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Altered hippocampal transcriptome dynamics following sleep deprivation

Widespread sleep deprivation is a continuing public health problem in the United States and worldwide affecting adolescents and adults. Acute sleep deprivation results in decrements in spatial memory and cognitive impairments. The hippocampus is vulnerable to acute sleep deprivation with changes in...

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Autores principales: Gaine, Marie E., Bahl, Ethan, Chatterjee, Snehajyoti, Michaelson, Jacob J., Abel, Ted, Lyons, Lisa C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8361790/
https://www.ncbi.nlm.nih.gov/pubmed/34384474
http://dx.doi.org/10.1186/s13041-021-00835-1
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author Gaine, Marie E.
Bahl, Ethan
Chatterjee, Snehajyoti
Michaelson, Jacob J.
Abel, Ted
Lyons, Lisa C.
author_facet Gaine, Marie E.
Bahl, Ethan
Chatterjee, Snehajyoti
Michaelson, Jacob J.
Abel, Ted
Lyons, Lisa C.
author_sort Gaine, Marie E.
collection PubMed
description Widespread sleep deprivation is a continuing public health problem in the United States and worldwide affecting adolescents and adults. Acute sleep deprivation results in decrements in spatial memory and cognitive impairments. The hippocampus is vulnerable to acute sleep deprivation with changes in gene expression, cell signaling, and protein synthesis. Sleep deprivation also has long lasting effects on memory and performance that persist after recovery sleep, as seen in behavioral studies from invertebrates to humans. Although previous research has shown that acute sleep deprivation impacts gene expression, the extent to which sleep deprivation affects gene regulation remains unknown. Using an unbiased deep RNA sequencing approach, we investigated the effects of acute sleep deprivation on gene expression in the hippocampus. We identified 1,146 genes that were significantly dysregulated following sleep deprivation with 507 genes upregulated and 639 genes downregulated, including protein coding genes and long non-coding RNAs not previously identified as impacted by sleep deprivation. Notably, genes significantly upregulated after sleep deprivation were associated with RNA splicing and the nucleus. In contrast, downregulated genes were associated with cell adhesion, dendritic localization, the synapse, and postsynaptic membrane. Furthermore, we found through independent experiments analyzing a subset of genes that three hours of recovery sleep following acute sleep deprivation was sufficient to normalize mRNA abundance for most genes, although exceptions occurred for some genes that may affect RNA splicing or transcription. These results clearly demonstrate that sleep deprivation differentially regulates gene expression on multiple transcriptomic levels to impact hippocampal function. [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13041-021-00835-1.
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spelling pubmed-83617902021-08-17 Altered hippocampal transcriptome dynamics following sleep deprivation Gaine, Marie E. Bahl, Ethan Chatterjee, Snehajyoti Michaelson, Jacob J. Abel, Ted Lyons, Lisa C. Mol Brain Research Widespread sleep deprivation is a continuing public health problem in the United States and worldwide affecting adolescents and adults. Acute sleep deprivation results in decrements in spatial memory and cognitive impairments. The hippocampus is vulnerable to acute sleep deprivation with changes in gene expression, cell signaling, and protein synthesis. Sleep deprivation also has long lasting effects on memory and performance that persist after recovery sleep, as seen in behavioral studies from invertebrates to humans. Although previous research has shown that acute sleep deprivation impacts gene expression, the extent to which sleep deprivation affects gene regulation remains unknown. Using an unbiased deep RNA sequencing approach, we investigated the effects of acute sleep deprivation on gene expression in the hippocampus. We identified 1,146 genes that were significantly dysregulated following sleep deprivation with 507 genes upregulated and 639 genes downregulated, including protein coding genes and long non-coding RNAs not previously identified as impacted by sleep deprivation. Notably, genes significantly upregulated after sleep deprivation were associated with RNA splicing and the nucleus. In contrast, downregulated genes were associated with cell adhesion, dendritic localization, the synapse, and postsynaptic membrane. Furthermore, we found through independent experiments analyzing a subset of genes that three hours of recovery sleep following acute sleep deprivation was sufficient to normalize mRNA abundance for most genes, although exceptions occurred for some genes that may affect RNA splicing or transcription. These results clearly demonstrate that sleep deprivation differentially regulates gene expression on multiple transcriptomic levels to impact hippocampal function. [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13041-021-00835-1. BioMed Central 2021-08-12 /pmc/articles/PMC8361790/ /pubmed/34384474 http://dx.doi.org/10.1186/s13041-021-00835-1 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Gaine, Marie E.
Bahl, Ethan
Chatterjee, Snehajyoti
Michaelson, Jacob J.
Abel, Ted
Lyons, Lisa C.
Altered hippocampal transcriptome dynamics following sleep deprivation
title Altered hippocampal transcriptome dynamics following sleep deprivation
title_full Altered hippocampal transcriptome dynamics following sleep deprivation
title_fullStr Altered hippocampal transcriptome dynamics following sleep deprivation
title_full_unstemmed Altered hippocampal transcriptome dynamics following sleep deprivation
title_short Altered hippocampal transcriptome dynamics following sleep deprivation
title_sort altered hippocampal transcriptome dynamics following sleep deprivation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8361790/
https://www.ncbi.nlm.nih.gov/pubmed/34384474
http://dx.doi.org/10.1186/s13041-021-00835-1
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