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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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Proximal Events in Signaling by Plasma Membrane Estrogen Receptors
J. Biol. Chem., January 17, 2003; 278(4): 2701 - 2712.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
E. J. Dell, J. Connor, S. Chen, E. G. Stebbins, N. P. Skiba, D. Mochly-Rosen, and H. E. Hamm
The beta gamma Subunit of Heterotrimeric G Proteins Interacts with RACK1 and Two Other WD Repeat Proteins
J. Biol. Chem., December 13, 2002; 277(51): 49888 - 49895.
[Abstract] [Full Text] [PDF]


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Am. J. Pathol.Home page
J. Xu, B. Jian, R. Chu, Z. Lu, Q. Li, J. Dunlop, S. Rosenzweig-Lipson, P. McGonigle, R. J. Levy, and B. Liang
Serotonin Mechanisms in Heart Valve Disease II: The 5-HT2 Receptor and Its Signaling Pathway in Aortic Valve Interstitial Cells
Am. J. Pathol., December 1, 2002; 161(6): 2209 - 2218.
[Abstract] [Full Text] [PDF]


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Mol. Cell. Biol.Home page
Y. Pak, N. Pham, and D. Rotin
Direct Binding of the {beta}1 Adrenergic Receptor to the Cyclic AMP-Dependent Guanine Nucleotide Exchange Factor CNrasGEF Leads to Ras Activation
Mol. Cell. Biol., November 15, 2002; 22(22): 7942 - 7952.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
A. Pedram, M. Razandi, and E. R. Levin
Deciphering Vascular Endothelial Cell Growth Factor/Vascular Permeability Factor Signaling to Vascular Permeability. INHIBITION BY ATRIAL NATRIURETIC PEPTIDE
J. Biol. Chem., November 8, 2002; 277(46): 44385 - 44398.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
J. M. Schmitt and P. J. S. Stork
Galpha and Gbeta gamma Require Distinct Src-dependent Pathways to Activate Rap1 and Ras
J. Biol. Chem., November 1, 2002; 277(45): 43024 - 43032.
[Abstract] [Full Text] [PDF]


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Mol. Biol. CellHome page
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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Circ. Res.Home page
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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JEMHome page
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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Mol. Cell. Biol.Home page
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. Biol. Chem.Home page
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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Am. J. Physiol. Cell Physiol.Home page
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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Sci SignalHome page
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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J. Biol. Chem.Home page
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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J. Biol. Chem.Home page
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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J. Virol.Home page
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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HypertensionHome page
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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J. Cell Sci.Home page
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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J. Cell Sci.Home page
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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Am. J. Physiol. Gastrointest. Liver Physiol.Home page
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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J. Neurosci.Home page
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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Biol. Reprod.Home page
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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J. Biol. Chem.Home page
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. Biol. Chem.Home page
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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Am. J. Respir. Cell Mol. Bio.Home page
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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Mol. Pharmacol.Home page
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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Mol. Endocrinol.Home page
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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Mol. Pharmacol.Home page
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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J. Immunol.Home page
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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Mol. Cell. Biol.Home page
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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Mol. Pharmacol.Home page
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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J. Pharmacol. Exp. Ther.Home page
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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Endocr. Rev.Home page
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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Cell Growth Differ.Home page
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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Am. J. Physiol. Renal Physiol.Home page
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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HypertensionHome page
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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Genes Dev.Home page
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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Physiol. Rev.Home page
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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Mol. Cell. Biol.Home page
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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Am. J. Respir. Cell Mol. Bio.Home page
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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Mol. Endocrinol.Home page
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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