Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble
The epigenome and three-dimensional (3D) genomic architecture are emerging as key factors in the dynamic regulation of different transcriptional programs required for neuronal functions. In this study, we used an activity-dependent tagging system in mice to determine the epigenetic state, 3D genome...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Springer Science and Business Media LLC
2021
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| Online Access: | https://hdl.handle.net/1721.1/130450 |
| _version_ | 1826203937394393088 |
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| author | Marco, Asaf Meharena, Hiruy S. Dileep, Vishnu Raju, Ravikiran M. Davila Velderrain, Jose Zhang, Amy Letao Adaikkan, Chinnakkaruppan Young, Jennie Zin-Ney Gao, Fan Kellis, Manolis Tsai, Li-Huei |
| author2 | Picower Institute for Learning and Memory |
| author_facet | Picower Institute for Learning and Memory Marco, Asaf Meharena, Hiruy S. Dileep, Vishnu Raju, Ravikiran M. Davila Velderrain, Jose Zhang, Amy Letao Adaikkan, Chinnakkaruppan Young, Jennie Zin-Ney Gao, Fan Kellis, Manolis Tsai, Li-Huei |
| author_sort | Marco, Asaf |
| collection | MIT |
| description | The epigenome and three-dimensional (3D) genomic architecture are emerging as key factors in the dynamic regulation of different transcriptional programs required for neuronal functions. In this study, we used an activity-dependent tagging system in mice to determine the epigenetic state, 3D genome architecture and transcriptional landscape of engram cells over the lifespan of memory formation and recall. Our findings reveal that memory encoding leads to an epigenetic priming event, marked by increased accessibility of enhancers without the corresponding transcriptional changes. Memory consolidation subsequently results in spatial reorganization of large chromatin segments and promoter–enhancer interactions. Finally, with reactivation, engram neurons use a subset of de novo long-range interactions, where primed enhancers are brought in contact with their respective promoters to upregulate genes involved in local protein translation in synaptic compartments. Collectively, our work elucidates the comprehensive transcriptional and epigenomic landscape across the lifespan of memory formation and recall in the hippocampal engram ensemble. |
| first_indexed | 2024-09-23T12:45:47Z |
| format | Article |
| id | mit-1721.1/130450 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T12:45:47Z |
| publishDate | 2021 |
| publisher | Springer Science and Business Media LLC |
| record_format | dspace |
| spelling | mit-1721.1/1304502022-10-01T10:57:46Z Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble Marco, Asaf Meharena, Hiruy S. Dileep, Vishnu Raju, Ravikiran M. Davila Velderrain, Jose Zhang, Amy Letao Adaikkan, Chinnakkaruppan Young, Jennie Zin-Ney Gao, Fan Kellis, Manolis Tsai, Li-Huei Picower Institute for Learning and Memory Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Massachusetts Institute of Technology. Computer Science and Artificial Intelligence Laboratory The epigenome and three-dimensional (3D) genomic architecture are emerging as key factors in the dynamic regulation of different transcriptional programs required for neuronal functions. In this study, we used an activity-dependent tagging system in mice to determine the epigenetic state, 3D genome architecture and transcriptional landscape of engram cells over the lifespan of memory formation and recall. Our findings reveal that memory encoding leads to an epigenetic priming event, marked by increased accessibility of enhancers without the corresponding transcriptional changes. Memory consolidation subsequently results in spatial reorganization of large chromatin segments and promoter–enhancer interactions. Finally, with reactivation, engram neurons use a subset of de novo long-range interactions, where primed enhancers are brought in contact with their respective promoters to upregulate genes involved in local protein translation in synaptic compartments. Collectively, our work elucidates the comprehensive transcriptional and epigenomic landscape across the lifespan of memory formation and recall in the hippocampal engram ensemble. National Institutes of Health (Grants RF1AG062377, AF1AG054012, RO1NS102730, RF1AG064321, R01AG058002, U01NS110453, R01AG062335, UG3NS115064, R01AG067151, R01MH109978, U01MH119509, R01HG008155, U24HG009446, 5T32HD09806) 2021-04-12T16:00:55Z 2021-04-12T16:00:55Z 2020-10 2020-01 2021-04-06T15:30:40Z Article http://purl.org/eprint/type/JournalArticle 1097-6256 1546-1726 https://hdl.handle.net/1721.1/130450 Marco, Asaf et al. "Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble." Nature Neuroscience 23, 12 (October 2020): 1606–1617. © 2020 The Author(s) en http://dx.doi.org/10.1038/s41593-020-00717-0 Nature Neuroscience Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Springer Science and Business Media LLC PMC |
| spellingShingle | Marco, Asaf Meharena, Hiruy S. Dileep, Vishnu Raju, Ravikiran M. Davila Velderrain, Jose Zhang, Amy Letao Adaikkan, Chinnakkaruppan Young, Jennie Zin-Ney Gao, Fan Kellis, Manolis Tsai, Li-Huei Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble |
| title | Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble |
| title_full | Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble |
| title_fullStr | Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble |
| title_full_unstemmed | Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble |
| title_short | Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble |
| title_sort | mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble |
| url | https://hdl.handle.net/1721.1/130450 |
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