Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission

Endocannabinoids (eCBs) play key roles in brain function, acting as modulatory signals in synaptic transmission and plasticity. They are recognized as retrograde messengers that mediate long-term synaptic depression (LTD), but their ability to induce long-term potentiation (LTP) is poorly known. We...

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Autores: Gómez-Gonzalo, Marta, Navarrete, Marta, Perea, Gertrudis, Covelo, Ana, Martín-Fernández, Mario, Shigemoto, Ryuichi, Luján, Rafael, Araque, Alfonso
Tipo de recurso: artículo
Fecha de publicación:2015
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/133875
Acceso en línea:http://hdl.handle.net/10261/133875
Access Level:acceso abierto
Palabra clave:Endocannabinoid signaling
Astrocytes
mGluRs
Nitric oxide
LTP
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spelling Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmissionGómez-Gonzalo, MartaNavarrete, MartaPerea, GertrudisCovelo, AnaMartín-Fernández, MarioShigemoto, RyuichiLuján, RafaelAraque, AlfonsoEndocannabinoid signalingAstrocytesmGluRsNitric oxideLTPEndocannabinoids (eCBs) play key roles in brain function, acting as modulatory signals in synaptic transmission and plasticity. They are recognized as retrograde messengers that mediate long-term synaptic depression (LTD), but their ability to induce long-term potentiation (LTP) is poorly known. We show that eCBs induce the long-term enhancement of transmitter release at single hippocampal synapses through stimulation of astrocytes when coincident with postsynaptic activity. This LTP requires the coordinated activity of the 3 elements of the tripartite synapse: 1) eCB-evoked astrocyte calcium signal that stimulates glutamate release; 2) postsynaptic nitric oxide production; and 3) activation of protein kinase C and presynaptic group I metabotropic glutamate receptors, whose location at presynaptic sites was confirmed by immunoelectron microscopy. Hence, while eCBs act as retrograde signals to depress homoneuronal synapses, they serve as lateral messengers to induce LTP in distant heteroneuronal synapses through stimulation of astrocytes. Therefore, eCBs can trigger LTP through stimulation of astrocyte-neuron signaling, revealing novel cellular mechanisms of eCB effects on synaptic plasticity.Ministerio de Economia y Competitividad, Spain (MINECO; BFU2010-15832), European Union (HEALTH-F2-2007-202167), and Cajal Blue Brain to A.A. Grants from Spain (MINECO; BFU-2009-08404 and CSD2008-00005) to R.L. Grants from Spain (MINECO; Consolider, CSD2010-00045; Ramón y Cajal Program, RYC-2012-12014; and BFU2013-47265) to G.P.Peer ReviewedOxford University PressCajal Blue BrainEuropean CommissionMinisterio de Economía y Competitividad (España)CSIC - Patronato Santiago Ramón y Cajal de Ciencias Naturales y Médicas2016201620152016info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501http://hdl.handle.net/10261/133875reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/EC/FP7/202167info:eu-repo/semantics/openAccessoai:digital.csic.es:10261/1338752026-05-22T06:33:51Z
dc.title.none.fl_str_mv Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission
title Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission
spellingShingle Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission
Gómez-Gonzalo, Marta
Endocannabinoid signaling
Astrocytes
mGluRs
Nitric oxide
LTP
title_short Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission
title_full Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission
title_fullStr Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission
title_full_unstemmed Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission
title_sort Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission
dc.creator.none.fl_str_mv Gómez-Gonzalo, Marta
Navarrete, Marta
Perea, Gertrudis
Covelo, Ana
Martín-Fernández, Mario
Shigemoto, Ryuichi
Luján, Rafael
Araque, Alfonso
author Gómez-Gonzalo, Marta
author_facet Gómez-Gonzalo, Marta
Navarrete, Marta
Perea, Gertrudis
Covelo, Ana
Martín-Fernández, Mario
Shigemoto, Ryuichi
Luján, Rafael
Araque, Alfonso
author_role author
author2 Navarrete, Marta
Perea, Gertrudis
Covelo, Ana
Martín-Fernández, Mario
Shigemoto, Ryuichi
Luján, Rafael
Araque, Alfonso
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Cajal Blue Brain
European Commission
Ministerio de Economía y Competitividad (España)
CSIC - Patronato Santiago Ramón y Cajal de Ciencias Naturales y Médicas
dc.subject.none.fl_str_mv Endocannabinoid signaling
Astrocytes
mGluRs
Nitric oxide
LTP
topic Endocannabinoid signaling
Astrocytes
mGluRs
Nitric oxide
LTP
description Endocannabinoids (eCBs) play key roles in brain function, acting as modulatory signals in synaptic transmission and plasticity. They are recognized as retrograde messengers that mediate long-term synaptic depression (LTD), but their ability to induce long-term potentiation (LTP) is poorly known. We show that eCBs induce the long-term enhancement of transmitter release at single hippocampal synapses through stimulation of astrocytes when coincident with postsynaptic activity. This LTP requires the coordinated activity of the 3 elements of the tripartite synapse: 1) eCB-evoked astrocyte calcium signal that stimulates glutamate release; 2) postsynaptic nitric oxide production; and 3) activation of protein kinase C and presynaptic group I metabotropic glutamate receptors, whose location at presynaptic sites was confirmed by immunoelectron microscopy. Hence, while eCBs act as retrograde signals to depress homoneuronal synapses, they serve as lateral messengers to induce LTP in distant heteroneuronal synapses through stimulation of astrocytes. Therefore, eCBs can trigger LTP through stimulation of astrocyte-neuron signaling, revealing novel cellular mechanisms of eCB effects on synaptic plasticity.
publishDate 2015
dc.date.none.fl_str_mv 2015
2016
2016
2016
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/133875
url http://hdl.handle.net/10261/133875
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/EC/FP7/202167
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,812455

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