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Sleep exerts lasting effects on hematopoietic stem cell function and diversity
A sleepless night may feel awful in its aftermath, but sleep’s revitalizing powers are substantial, perpetuating the idea that convalescent sleep is a consequence-free physiological reset. Although recent studies have shown that catch-up sleep insufficiently neutralizes the negative effects of sleep...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Rockefeller University Press
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9499822/ https://www.ncbi.nlm.nih.gov/pubmed/36129517 http://dx.doi.org/10.1084/jem.20220081 |
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author | McAlpine, Cameron S. Kiss, Máté G. Zuraikat, Faris M. Cheek, David Schiroli, Giulia Amatullah, Hajera Huynh, Pacific Bhatti, Mehreen Z. Wong, Lai-Ping Yates, Abi G. Poller, Wolfram C. Mindur, John E. Chan, Christopher T. Janssen, Henrike Downey, Jeffrey Singh, Sumnima Sadreyev, Ruslan I. Nahrendorf, Matthias Jeffrey, Kate L. Scadden, David T. Naxerova, Kamila St-Onge, Marie-Pierre Swirski, Filip K. |
author_facet | McAlpine, Cameron S. Kiss, Máté G. Zuraikat, Faris M. Cheek, David Schiroli, Giulia Amatullah, Hajera Huynh, Pacific Bhatti, Mehreen Z. Wong, Lai-Ping Yates, Abi G. Poller, Wolfram C. Mindur, John E. Chan, Christopher T. Janssen, Henrike Downey, Jeffrey Singh, Sumnima Sadreyev, Ruslan I. Nahrendorf, Matthias Jeffrey, Kate L. Scadden, David T. Naxerova, Kamila St-Onge, Marie-Pierre Swirski, Filip K. |
author_sort | McAlpine, Cameron S. |
collection | PubMed |
description | A sleepless night may feel awful in its aftermath, but sleep’s revitalizing powers are substantial, perpetuating the idea that convalescent sleep is a consequence-free physiological reset. Although recent studies have shown that catch-up sleep insufficiently neutralizes the negative effects of sleep debt, the mechanisms that control prolonged effects of sleep disruption are not understood. Here, we show that sleep interruption restructures the epigenome of hematopoietic stem and progenitor cells (HSPCs) and increases their proliferation, thus reducing hematopoietic clonal diversity through accelerated genetic drift. Sleep fragmentation exerts a lasting influence on the HSPC epigenome, skewing commitment toward a myeloid fate and priming cells for exaggerated inflammatory bursts. Combining hematopoietic clonal tracking with mathematical modeling, we infer that sleep preserves clonal diversity by limiting neutral drift. In humans, sleep restriction alters the HSPC epigenome and activates hematopoiesis. These findings show that sleep slows decay of the hematopoietic system by calibrating the hematopoietic epigenome, constraining inflammatory output, and maintaining clonal diversity. |
format | Online Article Text |
id | pubmed-9499822 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Rockefeller University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-94998222023-03-21 Sleep exerts lasting effects on hematopoietic stem cell function and diversity McAlpine, Cameron S. Kiss, Máté G. Zuraikat, Faris M. Cheek, David Schiroli, Giulia Amatullah, Hajera Huynh, Pacific Bhatti, Mehreen Z. Wong, Lai-Ping Yates, Abi G. Poller, Wolfram C. Mindur, John E. Chan, Christopher T. Janssen, Henrike Downey, Jeffrey Singh, Sumnima Sadreyev, Ruslan I. Nahrendorf, Matthias Jeffrey, Kate L. Scadden, David T. Naxerova, Kamila St-Onge, Marie-Pierre Swirski, Filip K. J Exp Med Article A sleepless night may feel awful in its aftermath, but sleep’s revitalizing powers are substantial, perpetuating the idea that convalescent sleep is a consequence-free physiological reset. Although recent studies have shown that catch-up sleep insufficiently neutralizes the negative effects of sleep debt, the mechanisms that control prolonged effects of sleep disruption are not understood. Here, we show that sleep interruption restructures the epigenome of hematopoietic stem and progenitor cells (HSPCs) and increases their proliferation, thus reducing hematopoietic clonal diversity through accelerated genetic drift. Sleep fragmentation exerts a lasting influence on the HSPC epigenome, skewing commitment toward a myeloid fate and priming cells for exaggerated inflammatory bursts. Combining hematopoietic clonal tracking with mathematical modeling, we infer that sleep preserves clonal diversity by limiting neutral drift. In humans, sleep restriction alters the HSPC epigenome and activates hematopoiesis. These findings show that sleep slows decay of the hematopoietic system by calibrating the hematopoietic epigenome, constraining inflammatory output, and maintaining clonal diversity. Rockefeller University Press 2022-09-21 /pmc/articles/PMC9499822/ /pubmed/36129517 http://dx.doi.org/10.1084/jem.20220081 Text en © 2022 McAlpine et al. https://creativecommons.org/licenses/by-nc-sa/4.0/http://www.rupress.org/terms/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/). |
spellingShingle | Article McAlpine, Cameron S. Kiss, Máté G. Zuraikat, Faris M. Cheek, David Schiroli, Giulia Amatullah, Hajera Huynh, Pacific Bhatti, Mehreen Z. Wong, Lai-Ping Yates, Abi G. Poller, Wolfram C. Mindur, John E. Chan, Christopher T. Janssen, Henrike Downey, Jeffrey Singh, Sumnima Sadreyev, Ruslan I. Nahrendorf, Matthias Jeffrey, Kate L. Scadden, David T. Naxerova, Kamila St-Onge, Marie-Pierre Swirski, Filip K. Sleep exerts lasting effects on hematopoietic stem cell function and diversity |
title | Sleep exerts lasting effects on hematopoietic stem cell function and diversity |
title_full | Sleep exerts lasting effects on hematopoietic stem cell function and diversity |
title_fullStr | Sleep exerts lasting effects on hematopoietic stem cell function and diversity |
title_full_unstemmed | Sleep exerts lasting effects on hematopoietic stem cell function and diversity |
title_short | Sleep exerts lasting effects on hematopoietic stem cell function and diversity |
title_sort | sleep exerts lasting effects on hematopoietic stem cell function and diversity |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9499822/ https://www.ncbi.nlm.nih.gov/pubmed/36129517 http://dx.doi.org/10.1084/jem.20220081 |
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