Caffeine intake exerts dual genome-wide effects on hippocampal metabolism and learning-dependent transcription
Autor(a) principal: | |
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Data de Publicação: | 2022 |
Outros Autores: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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7160 |
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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 |
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Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
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RCAAP |
reponame_str |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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