Novel environment exposure drives temporally defined and region-specific chromatin accessibility and gene expression changes in the hippocampus

Abstract Exposure to novel environments (NE) induces structural and functional changes in multiple brain areas, including the hippocampus, driven in part by changes in gene expression. However, the cell-type-specific transcriptional and chromatin responses to NE remain poorly understood. We employed...

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Main Authors: Lisa Traunmüller, Erin E. Duffy, Hanqing Liu, Stella Sanalidou, Sebastian Krüttner, Elena G. Assad, Senmiao Sun, Naeem S. Pajarillo, Nancy Niu, Eric C. Griffith, Michael E. Greenberg
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-63029-6
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author Lisa Traunmüller
Erin E. Duffy
Hanqing Liu
Stella Sanalidou
Sebastian Krüttner
Elena G. Assad
Senmiao Sun
Naeem S. Pajarillo
Nancy Niu
Eric C. Griffith
Michael E. Greenberg
author_facet Lisa Traunmüller
Erin E. Duffy
Hanqing Liu
Stella Sanalidou
Sebastian Krüttner
Elena G. Assad
Senmiao Sun
Naeem S. Pajarillo
Nancy Niu
Eric C. Griffith
Michael E. Greenberg
author_sort Lisa Traunmüller
collection DOAJ
description Abstract Exposure to novel environments (NE) induces structural and functional changes in multiple brain areas, including the hippocampus, driven in part by changes in gene expression. However, the cell-type-specific transcriptional and chromatin responses to NE remain poorly understood. We employed single-nucleus multiomics and bulk RNA-seq of the hippocampal DG, CA3, and CA1 regions of male mice to profile gene expression and chromatin accessibility following NE exposure. We observed region-specific responses in excitatory neurons and diverse transcriptional changes in inhibitory and non-neuronal cells. NE-regulated genes were enriched for secreted factors, and their cell-type-specific receptor expression highlighted candidate signaling pathways involved in learning and memory. We identified thousands of cell-type-specific chromatin accessibility changes, with coordinated expression and accessibility patterns implicating FOS/AP-1 as a key regulator. These data provide a rich resource of chromatin accessibility and gene expression profiles across hippocampal cell types in response to NE, a physiological stimulus affecting learning and memory.
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issn 2041-1723
language English
publishDate 2025-08-01
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series Nature Communications
spelling doaj-art-4ec2880dd66c4037b759d8fd73a72ed02025-08-24T11:39:37ZengNature PortfolioNature Communications2041-17232025-08-0116111710.1038/s41467-025-63029-6Novel environment exposure drives temporally defined and region-specific chromatin accessibility and gene expression changes in the hippocampusLisa Traunmüller0Erin E. Duffy1Hanqing Liu2Stella Sanalidou3Sebastian Krüttner4Elena G. Assad5Senmiao Sun6Naeem S. Pajarillo7Nancy Niu8Eric C. Griffith9Michael E. Greenberg10Department of Neurobiology, Harvard Medical SchoolDepartment of Neurobiology, Harvard Medical SchoolDepartment of Neurobiology, Harvard Medical SchoolDepartment of Neurobiology, Harvard Medical SchoolDepartment of Neurobiology, Harvard Medical SchoolDepartment of Neurobiology, Harvard Medical SchoolDepartment of Neurobiology, Harvard Medical SchoolDepartment of Neurobiology, Harvard Medical SchoolDepartment of Neurobiology, Harvard Medical SchoolDepartment of Neurobiology, Harvard Medical SchoolDepartment of Neurobiology, Harvard Medical SchoolAbstract Exposure to novel environments (NE) induces structural and functional changes in multiple brain areas, including the hippocampus, driven in part by changes in gene expression. However, the cell-type-specific transcriptional and chromatin responses to NE remain poorly understood. We employed single-nucleus multiomics and bulk RNA-seq of the hippocampal DG, CA3, and CA1 regions of male mice to profile gene expression and chromatin accessibility following NE exposure. We observed region-specific responses in excitatory neurons and diverse transcriptional changes in inhibitory and non-neuronal cells. NE-regulated genes were enriched for secreted factors, and their cell-type-specific receptor expression highlighted candidate signaling pathways involved in learning and memory. We identified thousands of cell-type-specific chromatin accessibility changes, with coordinated expression and accessibility patterns implicating FOS/AP-1 as a key regulator. These data provide a rich resource of chromatin accessibility and gene expression profiles across hippocampal cell types in response to NE, a physiological stimulus affecting learning and memory.https://doi.org/10.1038/s41467-025-63029-6
spellingShingle Lisa Traunmüller
Erin E. Duffy
Hanqing Liu
Stella Sanalidou
Sebastian Krüttner
Elena G. Assad
Senmiao Sun
Naeem S. Pajarillo
Nancy Niu
Eric C. Griffith
Michael E. Greenberg
Novel environment exposure drives temporally defined and region-specific chromatin accessibility and gene expression changes in the hippocampus
Nature Communications
title Novel environment exposure drives temporally defined and region-specific chromatin accessibility and gene expression changes in the hippocampus
title_full Novel environment exposure drives temporally defined and region-specific chromatin accessibility and gene expression changes in the hippocampus
title_fullStr Novel environment exposure drives temporally defined and region-specific chromatin accessibility and gene expression changes in the hippocampus
title_full_unstemmed Novel environment exposure drives temporally defined and region-specific chromatin accessibility and gene expression changes in the hippocampus
title_short Novel environment exposure drives temporally defined and region-specific chromatin accessibility and gene expression changes in the hippocampus
title_sort novel environment exposure drives temporally defined and region specific chromatin accessibility and gene expression changes in the hippocampus
url https://doi.org/10.1038/s41467-025-63029-6
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