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Molecular Endocrinology 14 (10): 1649-1660
Copyright © 2000 by The Endocrine Society

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

Edward J. Filardo, Jeffrey A. Quinn, Kirby I. Bland1 and A. Raymond Frackelton, Jr.

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

Estrogen rapidly activates the mitogen-activated protein kinases, Erk-1 and Erk-2, via an as yet unknown mechanism. Here, evidence is provided that estrogen-induced Erk-1/-2 activation occurs independently of known estrogen receptors, but requires the expression of the G protein-coupled receptor homolog, GPR30. We show that 17ß-estradiol activates Erk-1/-2 not only in MCF-7 cells, which express both estrogen receptor {alpha} (ER{alpha}) and ERß, but also in SKBR3 breast cancer cells, which fail to express either receptor. Immunoblot analysis using GPR30 peptide antibodies showed that this estrogen response was associated with the presence of GPR30 protein in these cells. MDA-MB-231 breast cancer cells (ER{alpha}-, ERß+) are GPR30 deficient and insensitive to Erk-1/-2 activation by 17ß-estradiol. Transfection of MDA-MB-231 cells with a GPR30 complementary DNA resulted in overexpression of GPR30 protein and conversion to an estrogen-responsive phenotype. In addition, GPR30-dependent Erk-1/-2 activation was triggered by ER antagonists, including ICI 182,780, yet not by 17{alpha}-estradiol or progesterone. Consistent with acting through a G protein-coupled receptor, estradiol signaling to Erk-1/-2 occurred via a Gß{gamma}-dependent, pertussis toxin-sensitive pathway that required Src-related tyrosine kinase activity and tyrosine phosphorylation of tyrosine 317 of the Shc adapter protein. Reinforcing this idea, estradiol signaling to Erk-1/-2 was dependent upon trans-activation of the epidermal growth factor (EGF) receptor via release of heparan-bound EGF (HB-EGF). Estradiol signaling to Erk-1/-2 could be blocked by: 1) inhibiting EGF-receptor tyrosine kinase activity, 2) neutralizing HB-EGF with antibodies, or 3) down-modulating HB-EGF from the cell surface with the diphtheria toxin mutant, CRM-197. Our data imply that ER-negative breast tumors that continue to express GPR30 may use estrogen to drive growth factor-dependent cellular responses.




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J. Adamski and E. N. Benveniste
17{beta}-Estradiol Activation of the c-Jun N-Terminal Kinase Pathway Leads to Down-Regulation of Class II Major Histocompatibility Complex Expression
Mol. Endocrinol., January 1, 2005; 19(1): 113 - 124.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
M. Razandi, A. Pedram, I. Merchenthaler, G. L. Greene, and E. R. Levin
Plasma Membrane Estrogen Receptors Exist and Functions as Dimers
Mol. Endocrinol., December 1, 2004; 18(12): 2854 - 2865.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
M. Razandi, A. Pedram, E. M. Rosen, and E. R. Levin
BRCA1 Inhibits Membrane Estrogen and Growth Factor Receptor Signaling to Cell Proliferation in Breast Cancer
Mol. Cell. Biol., July 1, 2004; 24(13): 5900 - 5913.
[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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 Mol. Endocrinol.Home page
F. Barletta, C.-W. Wong, C. McNally, B. S. Komm, B. Katzenellenbogen, and B. J. Cheskis
Characterization of the Interactions of Estrogen Receptor and MNAR in the Activation of cSrc
Mol. Endocrinol., May 1, 2004; 18(5): 1096 - 1108.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
C. D. Toran-Allerand
Minireview: A Plethora of Estrogen Receptors in the Brain: Where Will It End?
Endocrinology, March 1, 2004; 145(3): 1069 - 1074.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
R. X. Song, C. J. Barnes, Z. Zhang, Y. Bao, R. Kumar, and R. J. Santen
The role of Shc and insulin-like growth factor 1 receptor in mediating the translocation of estrogen receptor {alpha} to the plasma membrane
PNAS, February 17, 2004; 101(7): 2076 - 2081.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
C. E. Navarro, S. A. Saeed, C. Murdock, A. J. Martinez-Fuentes, K. K. Arora, L. Z. Krsmanovic, and K. J. Catt
Erratum
Mol. Endocrinol., December 1, 2003; 17(12): A - 2658.
[Abstract] [Full Text] [PDF]

