on Transactivation of the Epidermal Growth Factor Receptor and Subsequent Activation of Extracellular Signal-regulated Kinases J. Biol. Chem., August 23, 2002; 277(35): 32116 - 32123. [Abstract] [Full Text] [PDF]
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 P. Robin, I. Boulven, C. Desmyter, S. Harbon, and D. Leiber ET-1 stimulates ERK signaling pathway through sequential activation of PKC and Src in rat myometrial cells Am J Physiol Cell Physiol, July 1, 2002; 283(1): C251 - C260. [Abstract] [Full Text] [PDF]
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 A. C. B. Cato, A. Nestl, and S. Mink Rapid Actions of Steroid Receptors in Cellular Signaling Pathways Sci. Signal., June 25, 2002; 2002(138): re9 - re9. [Abstract] [Full Text] [PDF]
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A. Yart, S. Roche, R. Wetzker, M. Laffargue, N. Tonks, P. Mayeux, H. Chap, and P. Raynal A Function for Phosphoinositide 3-Kinase beta Lipid Products in Coupling beta gamma to Ras Activation in Response to Lysophosphatidic Acid J. Biol. Chem., June 7, 2002; 277(24): 21167 - 21178. [Abstract] [Full Text] [PDF]
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D. Liu and J. S. Dillon Dehydroepiandrosterone Activates Endothelial Cell Nitric-oxide Synthase by a Specific Plasma Membrane Receptor Coupled to Galpha i2,3 J. Biol. Chem., June 7, 2002; 277(24): 21379 - 21388. [Abstract] [Full Text] [PDF]
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M. J. Smit, D. Verzijl, P. Casarosa, M. Navis, H. Timmerman, and R. Leurs Kaposi's Sarcoma-Associated Herpesvirus-Encoded G Protein-Coupled Receptor ORF74 Constitutively Activates p44/p42 MAPK and Akt via Gi and Phospholipase C-Dependent Signaling Pathways J. Virol., February 15, 2002; 76(4): 1744 - 1752. [Abstract] [Full Text] [PDF]
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 M. Mendez and M. C. LaPointe Trophic Effects of the Cyclooxygenase-2 Product Prostaglandin E2 in Cardiac Myocytes Hypertension, February 1, 2002; 39(2): 382 - 388. [Abstract] [Full Text] [PDF]
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 S. Paruchuri, B. Hallberg, M. Juhas, C. Larsson, and A. Sjolander Leukotriene D4 activates MAPK through a Ras-independent but PKC{epsilon}-dependent pathway in intestinal epithelial cells J. Cell Sci., January 5, 2002; 115(9): 1883 - 1893. [Abstract] [Full Text] [PDF]
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L. M. Luttrell and R. J. Lefkowitz The role of {beta}-arrestins in the termination and transduction of G-protein-coupled receptor signals J. Cell Sci., January 2, 2002; 115(3): 455 - 465. [Abstract] [Full Text] [PDF]
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C. A. Singer, S. Vang, and W. T. Gerthoffer Coupling of M2 muscarinic receptors to Src activation in cultured canine colonic smooth muscle cells Am J Physiol Gastrointest Liver Physiol, January 1, 2002; 282(1): G61 - G68. [Abstract] [Full Text] [PDF]
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R. D. Peavy, M. S. S. Chang, E. Sanders-Bush, and P. J. Conn Metabotropic Glutamate Receptor 5-Induced Phosphorylation of Extracellular Signal-Regulated Kinase in Astrocytes Depends on Transactivation of the Epidermal Growth Factor Receptor J. Neurosci., December 15, 2001; 21(24): 9619 - 9628. [Abstract] [Full Text] [PDF]
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 I. Faerge, B. Terry, J. Kalous, P. Wahl, M. Lessl, J.L. Ottesen, P. Hyttel, and C. Grondahl Resumption of Meiosis Induced by Meiosis-Activating Sterol Has a Different Signal Transduction Pathway than Spontaneous Resumption of Meiosis in Denuded Mouse Oocytes Cultured In Vitro Biol Reprod, December 1, 2001; 65(6): 1751 - 1758. [Abstract] [Full Text] [PDF]
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E. S. Gilmore, M. J. Stutts, and S. L. Milgram Src Family Kinases Mediate Epithelial Na+ Channel Inhibition by Endothelin J. Biol. Chem., November 2, 2001; 276(45): 42610 - 42617. [Abstract] [Full Text] [PDF]
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J. N. Hislop, H. M. Everest, A. Flynn, T. Harding, J. B. Uney, B. E. Troskie, R. P. Millar, and C. A. McArdle Differential Internalization of Mammalian and Non-mammalian Gonadotropin-releasing Hormone Receptors. UNCOUPLING OF DYNAMIN-DEPENDENT INTERNALIZATION FROM MITOGEN-ACTIVATED PROTEIN KINASE SIGNALING J. Biol. Chem., October 19, 2001; 276(43): 39685 - 39694. [Abstract] [Full Text] [PDF]
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Y. Chen, Y. H. Zhao, and R. Wu Differential Regulation of Airway Mucin Gene Expression and Mucin Secretion by Extracellular Nucleotide Triphosphates Am. J. Respir. Cell Mol. Biol., October 1, 2001; 25(4): 409 - 417. [Abstract] [Full Text] [PDF]
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X. Zhen, J. Zhang, G. P. Johnson, and E. Friedman D4 Dopamine Receptor Differentially Regulates Akt/Nuclear Factor-kappa B and Extracellular Signal-Regulated Kinase Pathways in D4MN9D Cells Mol. Pharmacol., October 1, 2001; 60(4): 857 - 864. [Abstract] [Full Text] [PDF]
