How sleep and wakefulness influence circadian rhythmicity: effects of insufficient and mistimed sleep on the animal and human transcriptome

Jun 11, 2015Journal of sleep research

How Sleep and Wake Timing Affect Daily Body Clocks: Impact of Poor and Misaligned Sleep on Gene Activity in Animals and Humans

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Abstract

In mice, sleep restriction leads to an ~80% reduction in circadian transcripts in the brain.

Disruption of sleep patterns is associated with adverse health outcomes, though mechanisms remain unclear.
In humans, sleep restriction results in a 1.9% reduction in circadian transcripts in whole blood.
Daytime sleep displacement causes 97% of rhythmic genes to lose their rhythm, affecting temporal expression profiles.
Despite changes in peripheral tissues, the suprachiasmatic nucleus's internal rhythms remain intact.
Potential physiological mediators of sleep disruption effects may include altered food intake and hormonal changes.

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The mammalian circadian system is a multi-oscillator, hierarchically organised system where a central pacemaker synchronises behavioural, physiological and gene expression rhythms in peripheral tissues. Epidemiological studies show that disruption of this internal synchronisation by short sleep and shift work is associated with adverse health outcomes through mechanisms that remain to be elucidated. Here, we review recent animal and human studies demonstrating the profound effects of insufficient and mistimed sleep on the rhythms of gene expression in central and peripheral tissues. In mice, sleep restriction leads to an ~80% reduction in circadian transcripts in the brain and profound disruption of the liver transcriptome. In humans, sleep restriction leads to a 1.9% reduction in circadian transcripts in whole blood, and when sleep is displaced to the daytime, 97% of rhythmic genes become arrhythmic and one-third of all genes show changes in temporal expression profiles. These changes in mice and humans include a significant reduction in the circadian regulation of transcription and translation and core clock genes in the periphery, while at the same time rhythms within the suprachiasmatic nucleus are not disrupted. Although the physiological mediators of these sleep disruption effects on the transcriptome have not been established, altered food intake, changes in hormones such as cortisol, and changes in body and brain temperature may play important roles. Processes and molecular pathways associated with these disruptions include metabolism, immune function, inflammatory and stress responses, and point to the molecular mechanisms underlying the established adverse health outcomes associated with short sleep duration and shift work, such as metabolic syndrome and cancer.

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How sleep and wakefulness influence circadian rhythmicity: effects of insufficient and mistimed sleep on the animal and human transcriptome

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