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Dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging

Dietary restriction (DR) improves health, delays tissue aging, and elongates survival in flies and worms. However, studies on laboratory mice and nonhuman primates revealed ambiguous effects of DR on lifespan despite improvements in health parameters. In this study, we analyzed consequences of adult...

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Autores principales: Tang, Duozhuang, Tao, Si, Chen, Zhiyang, Koliesnik, Ievgen Oleksandrovich, Calmes, Philip Gerald, Hoerr, Verena, Han, Bing, Gebert, Nadja, Zörnig, Martin, Löffler, Bettina, Morita, Yohei, Rudolph, Karl Lenhard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4821645/
https://www.ncbi.nlm.nih.gov/pubmed/26951333
http://dx.doi.org/10.1084/jem.20151100
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author Tang, Duozhuang
Tao, Si
Chen, Zhiyang
Koliesnik, Ievgen Oleksandrovich
Calmes, Philip Gerald
Hoerr, Verena
Han, Bing
Gebert, Nadja
Zörnig, Martin
Löffler, Bettina
Morita, Yohei
Rudolph, Karl Lenhard
author_facet Tang, Duozhuang
Tao, Si
Chen, Zhiyang
Koliesnik, Ievgen Oleksandrovich
Calmes, Philip Gerald
Hoerr, Verena
Han, Bing
Gebert, Nadja
Zörnig, Martin
Löffler, Bettina
Morita, Yohei
Rudolph, Karl Lenhard
author_sort Tang, Duozhuang
collection PubMed
description Dietary restriction (DR) improves health, delays tissue aging, and elongates survival in flies and worms. However, studies on laboratory mice and nonhuman primates revealed ambiguous effects of DR on lifespan despite improvements in health parameters. In this study, we analyzed consequences of adult-onset DR (24 h to 1 yr) on hematopoietic stem cell (HSC) function. DR ameliorated HSC aging phenotypes, such as the increase in number of HSCs and the skewing toward myeloid-biased HSCs during aging. Furthermore, DR increased HSC quiescence and improved the maintenance of the repopulation capacity of HSCs during aging. In contrast to these beneficial effects, DR strongly impaired HSC differentiation into lymphoid lineages and particularly inhibited the proliferation of lymphoid progenitors, resulting in decreased production of peripheral B lymphocytes and impaired immune function. The study shows that DR-dependent suppression of growth factors and interleukins mediates these divergent effects caused by DR. Supplementation of insulin-like growth factor 1 partially reverted the DR-induced quiescence of HSCs, whereas IL-6/IL-7 substitutions rescued the impairment of B lymphopoiesis exposed to DR. Together, these findings delineate positive and negative effects of long-term DR on HSC functionality involving distinct stress and growth signaling pathways.
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spelling pubmed-48216452016-10-04 Dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging Tang, Duozhuang Tao, Si Chen, Zhiyang Koliesnik, Ievgen Oleksandrovich Calmes, Philip Gerald Hoerr, Verena Han, Bing Gebert, Nadja Zörnig, Martin Löffler, Bettina Morita, Yohei Rudolph, Karl Lenhard J Exp Med Article Dietary restriction (DR) improves health, delays tissue aging, and elongates survival in flies and worms. However, studies on laboratory mice and nonhuman primates revealed ambiguous effects of DR on lifespan despite improvements in health parameters. In this study, we analyzed consequences of adult-onset DR (24 h to 1 yr) on hematopoietic stem cell (HSC) function. DR ameliorated HSC aging phenotypes, such as the increase in number of HSCs and the skewing toward myeloid-biased HSCs during aging. Furthermore, DR increased HSC quiescence and improved the maintenance of the repopulation capacity of HSCs during aging. In contrast to these beneficial effects, DR strongly impaired HSC differentiation into lymphoid lineages and particularly inhibited the proliferation of lymphoid progenitors, resulting in decreased production of peripheral B lymphocytes and impaired immune function. The study shows that DR-dependent suppression of growth factors and interleukins mediates these divergent effects caused by DR. Supplementation of insulin-like growth factor 1 partially reverted the DR-induced quiescence of HSCs, whereas IL-6/IL-7 substitutions rescued the impairment of B lymphopoiesis exposed to DR. Together, these findings delineate positive and negative effects of long-term DR on HSC functionality involving distinct stress and growth signaling pathways. The Rockefeller University Press 2016-04-04 2016-03-07 /pmc/articles/PMC4821645/ /pubmed/26951333 http://dx.doi.org/10.1084/jem.20151100 Text en © 2016 Tang et al. https://creativecommons.org/licenses/by/4.0/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 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Article
Tang, Duozhuang
Tao, Si
Chen, Zhiyang
Koliesnik, Ievgen Oleksandrovich
Calmes, Philip Gerald
Hoerr, Verena
Han, Bing
Gebert, Nadja
Zörnig, Martin
Löffler, Bettina
Morita, Yohei
Rudolph, Karl Lenhard
Dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging
title Dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging
title_full Dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging
title_fullStr Dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging
title_full_unstemmed Dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging
title_short Dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging
title_sort dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4821645/
https://www.ncbi.nlm.nih.gov/pubmed/26951333
http://dx.doi.org/10.1084/jem.20151100
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