Amygdalar CB2 cannabinoid receptor mediates fear extinction deficits promoted by orexin-A/hypocretin-1

Anxiety and stress disorders are often characterized by an inability to extinguish learned fear responses. Orexins/hypocretins are involved in the modulation of aversive memories, and dysregulation of this system may contribute to the aetiology of anxiety disorders characterized by pathological fear...

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Detalles Bibliográficos
Autores: Ten-Blanco, Marc, Flores de los Heros, África, 1985-, Pereda-Pérez, Inmaculada, Piscitelli, Fabiana, Izquierdo-Luengo, Cristina, Cristino, Luigia, Romero, Julián, Hillard, Cecilia J., Maldonado, Rafael, 1961-, Di Marzo, Vicenzo, Berrendero Díaz, Fernando, 1971-
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2022
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/53421
Acceso en línea:http://hdl.handle.net/10230/53421
http://dx.doi.org/10.1016/j.biopha.2022.112925
Access Level:acceso abierto
Palabra clave:Orexin
Fear extinction
Amygdala
2-AG
CB2R
Microglia
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spelling Amygdalar CB2 cannabinoid receptor mediates fear extinction deficits promoted by orexin-A/hypocretin-1Ten-Blanco, MarcFlores de los Heros, África, 1985-Pereda-Pérez, InmaculadaPiscitelli, FabianaIzquierdo-Luengo, CristinaCristino, LuigiaRomero, JuliánHillard, Cecilia J.Maldonado, Rafael, 1961-Di Marzo, VicenzoBerrendero Díaz, Fernando, 1971-OrexinFear extinctionAmygdala2-AGCB2RMicrogliaAnxiety and stress disorders are often characterized by an inability to extinguish learned fear responses. Orexins/hypocretins are involved in the modulation of aversive memories, and dysregulation of this system may contribute to the aetiology of anxiety disorders characterized by pathological fear. The mechanisms by which orexins regulate fear are unknown. Here we investigated the role of the endogenous cannabinoid system in the impaired fear extinction induced by orexin-A (OXA) in male mice. The selective inhibitor of 2-arachidonoylglycerol (2-AG) biosynthesis O7460 abolished the fear extinction deficits induced by OXA. Accordingly, increased 2-AG levels were observed in the amygdala and hippocampus of mice treated with OXA that do not extinguish fear, suggesting that high levels of this endocannabinoid are related to poor extinction. Impairment of fear extinction induced by OXA was associated with increased expression of CB2 cannabinoid receptor (CB2R) in microglial cells of the basolateral amygdala. Consistently, the intra-amygdala infusion of the CB2R antagonist AM630 completely blocked the impaired extinction promoted by OXA. Microglial and CB2R expression depletion in the amygdala with PLX5622 chow also prevented these extinction deficits. These results show that overactivation of the orexin system leads to impaired fear extinction through 2-AG and amygdalar CB2R. This novel mechanism could be of relevance for the development of novel potential approaches to treat diseases associated with inappropriate retention of fear, such as post-traumatic stress disorder, panic anxiety and phobias.This work was supported by MICINN [PID2020-116579RB-100/AEI/10.13039/501100011033] and "Ministerio de Economía y Competitividad" MINECO/FEDER, UE [SAF2017-85299-R] to FB and [PID2019-108992-RB-100] to JR, "Plan Nacional sobre Drogas" [#2019I024] to FB and “Proyectos de investigación Universidad Francisco de Vitoria [2018-2019]" to FB. M.T-B and C.I-L are supported by a predoctoral fellowship from Universidad Francisco de Vitoria. Any of the funding sources were involved in the study design and preparation. We are grateful to Dr Rosa María Tolón for her guidance on RT-PCR analyses, and Dr M. Ruth Pazos and Mario Amores for their assistance with microscopy evaluation.Elsevier202220222022info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/53421http://dx.doi.org/10.1016/j.biopha.2022.112925reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésBiomed Pharmacother. 2022 May;149:112925info:eu-repo/grantAgreement/ES/2PE/PID2020-116579RB-100info:eu-repo/grantAgreement/ES/2PE/SAF2017-85299-Rinfo:eu-repo/grantAgreement/ES/2PE/PID2019-108992-RB-100© 2022 The Author(s). Published by Elsevier Masson SAS. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).http://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/534212026-05-29T05:05:01Z