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 Exp. Biol. Med.Home page
C. S. Watson and B. Gametchu
Proteins of Multiple Classes May Participate in Nongenomic Steroid Actions
Experimental Biology and Medicine, December 1, 2003; 228(11): 1272 - 1281.
[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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 Cancer Res.Home page
P. A. Davol, R. Bagdasaryan, G. J. Elfenbein, A. L. Maizel, and A. R. Frackelton Jr.
Shc Proteins Are Strong, Independent Prognostic Markers for Both Node-Negative and Node-Positive Primary Breast Cancer
Cancer Res., October 15, 2003; 63(20): 6772 - 6783.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
O. A. Sukocheva, L. Wang, N. Albanese, S. M. Pitson, M. A. Vadas, and P. Xia
Sphingosine Kinase Transmits Estrogen Signaling in Human Breast Cancer Cells
Mol. Endocrinol., October 1, 2003; 17(10): 2002 - 2012.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
C. E. Navarro, S. Abdul Saeed, C. Murdock, A. J. Martinez-Fuentes, K. K. Arora, L. Z. Krsmanovic, and K. J. Catt
Regulation of Cyclic Adenosine 3',5'-Monophosphate Signaling and Pulsatile Neurosecretion by Gi-coupled Plasma Membrane Estrogen Receptors in Immortalized Gonadotropin-Releasing Hormone Neurons
Mol. Endocrinol., September 1, 2003; 17(9): 1792 - 1804.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
G. A. Finlay, D. S. Hunter, C. L. Walker, K. E. Paulson, and B. L. Fanburg
Regulation of PDGF production and ERK activation by estrogen is associated with TSC2 gene expression
Am J Physiol Cell Physiol, August 1, 2003; 285(2): C409 - C418.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
J. K. Wong, H. H. Le, A. Zsarnovszky, and S. M. Belcher
Estrogens and ICI182,780 (Faslodex) Modulate Mitosis and Cell Death in Immature Cerebellar Neurons via Rapid Activation of p44/p42 Mitogen-Activated Protein Kinase
J. Neurosci., June 15, 2003; 23(12): 4984 - 4995.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
G. E. Stoica, T. F. Franke, A. Wellstein, F. Czubayko, H.-J. List, R. Reiter, E. Morgan, M. B. Martin, and A. Stoica
Estradiol Rapidly Activates Akt via the ErbB2 Signaling Pathway
Mol. Endocrinol., May 1, 2003; 17(5): 818 - 830.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
Y. Zhu, C. D. Rice, Y. Pang, M. Pace, and P. Thomas
From the Cover: Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes
PNAS, March 4, 2003; 100(5): 2231 - 2236.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
M. Razandi, G. Alton, A. Pedram, S. Ghonshani, P. Webb, and E. R. Levin
Identification of a Structural Determinant Necessary for the Localization and Function of Estrogen Receptor {alpha} at the Plasma Membrane
Mol. Cell. Biol., March 1, 2003; 23(5): 1633 - 1646.
[Abstract] [Full Text] [PDF]

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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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 Mol. Interv.Home page
D. P. Edwards and V. Boonyaratanakornkit
Rapid Extranuclear Signaling by the Estrogen Receptor (ER): MNAR Couples ER and Src to the MAP Kinase Signaling Pathway
Mol. Interv., February 1, 2003; 3(1): 12 - 15.
[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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 JNCI J Natl Cancer InstHome page
G. Ferretti, S. Di Cosimo, P. Carlini, P. Papaldo, A. Fabi, and F. Cognetti
Re: Mastectomy and Oophorectomy by Menstrual Cycle Phase in Women With Operable Breast Cancer
J Natl Cancer Inst, November 20, 2002; 94(22): 1720 - 1720.
[Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Obrero, D. V. Yu, and D. J. Shapiro
Estrogen Receptor-dependent and Estrogen Receptor-independent Pathways for Tamoxifen and 4-Hydroxytamoxifen-induced Programmed Cell Death
J. Biol. Chem., November 15, 2002; 277(47): 45695 - 45703.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
C.-W. Wong, C. McNally, E. Nickbarg, B. S. Komm, and B. J. Cheskis
Estrogen receptor-interacting protein that modulates its nongenomic activity-crosstalk with Src/Erk phosphorylation cascade
PNAS, November 12, 2002; 99(23): 14783 - 14788.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
A. Gschwind, N. Prenzel, and A. Ullrich
Lysophosphatidic Acid-induced Squamous Cell Carcinoma Cell Proliferation and Motility Involves Epidermal Growth Factor Receptor Signal Transactivation
Cancer Res., November 1, 2002; 62(21): 6329 - 6336.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
C. D. Toran-Allerand, X. Guan, N. J. MacLusky, T. L. Horvath, S. Diano, M. Singh, E. S. Connolly Jr, I. S. Nethrapalli, and A. A. Tinnikov
ER-X: A Novel, Plasma Membrane-Associated, Putative Estrogen Receptor That Is Regulated during Development and after Ischemic Brain Injury
J. Neurosci., October 1, 2002; 22(19): 8391 - 8401.
[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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 Proc. Natl. Acad. Sci. USAHome page
E. F. Rissman, A. L. Heck, J. E. Leonard, M. A. Shupnik, and J.-A. Gustafsson
Disruption of estrogen receptor beta gene impairs spatial learning in female mice
PNAS, March 19, 2002; 99(6): 3996 - 4001.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
A. B. Ropero, B. Soria, and A. Nadal
A Nonclassical Estrogen Membrane Receptor Triggers Rapid Differential Actions in the Endocrine Pancreas
Mol. Endocrinol., March 1, 2002; 16(3): 497 - 505.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
E. Garcia Dos Santos, M. N. Dieudonne, R. Pecquery, V. Le Moal, Y. Giudicelli, and D. Lacasa
Rapid Nongenomic E2 Effects on p42/p44 MAPK, Activator Protein-1, and cAMP Response Element Binding Protein in Rat White Adipocytes
Endocrinology, March 1, 2002; 143(3): 930 - 940.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z. Guo, J. Krucken, W. P. M. Benten, and F. Wunderlich
Estradiol-induced Nongenomic Calcium Signaling Regulates Genotropic Signaling in Macrophages
J. Biol. Chem., February 22, 2002; 277(9): 7044 - 7050.
[Abstract] [Full Text] [PDF]


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