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Oscillations of Delta-like1 regulate the balance between differentiation and maintenance of muscle stem cells

Cell-cell interactions mediated by Notch are critical for the maintenance of skeletal muscle stem cells. However, dynamics, cellular source and identity of functional Notch ligands during expansion of the stem cell pool in muscle growth and regeneration remain poorly characterized. Here we demonstra...

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Autores principales: Zhang, Yao, Lahmann, Ines, Baum, Katharina, Shimojo, Hiromi, Mourikis, Philippos, Wolf, Jana, Kageyama, Ryoichiro, Birchmeier, Carmen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7910593/
https://www.ncbi.nlm.nih.gov/pubmed/33637744
http://dx.doi.org/10.1038/s41467-021-21631-4
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author Zhang, Yao
Lahmann, Ines
Baum, Katharina
Shimojo, Hiromi
Mourikis, Philippos
Wolf, Jana
Kageyama, Ryoichiro
Birchmeier, Carmen
author_facet Zhang, Yao
Lahmann, Ines
Baum, Katharina
Shimojo, Hiromi
Mourikis, Philippos
Wolf, Jana
Kageyama, Ryoichiro
Birchmeier, Carmen
author_sort Zhang, Yao
collection PubMed
description Cell-cell interactions mediated by Notch are critical for the maintenance of skeletal muscle stem cells. However, dynamics, cellular source and identity of functional Notch ligands during expansion of the stem cell pool in muscle growth and regeneration remain poorly characterized. Here we demonstrate that oscillating Delta-like 1 (Dll1) produced by myogenic cells is an indispensable Notch ligand for self-renewal of muscle stem cells in mice. Dll1 expression is controlled by the Notch target Hes1 and the muscle regulatory factor MyoD. Consistent with our mathematical model, our experimental analyses show that Hes1 acts as the oscillatory pacemaker, whereas MyoD regulates robust Dll1 expression. Interfering with Dll1 oscillations without changing its overall expression level impairs self-renewal, resulting in premature differentiation of muscle stem cells during muscle growth and regeneration. We conclude that the oscillatory Dll1 input into Notch signaling ensures the equilibrium between self-renewal and differentiation in myogenic cell communities.
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spelling pubmed-79105932021-03-04 Oscillations of Delta-like1 regulate the balance between differentiation and maintenance of muscle stem cells Zhang, Yao Lahmann, Ines Baum, Katharina Shimojo, Hiromi Mourikis, Philippos Wolf, Jana Kageyama, Ryoichiro Birchmeier, Carmen Nat Commun Article Cell-cell interactions mediated by Notch are critical for the maintenance of skeletal muscle stem cells. However, dynamics, cellular source and identity of functional Notch ligands during expansion of the stem cell pool in muscle growth and regeneration remain poorly characterized. Here we demonstrate that oscillating Delta-like 1 (Dll1) produced by myogenic cells is an indispensable Notch ligand for self-renewal of muscle stem cells in mice. Dll1 expression is controlled by the Notch target Hes1 and the muscle regulatory factor MyoD. Consistent with our mathematical model, our experimental analyses show that Hes1 acts as the oscillatory pacemaker, whereas MyoD regulates robust Dll1 expression. Interfering with Dll1 oscillations without changing its overall expression level impairs self-renewal, resulting in premature differentiation of muscle stem cells during muscle growth and regeneration. We conclude that the oscillatory Dll1 input into Notch signaling ensures the equilibrium between self-renewal and differentiation in myogenic cell communities. Nature Publishing Group UK 2021-02-26 /pmc/articles/PMC7910593/ /pubmed/33637744 http://dx.doi.org/10.1038/s41467-021-21631-4 Text en © The Author(s) 2021, corrected publication 2021 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
Zhang, Yao
Lahmann, Ines
Baum, Katharina
Shimojo, Hiromi
Mourikis, Philippos
Wolf, Jana
Kageyama, Ryoichiro
Birchmeier, Carmen
Oscillations of Delta-like1 regulate the balance between differentiation and maintenance of muscle stem cells
title Oscillations of Delta-like1 regulate the balance between differentiation and maintenance of muscle stem cells
title_full Oscillations of Delta-like1 regulate the balance between differentiation and maintenance of muscle stem cells
title_fullStr Oscillations of Delta-like1 regulate the balance between differentiation and maintenance of muscle stem cells
title_full_unstemmed Oscillations of Delta-like1 regulate the balance between differentiation and maintenance of muscle stem cells
title_short Oscillations of Delta-like1 regulate the balance between differentiation and maintenance of muscle stem cells
title_sort oscillations of delta-like1 regulate the balance between differentiation and maintenance of muscle stem cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7910593/
https://www.ncbi.nlm.nih.gov/pubmed/33637744
http://dx.doi.org/10.1038/s41467-021-21631-4
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