Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcription

Detalhes bibliográficos
Autor(a) principal: Paiva, Isabel
Data de Publicação: 2022
Outros Autores: Cellai, Lucrezia, Meriaux, Céline, Poncelet, Lauranne, Nebie, Ouada, Saliou, Jean-Michel, Lacoste, Anne-Sophie, Papegaey, Anthony, Drobecq, Hervé, Le Gras, Stéphanie, Schneider, Marion, Malik, Enas M, Müller, Christa E., Faivre, Emilie, Carvalho, Kevin, Gomez-Murcia, Victoria, Vieau, Didier, Thiroux, Bryan, Eddarkaoui, Sabiha, Lebouvier, Thibaud, Schueller, Estelle, Tzeplaeff, Laura, Grgurina, Iris, Seguin, Jonathan, Stauber, Jonathan, Lopes, Luísa V., Buee, Luc, Buée-Scherrer, Valerie, Cunha, Rodrigo A., Ait-Belkacem, Rima, Sergeant, Nicolas, Annicotte, Jean-Sébastien, Boutillier, Anne-Laurence, Blum, David
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10316/100338
https://doi.org/10.1172/JCI149371
Resumo: Caffeine is the most consumed psychoactive substance worldwide. Strikingly, molecular pathways engaged by its regular consumption remain unclear. We herein addressed the mechanisms associated with habitual (chronic) caffeine consumption in the mouse hippocampus using untargeted orthogonal-omics techniques. Our results revealed that chronic caffeine exerts concerted pleiotropic effects in the hippocampus, at the epigenomic, proteomic and metabolomic levels. Caffeine lowers metabolic-related processes in the bulk tissue, while it induces neuronal-specific epigenetic changes at synaptic transmission/plasticity-related genes and increased experience-driven transcriptional activity. Altogether, these findings suggest that regular caffeine intake improves the signal-to-noise ratio during information encoding, in part through a fine-tuning of metabolic genes while boosting the salience of information processing during learning in neuronal circuits.
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spelling Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcriptionEpigeneticsMemoryNeurosciencePharmacologyCaffeine is the most consumed psychoactive substance worldwide. Strikingly, molecular pathways engaged by its regular consumption remain unclear. We herein addressed the mechanisms associated with habitual (chronic) caffeine consumption in the mouse hippocampus using untargeted orthogonal-omics techniques. Our results revealed that chronic caffeine exerts concerted pleiotropic effects in the hippocampus, at the epigenomic, proteomic and metabolomic levels. Caffeine lowers metabolic-related processes in the bulk tissue, while it induces neuronal-specific epigenetic changes at synaptic transmission/plasticity-related genes and increased experience-driven transcriptional activity. Altogether, these findings suggest that regular caffeine intake improves the signal-to-noise ratio during information encoding, in part through a fine-tuning of metabolic genes while boosting the salience of information processing during learning in neuronal circuits.This work was supported by grants from Hauts-de-France (PARTEN-AIRR, COGNADORA; START-AIRR, INS-SPECT) and Programs d’Investissements d’Avenir LabEx (excellence laboratory) DISTALZ (Development of Innovative Strategies for a Transdisciplinary approach to ALZheimer’s disease) and EGID (European Genomic Institute for Diabetes ANR-10LABX-46). Our laboratories are also supported by ANR (GRAND to LB, ADORATAU, ADORASTrAU, METABOTAU to DB and BETAPLASTICITY to JSA), COEN (5008), Fondation pour la Recherche Médicale, France Alzheimer/Fondation de France, FHU VasCog research network (Lille, France), Fondation Vaincre Alzheimer (ADOMEMOTAU), European Foundation for the Study of Diabetes (EFSD to JSA), Fondation Plan Alzheimer as well as Inserm, CNRS, Université Lille, Lille Métropole Communauté Urbaine, DN2M. KC hold a doctoral grant from Lille University. VG-M was supported by Fondation pour la Recherche Médicale (SPF20160936000). CM was supported by Région Hauts753 30 754 de-France. ALB is supported by CNRS, Unistra (Strasbourg, France), ANR-16-CE92-0031 755 756 757 758 759 760 761 762 (EPIFUS), ANR-18-CE16-0008-02 (ADORASTrAU), Alsace Alzheimer 67, France Alzheimer (AAP SM 2017 #1664). IP is supported by Fondation pour la Recherche Médicale (SPF201909009162). CEM is grateful for the support by the Alzheimer Forschung Initiative e.V. (AFI, Düsseldorf, Germany). LC was funded by SIF Italian Society of Pharmacology. RAC was supported by LaCaixa Foundation (LCF/PR/HP17/52190001) and FCT (POCI-01-0145-FEDER-03127). Santa Casa da Misericórdia (MB-7-2018) and CEECIND/01497/2017 to LVL.American Society for Clinical Investigation2022-05-10info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://hdl.handle.net/10316/100338http://hdl.handle.net/10316/100338https://doi.org/10.1172/JCI149371eng1558-8238Paiva, IsabelCellai, LucreziaMeriaux, CélinePoncelet, LauranneNebie, OuadaSaliou, Jean-MichelLacoste, Anne-SophiePapegaey, AnthonyDrobecq, HervéLe Gras, StéphanieSchneider, MarionMalik, Enas MMüller, Christa E.Faivre, EmilieCarvalho, KevinGomez-Murcia, VictoriaVieau, DidierThiroux, BryanEddarkaoui, SabihaLebouvier, ThibaudSchueller, EstelleTzeplaeff, LauraGrgurina, IrisSeguin, JonathanStauber, JonathanLopes, Luísa V.Buee, LucBuée-Scherrer, ValerieCunha, Rodrigo A.Ait-Belkacem, RimaSergeant, NicolasAnnicotte, Jean-SébastienBoutillier, Anne-LaurenceBlum, Davidinfo:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-03-01T11:15:54Zoai:estudogeral.uc.pt:10316/100338Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T21:17:44.785032Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcription
title Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcription
spellingShingle Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcription
Paiva, Isabel
Epigenetics
Memory
Neuroscience
Pharmacology
title_short Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcription
title_full Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcription
title_fullStr Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcription
title_full_unstemmed Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcription
title_sort Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcription
author Paiva, Isabel
author_facet Paiva, Isabel
Cellai, Lucrezia
Meriaux, Céline
Poncelet, Lauranne
Nebie, Ouada
Saliou, Jean-Michel
Lacoste, Anne-Sophie
Papegaey, Anthony
Drobecq, Hervé
Le Gras, Stéphanie
Schneider, Marion
Malik, Enas M
Müller, Christa E.
