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...

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Authors: 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
Format: Article
Status:Published version
Publication date:2021
Country:España
Institution:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repository:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/49052
Online Access:http://hdl.handle.net/10230/49052
http://dx.doi.org/10.3389/fnmol.2021.664912
Access Level:Open access
Keyword:3D genome organization
Hi-C
Chromatin accessibility
Environmental enrichment
Epigenetics
Inter-chromosomal contacts
Learning
Postnatal development
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author Espeso Gil, Sergio, 1985-
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
author_browse Akbarian, Schahram
Albaigès-Ràfols, Júlia
Bonnin, Sarah
Chandrasekaran, Sandhya
Dierssen, Mara
Espeso Gil, Sergio, 1985-
Friedländer, Marc R.
Holik, Aliaksei Z.
Hor, Charlotte N.
Irimia Martínez, Manuel
Jhanwar, Shalu, 1986-
Maass, Philipp G.
Maher, Michael
Ossowski, Stephan
Permanyer, Jon
Pique Regi, Roger
Pons Espinal, Meritxell, 1986-
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
collection Recercat. Dipósit de la Recerca de Catalunya
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.
eu_rights_str_mv openAccess
format article
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institution 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)
network_acronym_str ES
network_name_str España
oai_identifier_str oai:recercat.cat:10230/49052
publishDate 2021
publishDateSort 2021
publisher Frontiers
publisherStr Frontiers
reponame_str Recercat. Dipósit de la Recerca de Catalunya
spelling Environmental enrichment induces epigenomic and genome organization changes relevant for cognition 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 3D genome organization Hi-C Chromatin accessibility Environmental enrichment Epigenetics Inter-chromosomal contacts Learning Postnatal development 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. 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. Frontiers http://hdl.handle.net/10230/49052 http://dx.doi.org/10.3389/fnmol.2021.664912
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
status_str publishedVersion
title 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_short Environmental enrichment induces epigenomic and genome organization changes relevant for cognition
title_sort Environmental enrichment induces epigenomic and genome organization changes relevant for cognition
topic 3D genome organization
Hi-C
Chromatin accessibility
Environmental enrichment
Epigenetics
Inter-chromosomal contacts
Learning
Postnatal development
topic_facet 3D genome organization
Hi-C
Chromatin accessibility
Environmental enrichment
Epigenetics
Inter-chromosomal contacts
Learning
Postnatal development
url http://hdl.handle.net/10230/49052
http://dx.doi.org/10.3389/fnmol.2021.664912