Abstract
Sleep is essential to all animals with a nervous system. Nevertheless, the core cellular function of sleep is unknown, and there is no conserved molecular marker to define sleep across phylogeny. Time-lapse imaging of chromosomal markers in single cells of live zebrafish revealed that sleep increases chromosome dynamics in individual neurons but not in two other cell types. Manipulation of sleep, chromosome dynamics, neuronal activity, and DNA double-strand breaks (DSBs) showed that chromosome dynamics are low and the number of DSBs accumulates during wakefulness. In turn, sleep increases chromosome dynamics, which are necessary to reduce the amount of DSBs. These results establish chromosome dynamics as a potential marker to define single sleeping cells, and propose that the restorative function of sleep is nuclear maintenance.
Highlights
Sleep is essential to all animals with a nervous system
double-strand breaks (DSBs) accumulate during wakefulness and sleep deprivation (SD), when chromosome dynamics are low
Imaging of spontaneous neuronal activity, single-cell optogenetic and pharmacological experiments indicated that DSB formation by neuronal activity and other factors, can reduce chromosome dynamics
Summary
The core cellular function of sleep is unknown, and there is no conserved molecular marker to define sleep across phylogeny. The nuclear architecture and the dynamic changes in chromatin organization regulate vital cellular processes, including epigenetics, genomic stability, transcription, cell cycle, and DNA replication and repair[23,24]. Chromatin dynamics, such as chromosome movements and structural genomic arrangements, are regulated by proteins that interact with the nuclear lamina and envelope in dividing cells[25,26,27]. Activity-induced DSBs facilitate the expression of immediate early genes in mouse and cell cultures, possibly because they resolve topological constraints in the genome[35]
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