Faivre, Emilie
Carvalho, Kevin
Gomez-Murcia, Victoria
Vieau, Didier
Thiroux, Bryan
Eddarkaoui, Sabiha
Lebouvier, Thibaud
Schueller, Estelle
Tzeplaeff, Laura
Grgurina, Iris
Seguin, Jonathan
Stauber, Jonathan
Lopes, Luísa V.
Buee, Luc
Buée-Scherrer, Valerie
Cunha, Rodrigo A.
Ait-Belkacem, Rima
Sergeant, Nicolas
Annicotte, Jean-Sébastien
Boutillier, Anne-Laurence
Blum, David
author_role author
author2 Cellai, Lucrezia
Meriaux, Céline
Poncelet, Lauranne
Nebie, Ouada
Saliou, Jean-Michel
Lacoste, Anne-Sophie
Papegaey, Anthony
Drobecq, Hervé
Le Gras, Stéphanie
Schneider, Marion
Malik, Enas M
Müller, Christa E.
Faivre, Emilie
Carvalho, Kevin
Gomez-Murcia, Victoria
Vieau, Didier
Thiroux, Bryan
Eddarkaoui, Sabiha
Lebouvier, Thibaud
Schueller, Estelle
Tzeplaeff, Laura
Grgurina, Iris
Seguin, Jonathan
Stauber, Jonathan
Lopes, Luísa V.
Buee, Luc
Buée-Scherrer, Valerie
Cunha, Rodrigo A.
Ait-Belkacem, Rima
Sergeant, Nicolas
Annicotte, Jean-Sébastien
Boutillier, Anne-Laurence
Blum, David
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Paiva, Isabel
Cellai, Lucrezia
Meriaux, Céline
Poncelet, Lauranne
Nebie, Ouada
Saliou, Jean-Michel
Lacoste, Anne-Sophie
Papegaey, Anthony
Drobecq, Hervé
Le Gras, Stéphanie
Schneider, Marion
Malik, Enas M
Müller, Christa E.
Faivre, Emilie
Carvalho, Kevin
Gomez-Murcia, Victoria
Vieau, Didier
Thiroux, Bryan
Eddarkaoui, Sabiha
Lebouvier, Thibaud
Schueller, Estelle
Tzeplaeff, Laura
Grgurina, Iris
Seguin, Jonathan
Stauber, Jonathan
Lopes, Luísa V.
Buee, Luc
Buée-Scherrer, Valerie
Cunha, Rodrigo A.
Ait-Belkacem, Rima
Sergeant, Nicolas
Annicotte, Jean-Sébastien
Boutillier, Anne-Laurence
Blum, David
dc.subject.por.fl_str_mv Epigenetics
Memory
Neuroscience
Pharmacology
topic Epigenetics
Memory
Neuroscience
Pharmacology
description Caffeine is the most consumed psychoactive substance worldwide. Strikingly, molecular pathways engaged by its regular consumption remain unclear. We herein addressed the mechanisms associated with habitual (chronic) caffeine consumption in the mouse hippocampus using untargeted orthogonal-omics techniques. Our results revealed that chronic caffeine exerts concerted pleiotropic effects in the hippocampus, at the epigenomic, proteomic and metabolomic levels. Caffeine lowers metabolic-related processes in the bulk tissue, while it induces neuronal-specific epigenetic changes at synaptic transmission/plasticity-related genes and increased experience-driven transcriptional activity. Altogether, these findings suggest that regular caffeine intake improves the signal-to-noise ratio during information encoding, in part through a fine-tuning of metabolic genes while boosting the salience of information processing during learning in neuronal circuits.
publishDate 2022
dc.date.none.fl_str_mv 2022-05-10
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10316/100338
http://hdl.handle.net/10316/100338
https://doi.org/10.1172/JCI149371
url http://hdl.handle.net/10316/100338
https://doi.org/10.1172/JCI149371
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 1558-8238
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv American Society for Clinical Investigation
publisher.none.fl_str_mv American Society for Clinical Investigation
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
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collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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