Frontiers in Molecular Neuroscience (May 2021)
Environmental Enrichment Induces Epigenomic and Genome Organization Changes Relevant for Cognition
- Sergio Espeso-Gil,
- Sergio Espeso-Gil,
- Sergio Espeso-Gil,
- Aliaksei Z. Holik,
- Sarah Bonnin,
- Shalu Jhanwar,
- Shalu Jhanwar,
- Sandhya Chandrasekaran,
- Sandhya Chandrasekaran,
- Roger Pique-Regi,
- Júlia Albaigès-Ràfols,
- Júlia Albaigès-Ràfols,
- Michael Maher,
- Michael Maher,
- Michael Maher,
- Jon Permanyer,
- Manuel Irimia,
- Manuel Irimia,
- Manuel Irimia,
- Marc R. Friedländer,
- Meritxell Pons-Espinal,
- Meritxell Pons-Espinal,
- Schahram Akbarian,
- Mara Dierssen,
- Mara Dierssen,
- Philipp G. Maass,
- Philipp G. Maass,
- Charlotte N. Hor,
- Charlotte N. Hor,
- Stephan Ossowski,
- Stephan Ossowski
Affiliations
- Sergio Espeso-Gil
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Sergio Espeso-Gil
- Universitat Pompeu Fabra (UPF), Barcelona, Spain
- Sergio Espeso-Gil
- Genetics and Genome Biology Program, SickKids Research Institute, Toronto, ON, Canada
- Aliaksei Z. Holik
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Sarah Bonnin
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Shalu Jhanwar
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Shalu Jhanwar
- Universitat Pompeu Fabra (UPF), Barcelona, Spain
- Sandhya Chandrasekaran
- MD/PhD Program in the Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, United States
- Sandhya Chandrasekaran
- Department of Psychiatry and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United States
- Roger Pique-Regi
- Center for Molecular Medicine and Genetics, Wayne State University, Detroit, MI, United States
- Júlia Albaigès-Ràfols
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Júlia Albaigès-Ràfols
- Universitat Pompeu Fabra (UPF), Barcelona, Spain
- Michael Maher
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Michael Maher
- Universitat Pompeu Fabra (UPF), Barcelona, Spain
- Michael Maher
- Universitat Pompeu Fabra (UPF), Barcelona, Spain
- Jon Permanyer
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Manuel Irimia
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Manuel Irimia
- Universitat Pompeu Fabra (UPF), Barcelona, Spain
- Manuel Irimia
- ICREA, Pg. Lluis Companys 23, Barcelona, Spain
- Marc R. Friedländer
- Science for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, Sweden
- Meritxell Pons-Espinal
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Meritxell Pons-Espinal
- Universitat Pompeu Fabra (UPF), Barcelona, Spain
- Schahram Akbarian
- Department of Psychiatry and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United States
- Mara Dierssen
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Mara Dierssen
- Universitat Pompeu Fabra (UPF), Barcelona, Spain
- Philipp G. Maass
- Genetics and Genome Biology Program, SickKids Research Institute, Toronto, ON, Canada
- Philipp G. Maass
- Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada
- Charlotte N. Hor
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Charlotte N. Hor
- Universitat Pompeu Fabra (UPF), Barcelona, Spain
- Stephan Ossowski
- Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Stephan Ossowski
- Universitat Pompeu Fabra (UPF), Barcelona, Spain
- DOI
- https://doi.org/10.3389/fnmol.2021.664912
- Journal volume & issue
-
Vol. 14
Abstract
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.
Keywords
- environmental enrichment
- epigenetics
- 3D genome organization
- learning
- postnatal development
- chromatin accessibility
