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Molecular Endocrinology 16 (1): 70-84
Copyright © 2002 by The Endocrine Society

Estrogen Action Via the G Protein-Coupled Receptor, GPR30: Stimulation of Adenylyl Cyclase and cAMP-Mediated Attenuation of the Epidermal Growth Factor Receptor-to-MAPK Signaling Axis

Edward J. Filardo, Jeffrey A. Quinn, A. Raymond Frackelton, Jr. and Kirby I. Bland

Departments of Surgery (E.J.F., K.I.B.) and Medicine (E.J.F., J.A.Q.), Rhode Island Hospital (E.J.F., J.A.Q., K.I.B.) and Roger Williams Hospital (A.R.F.) and Brown University, Providence, Rhode Island 02903

Address all correspondence and requests for reprints to: Edward J. Filardo, Rhode Island Hospital, Department of Medicine, Division of Clinical Pharmacology, Aldrich Building, Room 712, 593 Eddy Street, Providence, Rhode Island 02903. E-mail: Edward_Filardo{at}brown.edu

Estrogen triggers rapid yet transient activation of the MAPKs, extracellular signal-regulated kinase (Erk)-1 and Erk-2. We have reported that this estrogen action requires the G protein-coupled receptor, GPR30, and occurs via Gß{gamma}-subunit protein-dependent transactivation of the epidermal growth factor (EGF) receptor through the release of pro-heparan-bound EGF from the cell surface. Here we investigate the mechanism by which Erk-1/-2 activity is rapidly restored to basal levels after estrogen stimulation. Evidence is provided that attenuation of Erk-1/-2 activity by estrogen occurs via GPR30-dependent stimulation of adenylyl cyclase and cAMP-dependent signaling that results in Raf-1 inactivation. We show that 17ß-E2 represses EGF-induced activation of the Raf-to-Erk pathway in human breast carcinoma cells that express GPR30, including MCF-7 and SKBR3 cells which express both or neither, ER, respectively. MDA-MB-231 cells, which express ERß, but not ER{alpha}, and low levels of GPR30 protein, are unable to stimulate adenylyl cyclase or promote estrogen-mediated blockade of EGF-induced activation of Erk-1/-2. Pretreatment of MDA-MB-231 cells with cholera toxin, which ADP-ribosylates and activates G{alpha}s subunit proteins, results in G protein-coupled receptor (GPCR)-independent adenylyl cyclase activity and suppression of EGF-induced Erk-1/-2 activity. Transfection of GPR30 into MDA-MB-231 cells restores their ability to stimulate adenylyl cyclase and attenuate EGF-induced activation of Erk-1/-2 by estrogen. Moreover, GPR30-dependent, cAMP-mediated attenuation of EGF-induced Erk-1/-2 activity was achieved by ER antagonists such as tamoxifen or ICI 182, 780; yet not by 17{alpha}-E2 or progesterone. Thus, our data delineate a novel mechanism, requiring GPR30 and estrogen, that acts to regulate Erk-1/-2 activity via an inhibitory signal mediated by cAMP. Coupled with our prior findings, these current data imply that estrogen balances Erk-1/-2 activity through a single GPCR via two distinct G protein-dependent signaling pathways that have opposing effects on the EGF receptor-to-MAPK pathway.




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P. Thomas, Y. Pang, E. J. Filardo, and J. Dong
Identity of an Estrogen Membrane Receptor Coupled to a G Protein in Human Breast Cancer Cells
Endocrinology, February 1, 2005; 146(2): 624 - 632.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
B. Schafer, B. Marg, A. Gschwind, and A. Ullrich
Distinct ADAM Metalloproteinases Regulate G Protein-coupled Receptor-induced Cell Proliferation and Survival
J. Biol. Chem., November 12, 2004; 279(46): 47929 - 47938.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
R. I. Fernando and J. Wimalasena
Estradiol Abrogates Apoptosis in Breast Cancer Cells through Inactivation of BAD: Ras-dependent Nongenomic Pathways Requiring Signaling through ERK and Akt
Mol. Biol. Cell, July 1, 2004; 15(7): 3266 - 3284.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H. E. Cunliffe, M. Ringner, S. Bilke, R. L. Walker, J. M. Cheung, Y. Chen, and P. S. Meltzer
The Gene Expression Response of Breast Cancer to Growth Regulators: Patterns and Correlation with Tumor Expression Profiles
Cancer Res., November 1, 2003; 63(21): 7158 - 7166.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
L. B. Lutz, M. Jamnongjit, W.-H. Yang, D. Jahani, A. Gill, and S. R. Hammes
Selective Modulation of Genomic and Nongenomic Androgen Responses by Androgen Receptor Ligands
Mol. Endocrinol., June 1, 2003; 17(6): 1106 - 1116.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
S. R. Hammes
The further redefining of steroid-mediated signaling
PNAS, March 4, 2003; 100(5): 2168 - 2170.
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 Mol. Endocrinol.Home page
E. R. Levin
Bidirectional Signaling between the Estrogen Receptor and the Epidermal Growth Factor Receptor
Mol. Endocrinol., March 1, 2003; 17(3): 309 - 317.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Razandi, A. Pedram, S. T. Park, and E. R. Levin
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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 EndocrinologyHome page
T. M. Ahola, N. Alkio, T. Manninen, and T. Ylikomi
Progestin and G Protein-Coupled Receptor 30 Inhibit Mitogen-Activated Protein Kinase Activity in MCF-7 Breast Cancer Cells
Endocrinology, December 1, 2002; 143(12): 4620 - 4626.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. Rueda, B. Navarro, A. Martinez-Serrano, M. Guzman, and I. Galve-Roperh
The Endocannabinoid Anandamide Inhibits Neuronal Progenitor Cell Differentiation through Attenuation of the Rap1/B-Raf/ERK Pathway
J. Biol. Chem., November 22, 2002; 277(48): 46645 - 46650.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. Duchene, J. P. Schanstra, C. Pecher, A. Pizard, C. Susini, J.-P. Esteve, J.-L. Bascands, and J.-P. Girolami
A Novel Protein-Protein Interaction between a G Protein-coupled Receptor and the Phosphatase SHP-2 Is Involved in Bradykinin-induced Inhibition of Cell Proliferation
J. Biol. Chem., October 18, 2002; 277(43): 40375 - 40383.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
T. M. Ahola, T. Manninen, N. Alkio, and T. Ylikomi
G Protein-Coupled Receptor 30 Is Critical for a Progestin-Induced Growth Inhibition in MCF-7 Breast Cancer Cells
Endocrinology, September 1, 2002; 143(9): 3376 - 3384.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z. Guo, W. P. M. Benten, J. Krucken, and F. Wunderlich
Nongenomic Testosterone Calcium Signaling. GENOTROPIC ACTIONS IN ANDROGEN RECEPTOR-FREE MACROPHAGES
J. Biol. Chem., August 9, 2002; 277(33): 29600 - 29607.
[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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