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Primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging

During aging, the regenerative capacity of muscle stem cells (MuSCs) decreases, diminishing the ability of muscle to repair following injury. We found that the ability of MuSCs to regenerate is regulated by the primary cilium, a cellular protrusion that serves as a sensitive sensory organelle. Aboli...

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Autores principales: Palla, Adelaida R., Hilgendorf, Keren I., Yang, Ann V., Kerr, Jaclyn P., Hinken, Aaron C., Demeter, Janos, Kraft, Peggy, Mooney, Nancie A., Yucel, Nora, Burns, David M., Wang, Yu Xin, Jackson, Peter K., Blau, Helen M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8931095/
https://www.ncbi.nlm.nih.gov/pubmed/35301320
http://dx.doi.org/10.1038/s41467-022-29150-6
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author Palla, Adelaida R.
Hilgendorf, Keren I.
Yang, Ann V.
Kerr, Jaclyn P.
Hinken, Aaron C.
Demeter, Janos
Kraft, Peggy
Mooney, Nancie A.
Yucel, Nora
Burns, David M.
Wang, Yu Xin
Jackson, Peter K.
Blau, Helen M.
author_facet Palla, Adelaida R.
Hilgendorf, Keren I.
Yang, Ann V.
Kerr, Jaclyn P.
Hinken, Aaron C.
Demeter, Janos
Kraft, Peggy
Mooney, Nancie A.
Yucel, Nora
Burns, David M.
Wang, Yu Xin
Jackson, Peter K.
Blau, Helen M.
author_sort Palla, Adelaida R.
collection PubMed
description During aging, the regenerative capacity of muscle stem cells (MuSCs) decreases, diminishing the ability of muscle to repair following injury. We found that the ability of MuSCs to regenerate is regulated by the primary cilium, a cellular protrusion that serves as a sensitive sensory organelle. Abolishing MuSC cilia inhibited MuSC proliferation in vitro and severely impaired injury-induced muscle regeneration in vivo. In aged muscle, a cell intrinsic defect in MuSC ciliation was associated with the decrease in regenerative capacity. Exogenous activation of Hedgehog signaling, known to be localized in the primary cilium, promoted MuSC expansion, both in vitro and in vivo. Delivery of the small molecule Smoothened agonist (SAG1.3) to muscles of aged mice restored regenerative capacity leading to increased strength post-injury. These findings provide fresh insights into the signaling dysfunction in aged MuSCs and identify the ciliary Hedgehog signaling pathway as a potential therapeutic target to counter the loss of muscle regenerative capacity which accompanies aging.
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spelling pubmed-89310952022-04-01 Primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging Palla, Adelaida R. Hilgendorf, Keren I. Yang, Ann V. Kerr, Jaclyn P. Hinken, Aaron C. Demeter, Janos Kraft, Peggy Mooney, Nancie A. Yucel, Nora Burns, David M. Wang, Yu Xin Jackson, Peter K. Blau, Helen M. Nat Commun Article During aging, the regenerative capacity of muscle stem cells (MuSCs) decreases, diminishing the ability of muscle to repair following injury. We found that the ability of MuSCs to regenerate is regulated by the primary cilium, a cellular protrusion that serves as a sensitive sensory organelle. Abolishing MuSC cilia inhibited MuSC proliferation in vitro and severely impaired injury-induced muscle regeneration in vivo. In aged muscle, a cell intrinsic defect in MuSC ciliation was associated with the decrease in regenerative capacity. Exogenous activation of Hedgehog signaling, known to be localized in the primary cilium, promoted MuSC expansion, both in vitro and in vivo. Delivery of the small molecule Smoothened agonist (SAG1.3) to muscles of aged mice restored regenerative capacity leading to increased strength post-injury. These findings provide fresh insights into the signaling dysfunction in aged MuSCs and identify the ciliary Hedgehog signaling pathway as a potential therapeutic target to counter the loss of muscle regenerative capacity which accompanies aging. Nature Publishing Group UK 2022-03-17 /pmc/articles/PMC8931095/ /pubmed/35301320 http://dx.doi.org/10.1038/s41467-022-29150-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Palla, Adelaida R.
Hilgendorf, Keren I.
Yang, Ann V.
Kerr, Jaclyn P.
Hinken, Aaron C.
Demeter, Janos
Kraft, Peggy
Mooney, Nancie A.
Yucel, Nora
Burns, David M.
Wang, Yu Xin
Jackson, Peter K.
Blau, Helen M.
Primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging
title Primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging
title_full Primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging
title_fullStr Primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging
title_full_unstemmed Primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging
title_short Primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging
title_sort primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8931095/
https://www.ncbi.nlm.nih.gov/pubmed/35301320
http://dx.doi.org/10.1038/s41467-022-29150-6
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