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      Estrogen Actions on Neuroendocrine Glia

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          Abstract

          Astrocytes are the most abundant cells in the central nervous system (CNS). It appears that astrocytes are as diverse as neurons, having different phenotypes in various regions throughout the brain and participating in intercellular communication that involves signaling to neurons. It is not surprising then that astrocytes in the hypothalamus have an active role in the CNS regulation of reproduction. In addition to the traditional mechanism involving ensheathment of neurons and processes, astrocytes may have a critical role in regulating estrogen-positive feedback. Work in our laboratory has focused on the relationship between circulating estradiol and progesterone synthesized de novo in the brain. We have demonstrated that circulating estradiol stimulates the synthesis of progesterone in adult hypothalamic astrocytes, and this neuroprogesterone is critical for initiating the LH surge. Estradiol cell signaling is initiated at the cell membrane and involves the transactivation of metabotropic glutamate receptor type 1a (mGluR1a) leading to the release of intracellular stores of calcium. We used surface biotinylation to demonstrate that estrogen receptor-α (ERα) is present in the cell membrane and has an extracellular portion. Like other membrane receptors, ERα is inserted into the membrane and removed via internalization after agonist stimulation. This trafficking is directly regulated by estradiol, which rapidly and transiently increases the levels of membrane ERα, and upon activation, increases internalization that finally leads to ERα degradation. This autoregulation temporally limits membrane-initiated estradiol cell signaling. Thus, neuroprogesterone, the necessary signal for the LH surge, is released when circulating levels of estradiol peak on proestrus and activate progesterone receptors whose expression has been induced by the gradual rise of estradiol during follicular development.

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          Most cited references106

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          Astrocytic purinergic signaling coordinates synaptic networks.

          To investigate the role of astrocytes in regulating synaptic transmission, we generated inducible transgenic mice that express a dominant-negative SNARE domain selectively in astrocytes to block the release of transmitters from these glial cells. By releasing adenosine triphosphate, which accumulates as adenosine, astrocytes tonically suppressed synaptic transmission, thereby enhancing the dynamic range for long-term potentiation and mediated activity-dependent, heterosynaptic depression. These results indicate that astrocytes are intricately linked in the regulation of synaptic strength and plasticity and provide a pathway for synaptic cross-talk.
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            Astrocyte control of synaptic transmission and neurovascular coupling.

            From a structural perspective, the predominant glial cell of the central nervous system, the astrocyte, is positioned to regulate synaptic transmission and neurovascular coupling: the processes of one astrocyte contact tens of thousands of synapses, while other processes of the same cell form endfeet on capillaries and arterioles. The application of subcellular imaging of Ca2+ signaling to astrocytes now provides functional data to support this structural notion. Astrocytes express receptors for many neurotransmitters, and their activation leads to oscillations in internal Ca2+. These oscillations induce the accumulation of arachidonic acid and the release of the chemical transmitters glutamate, d-serine, and ATP. Ca2+ oscillations in astrocytic endfeet can control cerebral microcirculation through the arachidonic acid metabolites prostaglandin E2 and epoxyeicosatrienoic acids that induce arteriole dilation, and 20-HETE that induces arteriole constriction. In addition to actions on the vasculature, the release of chemical transmitters from astrocytes regulates neuronal function. Astrocyte-derived glutamate, which preferentially acts on extrasynaptic receptors, can promote neuronal synchrony, enhance neuronal excitability, and modulate synaptic transmission. Astrocyte-derived d-serine, by acting on the glycine-binding site of the N-methyl-d-aspartate receptor, can modulate synaptic plasticity. Astrocyte-derived ATP, which is hydrolyzed to adenosine in the extracellular space, has inhibitory actions and mediates synaptic cross-talk underlying heterosynaptic depression. Now that we appreciate this range of actions of astrocytic signaling, some of the immediate challenges are to determine how the astrocyte regulates neuronal integration and how both excitatory (glutamate) and inhibitory signals (adenosine) provided by the same glial cell act in concert to regulate neuronal function.
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              New roles for astrocytes: redefining the functional architecture of the brain.

              Astrocytes have traditionally been considered ancillary, satellite cells of the nervous system. However, work over the past decade has revealed that they interact with the vasculature to form a gliovascular network that might organize not only the structural architecture of the brain but also its communication pathways, activation, thresholds and plasticity. The net effect is that astroglia demarcate gray matter regions, both cortical and subcortical, into functional compartments whose internal activation thresholds and external outputs are regulated by single glial cells. The array of these astrocyte-delimited microdomains along the capillary microvasculature allows the formation of higher-order gliovascular units, which serve to match local neural activity and blood flow while regulating neuronal firing thresholds through coordinative glial signaling. By these means, astrocytes might establish the functional as well as the structural architecture of the adult brain.
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                Author and article information

                Journal
                NEN
                Neuroendocrinology
                10.1159/issn.0028-3835
                Neuroendocrinology
                S. Karger AG
                0028-3835
                1423-0194
                2010
                June 2010
                24 March 2010
                : 91
                : 3
                : 211-222
                Affiliations
                aDepartment of Neurobiology, Laboratory of Neuroendocrinology, UCLA Brain Research Institute, and bDepartment of Obstetrics and Gynecology, David Geffen School of Medicine at UCLA, Los Angeles, Calif., USA
                Author notes
                *Paul Micevych, Department of Neurobiology, David Geffen School of Medicine at UCLA, 10833 LeConte Avenue, 73-078 CHS, Los Angeles, CA 90095-1763 (USA), Tel. +1 310 206 8265, Fax +1 310 825 2224, E-Mail pmicevych@mednet.ucla.edu
                Article
                289568 PMC2889254 Neuroendocrinology 2010;91:211–222
                10.1159/000289568
                PMC2889254
                20332598
                9271673c-f785-45d6-a74e-1e11e208271b
                © 2010 S. Karger AG, Basel

                Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher. Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug. Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

                History
                : 20 November 2009
                : 18 February 2010
                Page count
                Figures: 5, References: 137, Pages: 12
                Categories
                At the Cutting Edge

                Endocrinology & Diabetes,Neurology,Nutrition & Dietetics,Sexual medicine,Internal medicine,Pharmacology & Pharmaceutical medicine
                Surface biotinylation,Astrocytes,Estrogen receptor-alpha trafficking

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