Astrocytic Ca2+ activation by chemogenetics mitigates the effect of kainic acid-induced excitotoxicity on the hippocampus

Astrocytes play a multifaceted role regulating brain glucose metabolism, ion homeostasis, neurotransmitters clearance, and water dynamics being essential in supporting synaptic function. Under different pathological conditions such as brain stroke, epilepsy, and neurodegenerative disorders, excitoto...

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Autores: Hernández-Martín, N., Martínez, M.G., Bascuñana, Pablo, Fernandez de la Rosa, Ruben, García-García, Luis, Gómez, Francisca, Solas, M. Teresa, Martín, Eduardo D., Pozo, Miguel A.
Tipo de documento: artigo
Estado:Versão publicada
Data de publicação:2024
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositório:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/377768
Acesso em linha:http://hdl.handle.net/10261/377768
Access Level:Acceso aberto
Palavra-chave:DREADDs
FDG PET
astrocyte
excitotoxicity
metabolism.
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spelling Astrocytic Ca2+ activation by chemogenetics mitigates the effect of kainic acid-induced excitotoxicity on the hippocampusHernández-Martín, N.Martínez, M.G.Bascuñana, PabloFernandez de la Rosa, RubenGarcía-García, LuisGómez, FranciscaSolas, M. TeresaMartín, Eduardo D.Pozo, Miguel A.DREADDsFDG PETastrocyteexcitotoxicitymetabolism.Astrocytes play a multifaceted role regulating brain glucose metabolism, ion homeostasis, neurotransmitters clearance, and water dynamics being essential in supporting synaptic function. Under different pathological conditions such as brain stroke, epilepsy, and neurodegenerative disorders, excitotoxicity plays a crucial role, however, the contribution of astrocytic activity in protecting neurons from excitotoxicity-induced damage is yet to be fully understood. In this work, we evaluated the effect of astrocytic activation by Designer Receptors Exclusively Activated by Designer Drugs (DREADDs) on brain glucose metabolism in wild-type (WT) mice, and we investigated the effects of sustained astrocyte activation following an insult induced by intrahippocampal (iHPC) kainic acid (KA) injection using 2-deoxy-2-[F]-fluoro-D-glucose (F-FDG) positron emission tomography (PET) imaging, along with behavioral test, nuclear magnetic resonance (NMR) spectroscopy and histochemistry. Astrocytic Ca activation increased the F-FDG uptake, but this effect was not found when the study was performed in knock out mice for type-2 inositol 1,4,5-trisphosphate receptor (Ip3r2) nor in floxed mice to abolish glucose transporter 1 (GLUT1) expression in hippocampal astrocytes (GLUT1). Sustained astrocyte activation after KA injection reversed the brain glucose hypometabolism, restored hippocampal function, prevented neuronal death, and increased hippocampal GABA levels. The findings of our study indicate that astrocytic GLUT1 function is crucial for regulating brain glucose metabolism. Astrocytic Ca activation has been shown to promote adaptive changes that significantly contribute to mitigating the effects of KA-induced damage. This evidence suggests a protective role of activated astrocytes against KA-induced excitotoxicity.This work was financially supported by Spanish Agencia Estatal de Investigación (AEI), Ministerio de Ciencia, Innovación y Universidades (MCIU) (AEI/10.13039/501100011033—M.A.P.: PDI2019-106968RB-100; E.D.M.: PID2020-116327GB-100; M.S.: SAF2017-87619-P).P.B. position is funded by a Miguel Servet grant (Instituto de Salud Carlos III, CP21/00020). N.H.M. position is funded by Alfonso Casanava fellowship granted by Universidad Complutense de Madrid.M.G.M. position was funded by Garantía Juvenil program granted by Comunidad de Madrid.John Wiley & SonsAgencia Estatal de Investigación (España)Ministerio de Ciencia, Innovación y Universidades (España)Instituto de Salud Carlos IIIUniversidad Complutense de MadridComunidad de MadridConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2025202520242025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/377768reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-106968RB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-116327GB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SAF2017-87619-Phttp://dx.doi.org/10.1002/glia.24607Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3777682026-05-22T06:33:51Z
dc.title.none.fl_str_mv Astrocytic Ca2+ activation by chemogenetics mitigates the effect of kainic acid-induced excitotoxicity on the hippocampus
