Control of the neurovascular coupling by nitric oxide-dependent regulation of astrocytic Ca2+ signaling

Neuronal activity must be tightly coordinated with blood flow to keep proper brain function, which is achieved by a mechanism known as neurovascular coupling. Then, an increase in synaptic activity leads to a dilation of local parenchymal arterioles that matches the enhanced metabolic demand. Neurov...

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Main Authors: Manuel Francisco Muñoz, Mariela ePuebla, Xavier eFigueroa
Format: Article
Language:English
Published: Frontiers Media S.A. 2015-03-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fncel.2015.00059/full
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author Manuel Francisco Muñoz
Mariela ePuebla
Xavier eFigueroa
author_facet Manuel Francisco Muñoz
Mariela ePuebla
Xavier eFigueroa
author_sort Manuel Francisco Muñoz
collection DOAJ
description Neuronal activity must be tightly coordinated with blood flow to keep proper brain function, which is achieved by a mechanism known as neurovascular coupling. Then, an increase in synaptic activity leads to a dilation of local parenchymal arterioles that matches the enhanced metabolic demand. Neurovascular coupling is orchestrated by astrocytes. These glial cells are located between neurons and the microvasculature, with the astrocytic endfeet ensheathing the vessels, which allows fine intercellular communication. The neurotransmitters released during neuronal activity reach astrocytic receptors and trigger a Ca2+ signaling that propagates to the endfeet, activating the release of vasoactive factors and arteriolar dilation. The astrocyte Ca2+ signaling is coordinated by gap junction channels and hemichannels formed by connexins (Cx43 and Cx30) and channels formed by pannexins (Panx-1). The neuronal activity-initiated Ca2+ waves are propagated among neighboring astrocytes directly via gap junctions or through ATP release via connexin hemichannels or pannexin channels. In addition, Ca2+ entry via connexin hemichannels or pannexin channels may participate in the regulation of the astrocyte signaling-mediated neurovascular coupling. Interestingly, nitric oxide (NO) can activate connexin hemichannel by S-nitrosylation and the Ca2+-dependent NO-synthesizing enzymes endothelial NO synthase (eNOS) and neuronal NOS (nNOS) are expressed in astrocytes. Therefore, the astrocytic Ca2+ signaling triggered in neurovascular coupling may activate NO production, which, in turn, may lead to Ca2+ influx through hemichannel activation. Furthermore, NO release from the hemichannels located at astrocytic endfeet may contribute to the vasodilation of parenchymal arterioles. In this review, we discuss the mechanisms involved in the regulation of the astrocytic Ca2+ signaling that mediates neurovascular coupling, with a special emphasis in the possible participation of NO in this process.
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spelling doaj.art-05d6c5e5085d4c96ae971d2d445bd8ef2022-12-22T01:34:45ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022015-03-01910.3389/fncel.2015.00059128838Control of the neurovascular coupling by nitric oxide-dependent regulation of astrocytic Ca2+ signalingManuel Francisco Muñoz0Mariela ePuebla1Xavier eFigueroa2Pontificia Universidad Catolica de ChilePontificia Universidad Catolica de ChilePontificia Universidad Catolica de ChileNeuronal activity must be tightly coordinated with blood flow to keep proper brain function, which is achieved by a mechanism known as neurovascular coupling. Then, an increase in synaptic activity leads to a dilation of local parenchymal arterioles that matches the enhanced metabolic demand. Neurovascular coupling is orchestrated by astrocytes. These glial cells are located between neurons and the microvasculature, with the astrocytic endfeet ensheathing the vessels, which allows fine intercellular communication. The neurotransmitters released during neuronal activity reach astrocytic receptors and trigger a Ca2+ signaling that propagates to the endfeet, activating the release of vasoactive factors and arteriolar dilation. The astrocyte Ca2+ signaling is coordinated by gap junction channels and hemichannels formed by connexins (Cx43 and Cx30) and channels formed by pannexins (Panx-1). The neuronal activity-initiated Ca2+ waves are propagated among neighboring astrocytes directly via gap junctions or through ATP release via connexin hemichannels or pannexin channels. In addition, Ca2+ entry via connexin hemichannels or pannexin channels may participate in the regulation of the astrocyte signaling-mediated neurovascular coupling. Interestingly, nitric oxide (NO) can activate connexin hemichannel by S-nitrosylation and the Ca2+-dependent NO-synthesizing enzymes endothelial NO synthase (eNOS) and neuronal NOS (nNOS) are expressed in astrocytes. Therefore, the astrocytic Ca2+ signaling triggered in neurovascular coupling may activate NO production, which, in turn, may lead to Ca2+ influx through hemichannel activation. Furthermore, NO release from the hemichannels located at astrocytic endfeet may contribute to the vasodilation of parenchymal arterioles. In this review, we discuss the mechanisms involved in the regulation of the astrocytic Ca2+ signaling that mediates neurovascular coupling, with a special emphasis in the possible participation of NO in this process.http://journal.frontiersin.org/Journal/10.3389/fncel.2015.00059/fullConnexinsGap Junctionscerebral blood flowpannexinsendothelial nitric oxide synthaseneuronal nitric oxide synthase
spellingShingle Manuel Francisco Muñoz
Mariela ePuebla
Xavier eFigueroa
Control of the neurovascular coupling by nitric oxide-dependent regulation of astrocytic Ca2+ signaling
Frontiers in Cellular Neuroscience
Connexins
Gap Junctions
cerebral blood flow
pannexins
endothelial nitric oxide synthase
neuronal nitric oxide synthase
title Control of the neurovascular coupling by nitric oxide-dependent regulation of astrocytic Ca2+ signaling
title_full Control of the neurovascular coupling by nitric oxide-dependent regulation of astrocytic Ca2+ signaling
title_fullStr Control of the neurovascular coupling by nitric oxide-dependent regulation of astrocytic Ca2+ signaling
title_full_unstemmed Control of the neurovascular coupling by nitric oxide-dependent regulation of astrocytic Ca2+ signaling
title_short Control of the neurovascular coupling by nitric oxide-dependent regulation of astrocytic Ca2+ signaling
title_sort control of the neurovascular coupling by nitric oxide dependent regulation of astrocytic ca2 signaling
topic Connexins
Gap Junctions
cerebral blood flow
pannexins
endothelial nitric oxide synthase
neuronal nitric oxide synthase
url http://journal.frontiersin.org/Journal/10.3389/fncel.2015.00059/full
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AT marielaepuebla controloftheneurovascularcouplingbynitricoxidedependentregulationofastrocyticca2signaling
AT xavierefigueroa controloftheneurovascularcouplingbynitricoxidedependentregulationofastrocyticca2signaling