Cell-type- and region-specific modulation of cocaine seeking by micro-RNA-1 in striatal projection neurons

The persistent and experience-dependent nature of drug addiction may result in part from epigenetic alterations, including non-coding micro-RNAs (miRNAs), which are both critical for neuronal function and modulated by cocaine in the striatum. Two major striatal cell populations, the striato-nigral a...

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Autores: Forget, Benoit, Martín García, Elena, 1975-, Godino, Arthur, Domingo Rodriguez, Laura, 1992-, Kappes, Vincent, Poirier, Pierre, Andrianarivelo, Andry, Senabre, Eric, Allichon, Marie-Charlotte, Marias, Mélanie, Vanhoutte, Peter, Girault, Jean-Antoine, Maldonado, Rafael, 1961-, Caboche, Jocelyne
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2021
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/49213
Acceso en línea:http://hdl.handle.net/10230/49213
http://dx.doi.org/10.1038/s41380-021-01328-2
Access Level:acceso abierto
Palabra clave:Molecular biology
Neuroscience
Physiology
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv Cell-type- and region-specific modulation of cocaine seeking by micro-RNA-1 in striatal projection neurons
title Cell-type- and region-specific modulation of cocaine seeking by micro-RNA-1 in striatal projection neurons
spellingShingle Cell-type- and region-specific modulation of cocaine seeking by micro-RNA-1 in striatal projection neurons
Forget, Benoit
Molecular biology
Neuroscience
Physiology
title_short Cell-type- and region-specific modulation of cocaine seeking by micro-RNA-1 in striatal projection neurons
title_full Cell-type- and region-specific modulation of cocaine seeking by micro-RNA-1 in striatal projection neurons
title_fullStr Cell-type- and region-specific modulation of cocaine seeking by micro-RNA-1 in striatal projection neurons
title_full_unstemmed Cell-type- and region-specific modulation of cocaine seeking by micro-RNA-1 in striatal projection neurons
title_sort Cell-type- and region-specific modulation of cocaine seeking by micro-RNA-1 in striatal projection neurons
dc.creator.none.fl_str_mv Forget, Benoit
Martín García, Elena, 1975-
Godino, Arthur
Domingo Rodriguez, Laura, 1992-
Kappes, Vincent
Poirier, Pierre
Andrianarivelo, Andry
Senabre, Eric
Allichon, Marie-Charlotte
Marias, Mélanie
Vanhoutte, Peter
Girault, Jean-Antoine
Maldonado, Rafael, 1961-
Caboche, Jocelyne
author Forget, Benoit
author_facet Forget, Benoit
Martín García, Elena, 1975-
Godino, Arthur
Domingo Rodriguez, Laura, 1992-
Kappes, Vincent
Poirier, Pierre
Andrianarivelo, Andry
Senabre, Eric
Allichon, Marie-Charlotte
Marias, Mélanie
Vanhoutte, Peter
Girault, Jean-Antoine
Maldonado, Rafael, 1961-
Caboche, Jocelyne
author_role author
author2 Martín García, Elena, 1975-
Godino, Arthur
Domingo Rodriguez, Laura, 1992-
Kappes, Vincent
Poirier, Pierre
Andrianarivelo, Andry
Senabre, Eric
Allichon, Marie-Charlotte
Marias, Mélanie
Vanhoutte, Peter
Girault, Jean-Antoine
Maldonado, Rafael, 1961-
Caboche, Jocelyne
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Molecular biology
Neuroscience
Physiology
topic Molecular biology
Neuroscience
Physiology
description The persistent and experience-dependent nature of drug addiction may result in part from epigenetic alterations, including non-coding micro-RNAs (miRNAs), which are both critical for neuronal function and modulated by cocaine in the striatum. Two major striatal cell populations, the striato-nigral and striato-pallidal projection neurons, express, respectively, the D1 (D1-SPNs) and D2 (D2-SPNs) dopamine receptor, and display distinct but complementary functions in drug-evoked responses. However, a cell-type-specific role for miRNAs action has yet to be clarified. Here, we evaluated the expression of a subset of miRNAs proposed to modulate cocaine effects in the nucleus accumbens (NAc) and dorsal striatum (DS) upon sustained cocaine exposure in mice and showed that these selected miRNAs were preferentially upregulated in the NAc. We focused on miR-1 considering the important role of some of its predicted mRNA targets, Fosb and Npas4, in the effects of cocaine. We validated these targets in vitro and in vivo. We explored the potential of miR-1 to regulate cocaine-induced behavior by overexpressing it in specific striatal cell populations. In DS D1-SPNs miR-1 overexpression downregulated Fosb and Npas4 and reduced cocaine-induced CPP reinstatement, but increased cue-induced cocaine seeking. In DS D2-SPNs miR-1 overexpression reduced the motivation to self-administer cocaine. Our results indicate a role of miR1 and its target genes, Fosb and Npas4, in these behaviors and highlight a precise cell-type- and region-specific modulatory role of miR-1, illustrating the importance of cell-specific investigations.
