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Reciprocal signalling by Notch–Collagen V–CALCR retains muscle stem cells in their niche

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  • Meryem B. Baghdadi

    (Institut Pasteur
    CNRS UMR 3738, Institut Pasteur
    Sorbonne Universités, UPMC, University of Paris 06)

  • David Castel

    (UMR8203, CNRS, Gustave Roussy, Université Paris-Sud, Université Paris-Saclay
    Gustave Roussy, Université Paris-Sud, Université Paris-Saclay)

  • Léo Machado

    (INSERM IMRB U955-E10, UPEC, ENVA, EFS)

  • So-ichiro Fukada

    (Graduate School of Pharmaceutical Sciences, Osaka University)

  • David E. Birk

    (University of South Florida Morsani College of Medicine)

  • Frederic Relaix

    (INSERM IMRB U955-E10, UPEC, ENVA, EFS)

  • Shahragim Tajbakhsh

    (Institut Pasteur
    CNRS UMR 3738, Institut Pasteur)

  • Philippos Mourikis

    (INSERM IMRB U955-E10, UPEC, ENVA, EFS)

Abstract

The cell microenvironment, which is critical for stem cell maintenance, contains both cellular and non-cellular components, including secreted growth factors and the extracellular matrix1–3. Although Notch and other signalling pathways have previously been reported to regulate quiescence of stem cells4–9, the composition and source of molecules that maintain the stem cell niche remain largely unknown. Here we show that adult muscle satellite (stem) cells in mice produce extracellular matrix collagens to maintain quiescence in a cell-autonomous manner. Using chromatin immunoprecipitation followed by sequencing, we identified NOTCH1/RBPJ-bound regulatory elements adjacent to specific collagen genes, the expression of which is deregulated in Notch-mutant mice. Moreover, we show that Collagen V (COLV) produced by satellite cells is a critical component of the quiescent niche, as depletion of COLV by conditional deletion of the Col5a1 gene leads to anomalous cell cycle entry and gradual diminution of the stem cell pool. Notably, the interaction of COLV with satellite cells is mediated by the Calcitonin receptor, for which COLV acts as a surrogate local ligand. Systemic administration of a calcitonin derivative is sufficient to rescue the quiescence and self-renewal defects found in COLV-null satellite cells. This study reveals a Notch–COLV–Calcitonin receptor signalling cascade that maintains satellite cells in a quiescent state in a cell-autonomous fashion, and raises the possibility that similar reciprocal mechanisms act in diverse stem cell populations.

Suggested Citation

  • Meryem B. Baghdadi & David Castel & Léo Machado & So-ichiro Fukada & David E. Birk & Frederic Relaix & Shahragim Tajbakhsh & Philippos Mourikis, 2018. "Reciprocal signalling by Notch–Collagen V–CALCR retains muscle stem cells in their niche," Nature, Nature, vol. 557(7707), pages 714-718, May.
  • Handle: RePEc:nat:nature:v:557:y:2018:i:7707:d:10.1038_s41586-018-0144-9
    DOI: 10.1038/s41586-018-0144-9
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    Cited by:

    1. Suyang Zhang & Feng Yang & Yile Huang & Liangqiang He & Yuying Li & Yi Ching Esther Wan & Yingzhe Ding & Kui Ming Chan & Ting Xie & Hao Sun & Huating Wang, 2023. "ATF3 induction prevents precocious activation of skeletal muscle stem cell by regulating H2B expression," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    2. Caroline E. Brun & Marie-Claude Sincennes & Alexander Y. T. Lin & Derek Hall & William Jarassier & Peter Feige & Fabien Le Grand & Michael A. Rudnicki, 2022. "GLI3 regulates muscle stem cell entry into GAlert and self-renewal," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Zhang, Yuan & Cao, Jinde & Liu, Lixia & Liu, Haihong & Li, Zhouhong, 2024. "Complex role of time delay in dynamical coordination of neural progenitor fate decisions mediated by Notch pathway," Chaos, Solitons & Fractals, Elsevier, vol. 180(C).
    4. Felicia Lazure & Rick Farouni & Korin Sahinyan & Darren M. Blackburn & Aldo Hernández-Corchado & Gabrielle Perron & Tianyuan Lu & Adrien Osakwe & Jiannis Ragoussis & Colin Crist & Theodore J. Perkins , 2023. "Transcriptional reprogramming of skeletal muscle stem cells by the niche environment," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Xiaoyan Wei & Angelos Rigopoulos & Matthias Lienhard & Sophie Pöhle-Kronawitter & Georgios Kotsaris & Julia Franke & Nikolaus Berndt & Joy Orezimena Mejedo & Hao Wu & Stefan Börno & Bernd Timmermann &, 2024. "Neurofibromin 1 controls metabolic balance and Notch-dependent quiescence of murine juvenile myogenic progenitors," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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