Sleep-wake-driven and circadian contributions to daily rhythms in gene expression and chromatin accessibility in the murine cortex.

Details

Serval ID
serval:BIB_6D830863EABB
Type
Article: article from journal or magazin.
Collection
Publications
Title
Sleep-wake-driven and circadian contributions to daily rhythms in gene expression and chromatin accessibility in the murine cortex.
Journal
Proceedings of the National Academy of Sciences of the United States of America
Author(s)
Hor C.N., Yeung J., Jan M., Emmenegger Y., Hubbard J., Xenarios I., Naef F., Franken P.
ISSN
1091-6490 (Electronic)
ISSN-L
0027-8424
Publication state
Published
Issued date
17/12/2019
Peer-reviewed
Oui
Volume
116
Number
51
Pages
25773-25783
Language
english
Notes
Publication types: Journal Article ; Research Support, Non-U.S. Gov't
Publication Status: ppublish
Abstract
The timing and duration of sleep results from the interaction between a homeostatic sleep-wake-driven process and a periodic circadian process, and involves changes in gene regulation and expression. Unraveling the contributions of both processes and their interaction to transcriptional and epigenomic regulatory dynamics requires sampling over time under conditions of unperturbed and perturbed sleep. We profiled mRNA expression and chromatin accessibility in the cerebral cortex of mice over a 3-d period, including a 6-h sleep deprivation (SD) on day 2. We used mathematical modeling to integrate time series of mRNA expression data with sleep-wake history, which established that a large proportion of rhythmic genes are governed by the homeostatic process with varying degrees of interaction with the circadian process, sometimes working in opposition. Remarkably, SD caused long-term effects on gene-expression dynamics, outlasting phenotypic recovery, most strikingly illustrated by a damped oscillation of most core clock genes, including Arntl/Bmal1, suggesting that enforced wakefulness directly impacts the molecular clock machinery. Chromatin accessibility proved highly plastic and dynamically affected by SD. Dynamics in distal regions, rather than promoters, correlated with mRNA expression, implying that changes in expression result from constitutively accessible promoters under the influence of enhancers or repressors. Serum response factor (SRF) was predicted as a transcriptional regulator driving immediate response, suggesting that SRF activity mirrors the build-up and release of sleep pressure. Our results demonstrate that a single, short SD has long-term aftereffects at the genomic regulatory level and highlights the importance of the sleep-wake distribution to diurnal rhythmicity and circadian processes.
Keywords
Animals, Cerebral Cortex/metabolism, Chromatin/genetics, Circadian Rhythm/genetics, Epigenomics, Gene Expression/genetics, Male, Mice, Mice, Inbred C57BL, Serum Response Factor/metabolism, Sleep/genetics, Sleep Deprivation/genetics, Wakefulness/genetics, circadian, epigenetics, gene expression, long-term effects, sleep
Pubmed
Web of science
Open Access
Yes
Create date
05/12/2019 23:15
Last modification date
27/04/2020 6:20
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