Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues
Autor(a) principal: | |
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Data de Publicação: | 2013 |
Outros Autores: | , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Institucional da UNIFESP |
Texto Completo: | http://repositorio.unifesp.br/handle/11600/36352 http://dx.doi.org/10.1186/1471-2164-14-362 |
Resumo: | Background: Many have assumed that the primary function of sleep is for the brain. We evaluated the molecular consequences of sleep and sleep deprivation outside the brain, in heart and lung. Using microarrays we compared gene expression in tissue from sleeping and sleep deprived mice euthanized at the same diurnal times.Results: in each tissue, nearly two thousand genes demonstrated statistically significant differential expression as a function of sleep/wake behavioral state. To mitigate the influence of an artificial deprivation protocol, we identified a subset of these transcripts as specifically sleep-enhanced or sleep-repressed by requiring that their expression also change over the course of unperturbed sleep. 3% and 6% of the assayed transcripts showed sleep specific changes in the lung and heart respectively. Sleep specific transcripts in these tissues demonstrated highly significant overlap and shared temporal dynamics. Markers of cellular stress and the unfolded protein response were reduced during sleep in both tissues. These results mirror previous findings in brain. Sleep-enhanced pathways reflected the unique metabolic functions of each tissue. Transcripts related to carbohydrate and sulfur metabolic processes were enhanced by sleep in the lung, and collectively favor buffering from oxidative stress. DNA repair and protein metabolism annotations were significantly enriched among the sleep-enhanced transcripts in the heart. Our results also suggest that sleep may provide a Zeitgeber, or synchronizing cue, in the lung as a large cluster of transcripts demonstrated systematic changes in inter-animal variability as a function of both sleep duration and circadian time.Conclusion: Our data support the notion that the molecular consequences of sleep/wake behavioral state extend beyond the brain to include peripheral tissues. Sleep state induces a highly overlapping response in both heart and lung. We conclude that sleep enhances organ specific molecular functions and that it has a ubiquitous role in reducing cellular metabolic stress in both brain and peripheral tissues. Finally, our data suggest a novel role for sleep in synchronizing transcription in peripheral tissues. |
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Anafi, Ron C.Pellegrino, Renata [UNIFESP]Shockley, Keith R.Romer, MicahTufik, Sergio [UNIFESP]Pack, Allan I.Univ PennChildrens Hosp PhiladelphiaUniversidade Federal de São Paulo (UNIFESP)NIEHS2016-01-24T14:31:47Z2016-01-24T14:31:47Z2013-05-30Bmc Genomics. London: Biomed Central Ltd, v. 14, 19 p., 2013.1471-2164http://repositorio.unifesp.br/handle/11600/36352http://dx.doi.org/10.1186/1471-2164-14-362WOS000321386100002.pdf10.1186/1471-2164-14-362WOS:000321386100002Background: Many have assumed that the primary function of sleep is for the brain. We evaluated the molecular consequences of sleep and sleep deprivation outside the brain, in heart and lung. Using microarrays we compared gene expression in tissue from sleeping and sleep deprived mice euthanized at the same diurnal times.Results: in each tissue, nearly two thousand genes demonstrated statistically significant differential expression as a function of sleep/wake behavioral state. To mitigate the influence of an artificial deprivation protocol, we identified a subset of these transcripts as specifically sleep-enhanced or sleep-repressed by requiring that their expression also change over the course of unperturbed sleep. 3% and 6% of the assayed transcripts showed sleep specific changes in the lung and heart respectively. Sleep specific transcripts in these tissues demonstrated highly significant overlap and shared temporal dynamics. Markers of cellular stress and the unfolded protein response were reduced during sleep in both tissues. These results mirror previous findings in brain. Sleep-enhanced pathways reflected the unique metabolic functions of each tissue. Transcripts related to carbohydrate and sulfur metabolic processes were enhanced by sleep in the lung, and collectively favor buffering from oxidative stress. DNA repair and protein metabolism annotations were significantly enriched among the sleep-enhanced transcripts in the heart. Our results also suggest that sleep may provide a Zeitgeber, or synchronizing cue, in the lung as a large cluster of transcripts demonstrated systematic changes in inter-animal variability as a function of both sleep duration and circadian time.Conclusion: Our data support the notion that the molecular consequences of sleep/wake behavioral state extend beyond the brain to include peripheral tissues. Sleep state induces a highly overlapping response in both heart and lung. We conclude that sleep enhances organ specific molecular functions and that it has a ubiquitous role in reducing cellular metabolic stress in both brain and peripheral tissues. Finally, our data suggest a novel role for sleep in synchronizing transcription in peripheral tissues.Intramural Research Program of the National Institutes of Health, National Institute of Environmental Health SciencesNational Institutes of HealthAmerican Sleep Medicine FoundationNational Heart Lung Blood InstituteUniv Penn, Perelman Sch Med, Div Sleep Med, Philadelphia, PA 19104 USAUniv Penn, Perelman Sch Med, Ctr Sleep & Circadian Neurobiol, Philadelphia, PA 19104 USAChildrens Hosp Philadelphia, Ctr Appl Genom, Philadelphia, PA 19104 USAUniversidade Federal de São Paulo UNIFESP, São Paulo, BrazilNIEHS, US Dept HHS, Biostat Branch, NIH, Res Triangle Pk, NC 27709 USAUniversidade Federal de São Paulo UNIFESP, EPM, São Paulo, BrazilNational Institutes of Health: AG-17628National Heart Lung Blood Institute: HL090021: K12Web