Environmental enrichment induces epigenomic and genome organization changes relevant for cognition
In early development, the environment triggers mnemonic epigenomic programs resulting in memory and learning experiences to confer cognitive phenotypes into adulthood. To uncover how environmental stimulation impacts the epigenome and genome organization, we used the paradigm of environmental enrich...
| Autores: | , , , , , , , , , , , , , , , , |
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| 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:10230/49052 |
| Acceso en línea: | http://hdl.handle.net/10230/49052 http://dx.doi.org/10.3389/fnmol.2021.664912 |
| Access Level: | acceso abierto |
| Palabra clave: | 3D genome organization Hi-C Chromatin accessibility Environmental enrichment Epigenetics Inter-chromosomal contacts Learning Postnatal development |
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Environmental enrichment induces epigenomic and genome organization changes relevant for cognitionEspeso Gil, Sergio, 1985-Holik, Aliaksei Z.Bonnin, SarahJhanwar, Shalu, 1986-Chandrasekaran, SandhyaPique Regi, RogerAlbaigès-Ràfols, JúliaMaher, MichaelPermanyer, JonIrimia Martínez, ManuelFriedländer, Marc R.Pons Espinal, Meritxell, 1986-Akbarian, SchahramDierssen, MaraMaass, Philipp G.Hor, Charlotte N.Ossowski, Stephan3D genome organizationHi-CChromatin accessibilityEnvironmental enrichmentEpigeneticsInter-chromosomal contactsLearningPostnatal developmentIn early development, the environment triggers mnemonic epigenomic programs resulting in memory and learning experiences to confer cognitive phenotypes into adulthood. To uncover how environmental stimulation impacts the epigenome and genome organization, we used the paradigm of environmental enrichment (EE) in young mice constantly receiving novel stimulation. We profiled epigenome and chromatin architecture in whole cortex and sorted neurons by deep-sequencing techniques. Specifically, we studied chromatin accessibility, gene and protein regulation, and 3D genome conformation, combined with predicted enhancer and chromatin interactions. We identified increased chromatin accessibility, transcription factor binding including CTCF-mediated insulation, differential occupancy of H3K36me3 and H3K79me2, and changes in transcriptional programs required for neuronal development. EE stimuli led to local genome re-organization by inducing increased contacts between chromosomes 7 and 17 (inter-chromosomal). Our findings support the notion that EE-induced learning and memory processes are directly associated with the epigenome and genome organization.We acknowledge support of the Spanish Ministry of Economy and Competitiveness (SAF2011-26216), “Centro de Excelencia Severo Ochoa 2017-2021,” SEV-2016-0571, the CERCA Programme/Generalitat de Catalunya and Jerome Lejeune Foundation, Swiss National Science Foundation Fellowship (PBLAP3_136878) and Co-funded by Marie Curie Actions to CNH. Resources for analyses conducted by SE-G were partially supported by the U.S. National Institutes of Mental Health Funds R01MH104341 and R01MH117790 and by the Social Sciences and Humanities Research Council of Canada (NFRFE-2018-01305). We acknowledge support of the Spanish Ministry of Science and Innovation to the EMBL partnership, Agencia Estatal de Investigaci n (PID2019-110755RB-I00/AEI / 10.13039/501100011033), the European Union’s Horizon 2020 Research and Innovation programme under grant agreement No 848077, Jerôme Lejeune Foundation, NIH (Grant Number: 1R01EB 028159-01), Marató TV3 (#2016/20-30). RP-R resources were supported by R01GM109215. We thank the support of the University of Tübingen for the Open Access Publication Funds contribution.Frontiers202120212021info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/49052http://dx.doi.org/10.3389/fnmol.2021.664912reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésFront Mol Neurosci. 2021;14:664912info:eu-repo/grantAgreement/EC/H2020/848077info:eu-repo/grantAgreement/ES/3PN/SAF2011-26216© 2021 Espeso-Gil, Holik, Bonnin, Jhanwar, Chandrasekaran, Pique-Regi, Albaigès-Ràfols, Maher, Permanyer, Irimia, Friedländer, Pons-Espinal, Akbarian, Dierssen, Maass, Hor and Ossowski. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/490522026-06-12T07:21:37Z |
| dc.title.none.fl_str_mv |
Environmental enrichment induces epigenomic and genome organization changes relevant for cognition |
| title |
Environmental enrichment induces epigenomic and genome organization changes relevant for cognition |
| spellingShingle |
Environmental enrichment induces epigenomic and genome organization changes relevant for cognition Espeso Gil, Sergio, 1985- 3D genome organization Hi-C Chromatin accessibility Environmental enrichment Epigenetics Inter-chromosomal contacts Learning Postnatal development |
