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Science 307 (5715): 1625-1630

Copyright © 2005 by the American Association for the Advancement of Science

A Transmembrane Intracellular Estrogen Receptor Mediates Rapid Cell Signaling

Chetana M. Revankar,1,2 Daniel F. Cimino,1,2 Larry A. Sklar,2,3 Jeffrey B. Arterburn,4 Eric R. Prossnitz1,2*

Abstract: The steroid hormone estrogen regulates many functionally unrelated processes in numerous tissues. Although it is traditionally thought to control transcriptional activation through the classical nuclear estrogen receptors, it also initiates many rapid nongenomic signaling events. We found that of all G protein–coupled receptors characterized to date, GPR30 is uniquely localized to the endoplasmic reticulum, where it specifically binds estrogen and fluorescent estrogen derivatives. Activating GPR30 by estrogen resulted in intracellular calcium mobilization and synthesis of phosphatidylinositol 3,4,5-trisphosphate in the nucleus. Thus, GPR30 represents an intracellular transmembrane estrogen receptor that may contribute to normal estrogen physiology as well as pathophysiology.

1 Department of Cell Biology and Physiology, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USA.
2 Cancer Research and Treatment Center, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USA.
3 Department of Pathology, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USA.
4 Department of Chemistry and Biochemistry, New Mexico State University, Las Cruces, NM 88003, USA.

* To whom correspondence should be addressed. E-mail: eprossnitz{at}salud.unm.edu

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Estrogen Suppresses MLK3-Mediated Apoptosis Sensitivity in ER+ Breast Cancer Cells.
V. Rangasamy, R. Mishra, S. Mehrotra, G. Sondarva, R. S. Ray, A. Rao, M. Chatterjee, B. Rana, and A. Rana (2010)
Cancer Res. 70, 1731-1740
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The unfolding stories of GPR30, a new membrane-bound estrogen receptor.
M. Maggiolini and D. Picard (2010)
J. Endocrinol. 204, 105-114
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17-{beta} Estradiol Promotion of Herpes Simplex Virus Type 1 Reactivation Is Estrogen Receptor Dependent.
R. D. Vicetti Miguel, B. S. Sheridan, S. A. K. Harvey, R. S. Schreiner, R. L. Hendricks, and T. L. Cherpes (2010)
J. Virol. 84, 565-572
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Locally produced relaxin may affect testis and vas deferens function in rats.
L. C. Cardoso, A. R. Nascimento, C. Royer, C. S. Porto, and M. F. M. Lazari (2010)
Reproduction 139, 185-196
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A novel estrogen receptor GPER inhibits mitochondria permeability transition pore opening and protects the heart against ischemia-reperfusion injury.
J. C. Bopassa, M. Eghbali, L. Toro, and E. Stefani (2010)
Am J Physiol Heart Circ Physiol 298, H16-H23
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Rapid Regulation of KATP Channel Activity by 17{beta}-Estradiol in Pancreatic {beta}-Cells Involves the Estrogen Receptor {beta} and the Atrial Natriuretic Peptide Receptor.
S. Soriano, A. B. Ropero, P. Alonso-Magdalena, C. Ripoll, I. Quesada, B. Gassner, M. Kuhn, J.-A. Gustafsson, and A. Nadal (2009)
Mol. Endocrinol. 23, 1973-1982
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G Protein-Coupled Receptor 30 Expression Is Up-Regulated by EGF and TGF{alpha} in Estrogen Receptor {alpha}-Positive Cancer Cells.
A. Vivacqua, R. Lappano, P. De Marco, D. Sisci, S. Aquila, F. De Amicis, S. A. W. Fuqua, S. Ando, and M. Maggiolini (2009)
Mol. Endocrinol. 23, 1815-1826
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Estradiol-mediated ERK phosphorylation and apoptosis in vascular smooth muscle cells requires GPR 30.
Q. Ding, R. Gros, L. E. Limbird, J. Chorazyczewski, and R. D. Feldman (2009)
Am J Physiol Cell Physiol 297, C1178-C1187
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Activation of a novel estrogen receptor, GPER, is cardioprotective in male and female rats.
A. M. Deschamps and E. Murphy (2009)
Am J Physiol Heart Circ Physiol 297, H1806-H1813
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Membrane oestrogen receptor signalling to cell functions.
E. R. Levin (2009)
J. Physiol. 587, 5019-5023
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The role of oestrogens in the adaptation of islets to insulin resistance.
A. Nadal, P. Alonso-Magdalena, S. Soriano, A. B. Ropero, and I. Quesada (2009)
J. Physiol. 587, 5031-5037
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Importance of Extranuclear Estrogen Receptor-{alpha} and Membrane G Protein-Coupled Estrogen Receptor in Pancreatic Islet Survival.
S. Liu, C. Le May, W. P.S. Wong, R. D. Ward, D. J. Clegg, M. Marcelli, K. S. Korach, and F. Mauvais-Jarvis (2009)
Diabetes 58, 2292-2302
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Functional requirement of AgRP and NPY neurons in ovarian cycle-dependent regulation of food intake.
L. E. Olofsson, A. A. Pierce, and A. W. Xu (2009)
PNAS 106, 15932-15937
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Estrogen can signal through multiple pathways to regulate oocyte cyst breakdown and primordial follicle assembly in the neonatal mouse ovary.
Y. Chen, K. Breen, and M. E Pepling (2009)
J. Endocrinol. 202, 407-417
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ER{alpha}, ER{beta}, and gpER: novel aspects of oestrogen receptor signalling in atherosclerosis.
M. R. Meyer and M. Barton (2009)
Cardiovasc Res 83, 605-610
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Localisation of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues.
G. G J Hazell, S. T Yao, J. A Roper, E. R Prossnitz, A.-M. O'Carroll, and S. J Lolait (2009)
J. Endocrinol. 202, 223-236
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Chronic Treatment with the G Protein-Coupled Receptor 30 Agonist G-1 Decreases Blood Pressure in Ovariectomized mRen2.Lewis Rats.
S. H. Lindsey, J. A. Cohen, K. B. Brosnihan, P. E. Gallagher, and M. C. Chappell (2009)
Endocrinology 150, 3753-3758
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Intracellular activation of vasopressin V2 receptor mutants in nephrogenic diabetes insipidus by nonpeptide agonists.
J. H. Robben, M. L. A. Kortenoeven, M. Sze, C. Yae, G. Milligan, V. M. Oorschot, J. Klumperman, N. V. A. M. Knoers, and P. M. T. Deen (2009)
PNAS 106, 12195-12200
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