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

BACKGROUND: Inadequate 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 t...

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Autores principales: Lin, Wentao, Saner, Nicholas J., Weng, Xiquan, Caruana, Nikeisha J., Botella, Javier, Kuang, Jujiao, Lee, Matthew J-C., Jamnick, Nicholas A., Pitchford, Nathan W., Garnham, Andrew, Bartlett, Jonathan D., Chen, Hao, Bishop, David J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9355502/
https://www.ncbi.nlm.nih.gov/pubmed/35937838
http://dx.doi.org/10.3389/fendo.2022.863224
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author Lin, Wentao
Saner, Nicholas J.
Weng, Xiquan
Caruana, Nikeisha J.
Botella, Javier
Kuang, Jujiao
Lee, Matthew J-C.
Jamnick, Nicholas A.
Pitchford, Nathan W.
Garnham, Andrew
Bartlett, Jonathan D.
Chen, Hao
Bishop, David J.
author_facet Lin, Wentao
Saner, Nicholas J.
Weng, Xiquan
Caruana, Nikeisha J.
Botella, Javier
Kuang, Jujiao
Lee, Matthew J-C.
Jamnick, Nicholas A.
Pitchford, Nathan W.
Garnham, Andrew
Bartlett, Jonathan D.
Chen, Hao
Bishop, David J.
author_sort Lin, Wentao
collection PubMed
description BACKGROUND: Inadequate 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. METHODS: 20 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). RESULTS: Gene 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. CONCLUSION: The 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.
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spelling pubmed-93555022022-08-06 The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males Lin, Wentao Saner, Nicholas J. Weng, Xiquan Caruana, Nikeisha J. Botella, Javier Kuang, Jujiao Lee, Matthew J-C. Jamnick, Nicholas A. Pitchford, Nathan W. Garnham, Andrew Bartlett, Jonathan D. Chen, Hao Bishop, David J. Front Endocrinol (Lausanne) Endocrinology BACKGROUND: Inadequate 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. METHODS: 20 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). RESULTS: Gene 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. CONCLUSION: The 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. Frontiers Media S.A. 2022-07-22 /pmc/articles/PMC9355502/ /pubmed/35937838 http://dx.doi.org/10.3389/fendo.2022.863224 Text en Copyright © 2022 Lin, Saner, Weng, Caruana, Botella, Kuang, Lee, Jamnick, Pitchford, Garnham, Bartlett, Chen and Bishop https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Endocrinology
Lin, Wentao
Saner, Nicholas J.
Weng, Xiquan
Caruana, Nikeisha J.
Botella, Javier
Kuang, Jujiao
Lee, Matthew J-C.
Jamnick, Nicholas A.
Pitchford, Nathan W.
Garnham, Andrew
Bartlett, Jonathan D.
Chen, Hao
Bishop, David J.
The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males
title The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males
title_full The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males
title_fullStr The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males
title_full_unstemmed The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males
title_short The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males
title_sort effect of sleep restriction, with or without exercise, on skeletal muscle transcriptomic profiles in healthy young males
topic Endocrinology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9355502/
https://www.ncbi.nlm.nih.gov/pubmed/35937838
http://dx.doi.org/10.3389/fendo.2022.863224
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