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 J. Smith, R. Yu, and P. M. Hinkle Activation of MAPK by TRH Requires Clathrin-Dependent Endocytosis and PKC but Not Receptor Interaction with {beta}-Arrestin or Receptor Endocytosis Mol. Endocrinol., September 1, 2001; 15(9): 1539 - 1548. [Abstract] [Full Text] [PDF]
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S. Faivre, K. Regnauld, E. Bruyneel, Q.-D. Nguyen, M. Mareel, S. Emami, and C. Gespach Suppression of Cellular Invasion by Activated G-Protein Subunits Galpha o, Galpha i1, Galpha i2, and Galpha i3 and Sequestration of Gbeta gamma Mol. Pharmacol., August 1, 2001; 60(2): 363 - 372. [Abstract] [Full Text] [PDF]
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 I. Shefler and R. Sagi-Eisenberg Gi-Mediated Activation of the Syk Kinase by the Receptor Mimetic Basic Secretagogues of Mast Cells: Role in Mediating Arachidonic Acid/Metabolites Release J. Immunol., July 1, 2001; 167(1): 475 - 481. [Abstract] [Full Text] [PDF]
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D.-W. Kim and B. H. Cochran JAK2 Activates TFII-I and Regulates Its Interaction with Extracellular Signal-Regulated Kinase Mol. Cell. Biol., May 15, 2001; 21(10): 3387 - 3397. [Abstract] [Full Text]
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F. Alderton, P. P. A. Humphrey, and L. A. Sellers High-Intensity p38 Kinase Activity Is Critical for p21cip1 Induction and the Antiproliferative Function of Gi Protein-Coupled Receptors Mol. Pharmacol., April 16, 2001; 59(5): 1119 - 1128. [Abstract] [Full Text]
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Y. Gao, S. Tang, S. Zhou, and J. A. Ware The Thromboxane A2 Receptor Activates Mitogen-Activated Protein Kinase via Protein Kinase C-Dependent Gi Coupling and Src-Dependent Phosphorylation of the Epidermal Growth Factor Receptor J. Pharmacol. Exp. Ther., April 13, 2001; 296(2): 426 - 433. [Abstract] [Full Text]
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 G. Pearson, F. Robinson, T. Beers Gibson, B.-e Xu, M. Karandikar, K. Berman, and M. H. Cobb Mitogen-Activated Protein (MAP) Kinase Pathways: Regulation and Physiological Functions Endocr. Rev., April 1, 2001; 22(2): 153 - 183. [Abstract] [Full Text]
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 Y.-M. Yang, W. C. Hatch, Z.-Y. Liu, B. Du, and J. E. Groopman {beta}-Chemokine Induction of Activation Protein-1 and Cyclic AMP Responsive Element Activation in Human Myeloid Cells Cell Growth Differ., April 1, 2001; 12(4): 211 - 221. [Abstract] [Full Text]
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O. Kifor, R. J. MacLeod, R. Diaz, M. Bai, T. Yamaguchi, T. Yao, I. Kifor, and E. M. Brown Regulation of MAP kinase by calcium-sensing receptor in bovine parathyroid and CaR-transfected HEK293 cells Am J Physiol Renal Physiol, February 1, 2001; 280(2): F291 - F302. [Abstract] [Full Text] [PDF]
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Q. He and M. C. LaPointe Src and Rac Mediate Endothelin-1 and Lysophosphatidic Acid Stimulation of the Human Brain Natriuretic Peptide Promoter Hypertension, February 1, 2001; 37(2): 478 - 484. [Abstract] [Full Text] [PDF]
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 L. Xing, A. M. Venegas, A. Chen, L. Garrett-Beal, B. F. Boyce, H. E. Varmus, and P. L. Schwartzberg Genetic evidence for a role for Src family kinases in TNF family receptor signaling and cell survival Genes & Dev., January 15, 2001; 15(2): 241 - 253. [Abstract] [Full Text]
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 E. Feraille and A. Doucet Sodium-Potassium-Adenosinetriphosphatase-Dependent Sodium Transport in the Kidney: Hormonal Control Physiol Rev, January 1, 2001; 81(1): 345 - 418. [Abstract] [Full Text] [PDF]
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R. A. Blake, M. A. Broome, X. Liu, J. Wu, M. Gishizky, L. Sun, and S. A. Courtneidge SU6656, a Selective Src Family Kinase Inhibitor, Used To Probe Growth Factor Signaling Mol. Cell. Biol., December 1, 2000; 20(23): 9018 - 9027. [Abstract] [Full Text]
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V. P. Krymskaya, M. J. Orsini, A. J. Eszterhas, K. C. Brodbeck, J. L. Benovic, R. A. Panettieri Jr., and R. B. Penn Mechanisms of Proliferation Synergy by Receptor Tyrosine Kinase and G Protein-Coupled Receptor Activation in Human Airway Smooth Muscle Am. J. Respir. Cell Mol. Biol., October 1, 2000; 23(4): 546 - 554. [Abstract] [Full Text]
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E. J. Filardo, J. A. Quinn, K. I. Bland, and A. R. Frackelton Jr. Estrogen-Induced Activation of Erk-1 and Erk-2 Requires the G Protein-Coupled Receptor Homolog, GPR30, and Occurs via Trans-Activation of the Epidermal Growth Factor Receptor through Release of HB-EGF Mol. Endocrinol., October 1, 2000; 14(10): 1649 - 1660. [Abstract] [Full Text]
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