dc.title.none.fl_str_mv Amygdalar CB2 cannabinoid receptor mediates fear extinction deficits promoted by orexin-A/hypocretin-1
title Amygdalar CB2 cannabinoid receptor mediates fear extinction deficits promoted by orexin-A/hypocretin-1
spellingShingle Amygdalar CB2 cannabinoid receptor mediates fear extinction deficits promoted by orexin-A/hypocretin-1
Ten-Blanco, Marc
Orexin
Fear extinction
Amygdala
2-AG
CB2R
Microglia
title_short Amygdalar CB2 cannabinoid receptor mediates fear extinction deficits promoted by orexin-A/hypocretin-1
title_full Amygdalar CB2 cannabinoid receptor mediates fear extinction deficits promoted by orexin-A/hypocretin-1
title_fullStr Amygdalar CB2 cannabinoid receptor mediates fear extinction deficits promoted by orexin-A/hypocretin-1
title_full_unstemmed Amygdalar CB2 cannabinoid receptor mediates fear extinction deficits promoted by orexin-A/hypocretin-1
title_sort Amygdalar CB2 cannabinoid receptor mediates fear extinction deficits promoted by orexin-A/hypocretin-1
dc.creator.none.fl_str_mv Ten-Blanco, Marc
Flores de los Heros, África, 1985-
Pereda-Pérez, Inmaculada
Piscitelli, Fabiana
Izquierdo-Luengo, Cristina
Cristino, Luigia
Romero, Julián
Hillard, Cecilia J.
Maldonado, Rafael, 1961-
Di Marzo, Vicenzo
Berrendero Díaz, Fernando, 1971-
author Ten-Blanco, Marc
author_facet Ten-Blanco, Marc
Flores de los Heros, África, 1985-
Pereda-Pérez, Inmaculada
Piscitelli, Fabiana
Izquierdo-Luengo, Cristina
Cristino, Luigia
Romero, Julián
Hillard, Cecilia J.
Maldonado, Rafael, 1961-
Di Marzo, Vicenzo
Berrendero Díaz, Fernando, 1971-
author_role author
author2 Flores de los Heros, África, 1985-
Pereda-Pérez, Inmaculada
Piscitelli, Fabiana
Izquierdo-Luengo, Cristina
Cristino, Luigia
Romero, Julián
Hillard, Cecilia J.
Maldonado, Rafael, 1961-
Di Marzo, Vicenzo
Berrendero Díaz, Fernando, 1971-
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Orexin
Fear extinction
Amygdala
2-AG
CB2R
Microglia
topic Orexin
Fear extinction
Amygdala
2-AG
CB2R
Microglia
description Anxiety and stress disorders are often characterized by an inability to extinguish learned fear responses. Orexins/hypocretins are involved in the modulation of aversive memories, and dysregulation of this system may contribute to the aetiology of anxiety disorders characterized by pathological fear. The mechanisms by which orexins regulate fear are unknown. Here we investigated the role of the endogenous cannabinoid system in the impaired fear extinction induced by orexin-A (OXA) in male mice. The selective inhibitor of 2-arachidonoylglycerol (2-AG) biosynthesis O7460 abolished the fear extinction deficits induced by OXA. Accordingly, increased 2-AG levels were observed in the amygdala and hippocampus of mice treated with OXA that do not extinguish fear, suggesting that high levels of this endocannabinoid are related to poor extinction. Impairment of fear extinction induced by OXA was associated with increased expression of CB2 cannabinoid receptor (CB2R) in microglial cells of the basolateral amygdala. Consistently, the intra-amygdala infusion of the CB2R antagonist AM630 completely blocked the impaired extinction promoted by OXA. Microglial and CB2R expression depletion in the amygdala with PLX5622 chow also prevented these extinction deficits. These results show that overactivation of the orexin system leads to impaired fear extinction through 2-AG and amygdalar CB2R. This novel mechanism could be of relevance for the development of novel potential approaches to treat diseases associated with inappropriate retention of fear, such as post-traumatic stress disorder, panic anxiety and phobias.
publishDate 2022
dc.date.none.fl_str_mv 2022
2022
2022
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/53421
http://dx.doi.org/10.1016/j.biopha.2022.112925
url http://hdl.handle.net/10230/53421
http://dx.doi.org/10.1016/j.biopha.2022.112925
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Biomed Pharmacother. 2022 May;149:112925
info:eu-repo/grantAgreement/ES/2PE/PID2020-116579RB-100
info:eu-repo/grantAgreement/ES/2PE/SAF2017-85299-R
info:eu-repo/grantAgreement/ES/2PE/PID2019-108992-RB-100
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
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