title Astrocytic Ca2+ activation by chemogenetics mitigates the effect of kainic acid-induced excitotoxicity on the hippocampus
spellingShingle Astrocytic Ca2+ activation by chemogenetics mitigates the effect of kainic acid-induced excitotoxicity on the hippocampus
Hernández-Martín, N.
DREADDs
FDG PET
astrocyte
excitotoxicity
metabolism.
title_short Astrocytic Ca2+ activation by chemogenetics mitigates the effect of kainic acid-induced excitotoxicity on the hippocampus
title_full Astrocytic Ca2+ activation by chemogenetics mitigates the effect of kainic acid-induced excitotoxicity on the hippocampus
title_fullStr Astrocytic Ca2+ activation by chemogenetics mitigates the effect of kainic acid-induced excitotoxicity on the hippocampus
title_full_unstemmed Astrocytic Ca2+ activation by chemogenetics mitigates the effect of kainic acid-induced excitotoxicity on the hippocampus
title_sort Astrocytic Ca2+ activation by chemogenetics mitigates the effect of kainic acid-induced excitotoxicity on the hippocampus
dc.creator.none.fl_str_mv Hernández-Martín, N.
Martínez, M.G.
Bascuñana, Pablo
Fernandez de la Rosa, Ruben
García-García, Luis
Gómez, Francisca
Solas, M. Teresa
Martín, Eduardo D.
Pozo, Miguel A.
author Hernández-Martín, N.
author_facet Hernández-Martín, N.
Martínez, M.G.
Bascuñana, Pablo
Fernandez de la Rosa, Ruben
García-García, Luis
Gómez, Francisca
Solas, M. Teresa
Martín, Eduardo D.
Pozo, Miguel A.
author_role author
author2 Martínez, M.G.
Bascuñana, Pablo
Fernandez de la Rosa, Ruben
García-García, Luis
Gómez, Francisca
Solas, M. Teresa
Martín, Eduardo D.
Pozo, Miguel A.
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Agencia Estatal de Investigación (España)
Ministerio de Ciencia, Innovación y Universidades (España)
Instituto de Salud Carlos III
Universidad Complutense de Madrid
Comunidad de Madrid
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv DREADDs
FDG PET
astrocyte
excitotoxicity
metabolism.
topic DREADDs
FDG PET
astrocyte
excitotoxicity
metabolism.
description Astrocytes play a multifaceted role regulating brain glucose metabolism, ion homeostasis, neurotransmitters clearance, and water dynamics being essential in supporting synaptic function. Under different pathological conditions such as brain stroke, epilepsy, and neurodegenerative disorders, excitotoxicity plays a crucial role, however, the contribution of astrocytic activity in protecting neurons from excitotoxicity-induced damage is yet to be fully understood. In this work, we evaluated the effect of astrocytic activation by Designer Receptors Exclusively Activated by Designer Drugs (DREADDs) on brain glucose metabolism in wild-type (WT) mice, and we investigated the effects of sustained astrocyte activation following an insult induced by intrahippocampal (iHPC) kainic acid (KA) injection using 2-deoxy-2-[F]-fluoro-D-glucose (F-FDG) positron emission tomography (PET) imaging, along with behavioral test, nuclear magnetic resonance (NMR) spectroscopy and histochemistry. Astrocytic Ca activation increased the F-FDG uptake, but this effect was not found when the study was performed in knock out mice for type-2 inositol 1,4,5-trisphosphate receptor (Ip3r2) nor in floxed mice to abolish glucose transporter 1 (GLUT1) expression in hippocampal astrocytes (GLUT1). Sustained astrocyte activation after KA injection reversed the brain glucose hypometabolism, restored hippocampal function, prevented neuronal death, and increased hippocampal GABA levels. The findings of our study indicate that astrocytic GLUT1 function is crucial for regulating brain glucose metabolism. Astrocytic Ca activation has been shown to promote adaptive changes that significantly contribute to mitigating the effects of KA-induced damage. This evidence suggests a protective role of activated astrocytes against KA-induced excitotoxicity.
publishDate 2024
dc.date.none.fl_str_mv 2024
2025
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/377768
url http://hdl.handle.net/10261/377768
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-106968RB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-116327GB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SAF2017-87619-P
http://dx.doi.org/10.1002/glia.24607

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dc.publisher.none.fl_str_mv John Wiley & Sons
publisher.none.fl_str_mv John Wiley & Sons
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