The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males

Abstract

BackgroundInadequate sleep is associated with many detrimental health effects, including increased risk of developing insulin resistance and type 2 diabetes. These effects have been associated with changes to the skeletal muscle transcriptome, although this has not been characterised in response to a period of sleep restriction. Exercise induces a beneficial transcriptional response within skeletal muscle that may counteract some of the negative effects associated with sleep restriction. We hypothesised that sleep restriction would down-regulate transcriptional pathways associated with glucose metabolism, but that performing exercise would mitigate these effects.Methods20 healthy young males were allocated to one of three experimental groups: a Normal Sleep (NS) group (8 h time in bed per night (TIB), for five nights (11 pm – 7 am)), a Sleep Restriction (SR) group (4 h TIB, for five nights (3 am – 7 am)), and a Sleep Restriction and Exercise group (SR+EX) (4 h TIB, for five nights (3 am – 7 am) and three high-intensity interval exercise (HIIE) sessions (performed at 10 am)). RNA sequencing was performed on muscle samples collected pre- and post-intervention. Our data was then compared to skeletal muscle transcriptomic data previously reported following sleep deprivation (24 h without sleep).ResultsGene set enrichment analysis (GSEA) indicated there was an increased enrichment of inflammatory and immune response related pathways in the SR group post-intervention. However, in the SR+EX group the direction of enrichment in these same pathways occurred in the opposite directions. Despite this, there were no significant changes at the individual gene level from pre- to post-intervention. A set of genes previously shown to be decreased with sleep deprivation was also decreased in the SR group, but increased in the SR+EX group.ConclusionThe alterations to inflammatory and immune related pathways in skeletal muscle, following five nights of sleep restriction, provide insight regarding the transcriptional changes that underpin the detrimental effects associated with sleep loss. Performing three sessions of HIIE during sleep restriction attenuated some of these transcriptional changes. Overall, the transcriptional alterations observed with a moderate period of sleep restriction were less evident than previously reported changes following a period of sleep deprivation.

The interactive effect of sustained sleep restriction and resistance exercise on skeletal muscle transcriptomics in young females

“…Despite the lack of differentially regulated individual transcripts, there are many similarities between the enriched transcriptional pathways reported in our study and the previous studies that have examined the skeletal muscle transcriptome responses to either one or five nights of sleep loss. Pathways associated with protein translation and oxidative metabolism were similarly down-regulated after one night of sleep deprivation (41) or five nights of sleep restriction (11) and support translational findings that skeletal muscle protein synthesis (6, 7) and mitochondrial respiratory function (44) are negatively influenced by sleep restriction. While there are large differences in the number of DEGs between acute sleep deprivation (i.e., 24 h wakefulness) and chronic sleep restriction (i.e., less than 7 h time in bed) studies (11,41), there are similar enrichment profiles of transcriptional pathways, suggesting that the magnitude of change may be influenced by the length and severity of the sleep intervention.…”

“…Some authors (10) but not others (6) have reported changes in the expression of circadian clock genes with inadequate sleep. At the muscle transcriptome level, 24 h sleep deprivation (10) but not five repeated nights of sleep restriction (4 h sleep per night) (11), alter the expression of individual genes associated with the regulation of circadian clock and protein metabolism pathways in males.…”

The effects of sleep disruption on metabolism, hunger, and satiety, and the influence of psychosocial stress and exercise: A narrative review

“…restriction, but exercise counteracted this pattern of gene set enrichment. 166 It should be noted that the degree of enrichment was much smaller than in prior studies that used total sleep deprivation, suggesting that moderate sleep restriction is not as detrimental as total sleep deprivation. It should also be noted that these findings were observed alongside reduced skeletal muscle mitochondrial function and impaired glucose tolerance following sleep restriction that were also counteracted by exercise.…”

The effect of sleep restriction, with or without high‐intensity interval exercise, on behavioural alertness and mood state in young healthy males

“…Participants were assigned to either normal sleep (NS, n = 8), sleep restriction (SR, n = 8), or sleep restriction and exercise (SR + EX, n = 8). Physiological data from this cohort of participants (including data relating to glucose tolerance and skeletal muscle analysis) has been previously reported elsewhere (Lin et al, 2022; Saner et al, 2021; Saner & Lee, 2020).…”

“…Indeed, acute aerobic exercise has been reported to improve mood (assessed via POMS) for up to 24 h upon completion (Maroulakis & Zervas, 1993; Reed & Ones, 2006) and exercise training can improve mood, alleviate depressive symptoms, and increase cognitive performance (including alertness and vigilance) (Carta et al, 2021; Monleon et al, 2015; Sibold & Berg, 2010). Previous work, including from our own group, has shown that performing high‐intensity interval exercise (HIIE) can mitigate the detrimental metabolic effects associated with a period of sleep restriction (de Souza et al, 2017; Lin et al, 2022; Saner et al, 2020; Saner et al, 2021; Sweeney et al, 2020). Despite this, research investigating the potential benefits of performing exercise to counteract the effects of sleep loss on mood and alertness are currently limited.…”