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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...

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Autores principales: 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.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2022
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.
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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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