of Science19engBiomed Central LtdBmc GenomicsSleepCircadian RhythmsSleep DeprivationUnfolded Protein ResponseHeartLungSynchronizationSleep is not just for the brain: transcriptional responses to sleep in peripheral tissuesinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UNIFESPinstname:Universidade Federal de São Paulo (UNIFESP)instacron:UNIFESPORIGINALWOS000321386100002.pdfapplication/pdf1330027${dspace.ui.url}/bitstream/11600/36352/1/WOS000321386100002.pdfcc75cc02c1a70126c2ad3bf9c0565bfeMD51open accessTEXTWOS000321386100002.pdf.txtWOS000321386100002.pdf.txtExtracted texttext/plain88407${dspace.ui.url}/bitstream/11600/36352/2/WOS000321386100002.pdf.txtf98f2a5f9268bb4a623ec59f4ae9e463MD52open access11600/363522022-06-02 09:06:00.004open accessoai:repositorio.unifesp.br:11600/36352Repositório InstitucionalPUBhttp://www.repositorio.unifesp.br/oai/requestopendoar:34652022-06-02T12:06Repositório Institucional da UNIFESP - Universidade Federal de São Paulo (UNIFESP)false |
dc.title.en.fl_str_mv |
Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues |
title |
Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues |
spellingShingle |
Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues Anafi, Ron C. Sleep Circadian Rhythms Sleep Deprivation Unfolded Protein Response Heart Lung Synchronization |
title_short |
Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues |
title_full |
Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues |
title_fullStr |
Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues |
title_full_unstemmed |
Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues |
title_sort |
Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues |
author |
Anafi, Ron C. |
author_facet |
Anafi, Ron C. Pellegrino, Renata [UNIFESP] Shockley, Keith R. Romer, Micah Tufik, Sergio [UNIFESP] Pack, Allan I. |
author_role |
author |
author2 |
Pellegrino, Renata [UNIFESP] Shockley, Keith R. Romer, Micah Tufik, Sergio [UNIFESP] Pack, Allan I. |
author2_role |
author author author author author |
dc.contributor.institution.none.fl_str_mv |
Univ Penn Childrens Hosp Philadelphia Universidade Federal de São Paulo (UNIFESP) NIEHS |
dc.contributor.author.fl_str_mv |
Anafi, Ron C. Pellegrino, Renata [UNIFESP] Shockley, Keith R. Romer, Micah Tufik, Sergio [UNIFESP] Pack, Allan I. |
dc.subject.eng.fl_str_mv |
Sleep Circadian Rhythms Sleep Deprivation Unfolded Protein Response Heart Lung Synchronization |
topic |
Sleep Circadian Rhythms Sleep Deprivation Unfolded Protein Response Heart Lung Synchronization |
description |
Background: Many have assumed that the primary function of sleep is for the brain. We evaluated the molecular consequences of sleep and sleep deprivation outside the brain, in heart and lung. Using microarrays we compared gene expression in tissue from sleeping and sleep deprived mice euthanized at the same diurnal times.Results: in each tissue, nearly two thousand genes demonstrated statistically significant differential expression as a function of sleep/wake behavioral state. To mitigate the influence of an artificial deprivation protocol, we identified a subset of these transcripts as specifically sleep-enhanced or sleep-repressed by requiring that their expression also change over the course of unperturbed sleep. 3% and 6% of the assayed transcripts showed sleep specific changes in the lung and heart respectively. Sleep specific transcripts in these tissues demonstrated highly significant overlap and shared temporal dynamics. Markers of cellular stress and the unfolded protein response were reduced during sleep in both tissues. These results mirror previous findings in brain. Sleep-enhanced pathways reflected the unique metabolic functions of each tissue. Transcripts related to carbohydrate and sulfur metabolic processes were enhanced by sleep in the lung, and collectively favor buffering from oxidative stress. DNA repair and protein metabolism annotations were significantly enriched among the sleep-enhanced transcripts in the heart. Our results also suggest that sleep may provide a Zeitgeber, or synchronizing cue, in the lung as a large cluster of transcripts demonstrated systematic changes in inter-animal variability as a function of both sleep duration and circadian time.Conclusion: Our data support the notion that the molecular consequences of sleep/wake behavioral state extend beyond the brain to include peripheral tissues. Sleep state induces a highly overlapping response in both heart and lung. We conclude that sleep enhances organ specific molecular functions and that it has a ubiquitous role in reducing cellular metabolic stress in both brain and peripheral tissues. Finally, our data suggest a novel role for sleep in synchronizing transcription in peripheral tissues. |
publishDate |
2013 |
dc.date.issued.fl_str_mv |
2013-05-30 |
dc.date.accessioned.fl_str_mv |
2016-01-24T14:31:47Z |
dc.date.available.fl_str_mv |
2016-01-24T14:31:47Z |
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info:eu-repo/semantics/article |
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article |
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dc.identifier.citation.fl_str_mv |
Bmc Genomics. London: Biomed Central Ltd, v. 14, 19 p., 2013. |
dc.identifier.uri.fl_str_mv |
http://repositorio.unifesp.br/handle/11600/36352 http://dx.doi.org/10.1186/1471-2164-14-362 |
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1471-2164 |
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WOS000321386100002.pdf |
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10.1186/1471-2164-14-362 |
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Bmc Genomics. London: Biomed Central Ltd, v. 14, 19 p., 2013. 1471-2164 WOS000321386100002.pdf 10.1186/1471-2164-14-362 WOS:000321386100002 |
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http://repositorio.unifesp.br/handle/11600/36352 http://dx.doi.org/10.1186/1471-2164-14-362 |
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Biomed Central Ltd |
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