| title_short |
Environmental enrichment induces epigenomic and genome organization changes relevant for cognition |
| title_full |
Environmental enrichment induces epigenomic and genome organization changes relevant for cognition |
| title_fullStr |
Environmental enrichment induces epigenomic and genome organization changes relevant for cognition |
| title_full_unstemmed |
Environmental enrichment induces epigenomic and genome organization changes relevant for cognition |
| title_sort |
Environmental enrichment induces epigenomic and genome organization changes relevant for cognition |
| dc.creator.none.fl_str_mv |
Espeso Gil, Sergio, 1985- Holik, Aliaksei Z. Bonnin, Sarah Jhanwar, Shalu, 1986- Chandrasekaran, Sandhya Pique Regi, Roger Albaigès-Ràfols, Júlia Maher, Michael Permanyer, Jon Irimia Martínez, Manuel Friedländer, Marc R. Pons Espinal, Meritxell, 1986- Akbarian, Schahram Dierssen, Mara Maass, Philipp G. Hor, Charlotte N. Ossowski, Stephan |
| author |
Espeso Gil, Sergio, 1985- |
| author_facet |
Espeso Gil, Sergio, 1985- Holik, Aliaksei Z. Bonnin, Sarah Jhanwar, Shalu, 1986- Chandrasekaran, Sandhya Pique Regi, Roger Albaigès-Ràfols, Júlia Maher, Michael Permanyer, Jon Irimia Martínez, Manuel Friedländer, Marc R. Pons Espinal, Meritxell, 1986- Akbarian, Schahram Dierssen, Mara Maass, Philipp G. Hor, Charlotte N. Ossowski, Stephan |
| author_role |
author |
| author2 |
Holik, Aliaksei Z. Bonnin, Sarah Jhanwar, Shalu, 1986- Chandrasekaran, Sandhya Pique Regi, Roger Albaigès-Ràfols, Júlia Maher, Michael Permanyer, Jon Irimia Martínez, Manuel Friedländer, Marc R. Pons Espinal, Meritxell, 1986- Akbarian, Schahram Dierssen, Mara Maass, Philipp G. Hor, Charlotte N. Ossowski, Stephan |
| author2_role |
author author author author author author author author author author author author author author author author |
| dc.subject.none.fl_str_mv |
3D genome organization Hi-C Chromatin accessibility Environmental enrichment Epigenetics Inter-chromosomal contacts Learning Postnatal development |
| topic |
3D genome organization Hi-C Chromatin accessibility Environmental enrichment Epigenetics Inter-chromosomal contacts Learning Postnatal development |
| description |
In early development, the environment triggers mnemonic epigenomic programs resulting in memory and learning experiences to confer cognitive phenotypes into adulthood. To uncover how environmental stimulation impacts the epigenome and genome organization, we used the paradigm of environmental enrichment (EE) in young mice constantly receiving novel stimulation. We profiled epigenome and chromatin architecture in whole cortex and sorted neurons by deep-sequencing techniques. Specifically, we studied chromatin accessibility, gene and protein regulation, and 3D genome conformation, combined with predicted enhancer and chromatin interactions. We identified increased chromatin accessibility, transcription factor binding including CTCF-mediated insulation, differential occupancy of H3K36me3 and H3K79me2, and changes in transcriptional programs required for neuronal development. EE stimuli led to local genome re-organization by inducing increased contacts between chromosomes 7 and 17 (inter-chromosomal). Our findings support the notion that EE-induced learning and memory processes are directly associated with the epigenome and genome organization. |
| publishDate |
2021 |
| dc.date.none.fl_str_mv |
2021 2021 2021 |
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info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion |
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article |
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publishedVersion |
| dc.identifier.none.fl_str_mv |
http://hdl.handle.net/10230/49052 http://dx.doi.org/10.3389/fnmol.2021.664912 |
| url |
http://hdl.handle.net/10230/49052 http://dx.doi.org/10.3389/fnmol.2021.664912 |
| dc.language.none.fl_str_mv |
Inglés |
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Inglés |
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Front Mol Neurosci. 2021;14:664912 info:eu-repo/grantAgreement/EC/H2020/848077 info:eu-repo/grantAgreement/ES/3PN/SAF2011-26216 |
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http://creativecommons.org/licenses/by/4.0/ info:eu-repo/semantics/openAccess |
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http://creativecommons.org/licenses/by/4.0/ |
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openAccess |
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application/pdf application/pdf |
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Frontiers |
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Frontiers |
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reponame:Repositorio Digital de la UPF instname:Universitat Pompeu Fabra |
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