SOXF factors regulate murine satellite cell self-renewal and function through inhibition of β-catenin activity

  1. Sonia Alonso-Martin  Is a corresponding author
  2. Frédéric Auradé
  3. Despoina Mademtzoglou
  4. Anne Rochat
  5. Peter S Zammit
  6. Frédéric Relaix  Is a corresponding author
  1. Institut Mondor de Recherche Biomedicale, INSERM U955-E10, France
  2. Sorbonne Universites, INSERM U974, France
  3. Kings College London, United Kingdom

Abstract

Muscle satellite cells are the primary source of stem cells for postnatal skeletal muscle growth and regeneration. Understanding genetic control of satellite cell formation, maintenance, and acquisition of their stem cell properties is on-going, and we have identified SOXF (SOX7, SOX17, SOX18) transcriptional factors as being induced during satellite cell specification. We demonstrate that SOXF factors regulate satellite cell quiescence, self-renewal and differentiation. Moreover, ablation of Sox17 in the muscle lineage impairs postnatal muscle growth and regeneration. We further determine that activities of SOX7, SOX17 and SOX18 overlap during muscle regeneration, with SOXF transcriptional activity requisite. Finally, we show that SOXF factors also control satellite cell expansion and renewal by directly inhibiting the output of β-catenin activity, including inhibition of Ccnd1 and Axin2. Together, our findings identify a key regulatory function of SoxF genes in muscle stem cells via direct transcriptional control and interaction with canonical Wnt/β-catenin signaling.

Data availability

Sequencing data have been deposited in GEO under accession code GSE63860 and previously published in:Gene Expression Profiling of Muscle Stem Cells Identifies Novel Regulators of Postnatal Myogenesis. Alonso-Martin S, Rochat A, Mademtzoglou D, Morais J, de Reyniès A, Auradé F, Chang TH, Zammit PS, Relaix F. Front Cell Dev Biol. 2016 Jun 21;4:58. doi: 10.3389/fcell.2016.00058. eCollection 2016. PMID: 27446912.

The following previously published data sets were used

Article and author information

Author details

  1. Sonia Alonso-Martin

    Institut Mondor de Recherche Biomedicale, INSERM U955-E10, Créteil, France
    For correspondence
    alonsomartin.s@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3254-0365
  2. Frédéric Auradé

    Center for Research in Myology, Sorbonne Universites, INSERM U974, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Despoina Mademtzoglou

    Institut Mondor de Recherche Biomedicale, INSERM U955-E10, Créteil, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Anne Rochat

    Center for Research in Myology, Sorbonne Universites, INSERM U974, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Peter S Zammit

    Randall Centre for Cell and Molecular Biophysics, Kings College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9562-3072
  6. Frédéric Relaix

    Institut Mondor de Recherche Biomedicale, INSERM U955-E10, Créteil, France
    For correspondence
    frelaix@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1270-1472

Funding

Basque Community (BF106.177)

  • Sonia Alonso-Martin

Muscular Dystrophy UK

  • Peter S Zammit

Medical Research Council

  • Peter S Zammit

FSH Society and BIODESIGN (262948-2)

  • Peter S Zammit

Deutsche Forschungsgemeinschaft (KFO192 (Sp1152/8-1))

  • Despoina Mademtzoglou

Fondation pour la Recherche Médicale (DEQ20130326526)

  • Frédéric Relaix

Agence Nationale de la Recherche (ANR-13-BSV1-0011-02)

  • Frédéric Relaix

Agence Nationale de la Recherche (ANR-12-BSV1-0038-04)

  • Frédéric Relaix

Agence Nationale de la Recherche (ANR-15-CE13-0011-01)

  • Frédéric Relaix

Agence Nationale de la Recherche (ANR-15-RHUS-0003)

  • Frédéric Relaix

Deutsche Forschungsgemeinschaft (GK 1631)

  • Despoina Mademtzoglou

INSERM Avenir Program

  • Frédéric Relaix

Association Française contre les Myopathies (TRANSLAMUSCLE 19507)

  • Frédéric Relaix

Association Institut de Myologie

  • Frédéric Relaix

Labex REVIVE (ANR-10-LABX-73)

  • Frédéric Relaix

European Union Sixth and Seventh Framework Program (MYORES and ENDOSTEM # 241440)

  • Peter S Zammit
  • Frédéric Relaix

Fondation pour la Recherche Médicale (FDT20130928236)

  • Frédéric Relaix

Agence Nationale de la Recherche (ANR 11 BSV2 017 02)

  • Frédéric Relaix

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Randy Schekman, Howard Hughes Medical Institute, University of California, Berkeley, United States

Ethics

Animal experimentation: All animals were maintained inside a barrier facility and all experiment were performed in accordance with the European and French regulations for animal care and handling (Project No: 01427.03 approved by MESR and File No: 15-018 from the Ethical Committee of Anses/ENVA/UPEC).

Version history

  1. Received: February 14, 2017
  2. Accepted: June 7, 2018
  3. Accepted Manuscript published: June 8, 2018 (version 1)
  4. Version of Record published: June 27, 2018 (version 2)

Copyright

© 2018, Alonso-Martin et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Sonia Alonso-Martin
  2. Frédéric Auradé
  3. Despoina Mademtzoglou
  4. Anne Rochat
  5. Peter S Zammit
  6. Frédéric Relaix
(2018)
SOXF factors regulate murine satellite cell self-renewal and function through inhibition of β-catenin activity
eLife 7:e26039.
https://doi.org/10.7554/eLife.26039

Share this article

https://doi.org/10.7554/eLife.26039

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