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*CHOLESTEROL
*ESTRADIOL

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The Journal of Neuroscience, October 1, 2002, 22(19):8391-8401

ER-X: A Novel, Plasma Membrane-Associated, Putative Estrogen Receptor That Is Regulated during Development and after Ischemic Brain Injury

C. Dominique Toran-Allerand1, 3, 5, 6, Xiaoping Guan2, 6, Neil J. MacLusky2, 6, Tamas L. Horvath7, Sabrina Diano7, Meharvan Singh2, 6, E. Sander Connolly Jr4, Imam S. Nethrapalli2, 6, *, and Alexander A. Tinnikov2, 6, *

Departments of 1 Anatomy and Cell Biology, 2 Obstetrics and Gynecology, 3 Neurology, and 4 Neurosurgery, and Centers for 5 Neurobiology and Behavior and 6 Reproductive Sciences, Columbia University College of Physicians and Surgeons, New York, New York 10032, and 7 Department of Obstetrics and Gynecology, Yale University School of Medicine, New Haven, Connecticut 06510

We showed previously in neocortical explants, derived from developing wild-type and estrogen receptor (ER)-alpha gene-disrupted (ERKO) mice, that both 17alpha - and 17beta -estradiol elicit the rapid and sustained phosphorylation and activation of the mitogen-activated protein kinase (MAPK) isoforms, the extracellular signal-regulated kinases ERK1 and ERK2. We proposed that the ER mediating activation of the MAPK cascade, a signaling pathway important for cell division, neuronal differentiation, and neuronal survival in the developing brain, is neither ER-alpha nor ER-beta but a novel, plasma membrane-associated, putative ER with unique properties. The data presented here provide further evidence that points strongly to the existence of a high-affinity, saturable, 3H-estradiol binding site (Kd, ~1.6 nM) in the plasma membrane. Unlike neocortical ER-alpha , which is intranuclear and developmentally regulated, and neocortical ER-beta , which is intranuclear and expressed throughout life, this functional, plasma membrane-associated ER, which we have designated "ER-X," is enriched in caveolar-like microdomains (CLMs) of postnatal, but not adult, wild-type and ERKO neocortical and uterine plasma membranes. We show further that ER-X is functionally distinct from ER-alpha and ER-beta , and that, like ER-alpha , it is re-expressed in the adult brain, after ischemic stroke injury. We also confirmed in a cell-free system that ER-alpha is an inhibitory regulator of ERK activation, as we showed previously in neocortical cultures. Association with CLM complexes positions ER-X uniquely to interact rapidly with kinases of the MAPK cascade and other signaling pathways, providing a novel mechanism for mediation of the influences of estrogen on neuronal differentiation, survival, and plasticity.

Key words: caveolae/caveolar-like microdomains; 17alpha -estradiol; 17beta -estradiol; ERK1/2; ERKO; brain; neocortex; uterus; development

* I.S.N. and A.A.T. contributed equally to this work.

Copyright © 2002 Society for Neuroscience  0270-6474/02/22198391-11$05.00/0


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