publishDate 2021
dc.date.none.fl_str_mv 2021
2021
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/10230/49213
http://dx.doi.org/10.1038/s41380-021-01328-2
url http://hdl.handle.net/10230/49213
http://dx.doi.org/10.1038/s41380-021-01328-2
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Mol Psychiatry. 2022 Feb;27(2):918-28
info:eu-repo/grantAgreement/ES/2PE/SAF2017-84060-R
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature Research
publisher.none.fl_str_mv Nature Research
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Cell-type- and region-specific modulation of cocaine seeking by micro-RNA-1 in striatal projection neuronsForget, BenoitMartín García, Elena, 1975-Godino, ArthurDomingo Rodriguez, Laura, 1992-Kappes, VincentPoirier, PierreAndrianarivelo, AndrySenabre, EricAllichon, Marie-CharlotteMarias, MélanieVanhoutte, PeterGirault, Jean-AntoineMaldonado, Rafael, 1961-Caboche, JocelyneMolecular biologyNeurosciencePhysiologyThe persistent and experience-dependent nature of drug addiction may result in part from epigenetic alterations, including non-coding micro-RNAs (miRNAs), which are both critical for neuronal function and modulated by cocaine in the striatum. Two major striatal cell populations, the striato-nigral and striato-pallidal projection neurons, express, respectively, the D1 (D1-SPNs) and D2 (D2-SPNs) dopamine receptor, and display distinct but complementary functions in drug-evoked responses. However, a cell-type-specific role for miRNAs action has yet to be clarified. Here, we evaluated the expression of a subset of miRNAs proposed to modulate cocaine effects in the nucleus accumbens (NAc) and dorsal striatum (DS) upon sustained cocaine exposure in mice and showed that these selected miRNAs were preferentially upregulated in the NAc. We focused on miR-1 considering the important role of some of its predicted mRNA targets, Fosb and Npas4, in the effects of cocaine. We validated these targets in vitro and in vivo. We explored the potential of miR-1 to regulate cocaine-induced behavior by overexpressing it in specific striatal cell populations. In DS D1-SPNs miR-1 overexpression downregulated Fosb and Npas4 and reduced cocaine-induced CPP reinstatement, but increased cue-induced cocaine seeking. In DS D2-SPNs miR-1 overexpression reduced the motivation to self-administer cocaine. Our results indicate a role of miR1 and its target genes, Fosb and Npas4, in these behaviors and highlight a precise cell-type- and region-specific modulatory role of miR-1, illustrating the importance of cell-specific investigations.This work was supported by Fondation pour la Recherche Médicale (DEQ20150734352 to JC), Centre National pour la Recherche Scientifique (CNRS, B.F., A.G., V.K., P.P., P.V., J.C.), Institut National pour la Santé et la Recherche Médicale (INSERM; B.F., A.G., V.K., P.P., P.V., J.-A.G., J.C.), Sorbonne Université, Faculté des Sciences et Ingénierie (B.F., A.G., V.K., P.P., P.V., J.-A.G., J.C.) Labex Biopsy Investissements d’Avenir, ANR-11-IDEX-0004-02 (B.F., A.G., V.K., P.P., P.V., J.-A.G., J.C.), the Spanish Ministerio de Economía y Competitividad-MINECO (#SAF2017-84060-R-AEI/FEDER-UE; E.M.-G., L.D.-R., R.M.), the Spanish Instituto de Salud Carlos III, RETICS-RTA (#RD12/0028/0023; E.M.-G., L.D.-R., R.M.), the Generalitat de Catalunya, AGAUR (#2017-SGR-669; E.M.-G., L.D.-R., R.M.), ICREA-Acadèmia (#2015) and the Spanish Ministerio de Sanidad, Servicios Sociales e Igualdad, Plan Nacional Sobre Drogas (#PNSD-2017I068) to R.M., Fundació La Marató-TV3 (#2016/20-30) to E.M.-G. Fondation pour la Recherche Médicale (FRM#DPA20140629798) and ANR (ANR-16-CE16-0018) to J.A.G.Nature Research202120212022info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/49213http://dx.doi.org/10.1038/s41380-021-01328-2reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésMol Psychiatry. 2022 Feb;27(2):918-28info:eu-repo/grantAgreement/ES/2PE/SAF2017-84060-R© The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/492132026-06-12T07:21:37Z
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