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Extraocular muscle stem cells exhibit distinct cellular properties associated with non-muscle molecular signatures

Daniela Di Girolamo, Maria Benavente-Diaz, Alexandre Grimaldi, Priscilla Thomas Lopes, Melania Murolo, View ORCID ProfileBrendan Evano, Stamatia Gioftsidi, Vincent Laville, Sebastian Mella, View ORCID ProfileShahragim Tajbakhsh, View ORCID ProfileGlenda Comai
doi: https://doi.org/10.1101/2023.03.10.532049
Daniela Di Girolamo
1Stem Cells & Development Unit, 25 rue du Dr. Roux, Institut Pasteur, 75015 Paris, France
2UMR CNRS 3738, Institut Pasteur, Paris, France
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Maria Benavente-Diaz
1Stem Cells & Development Unit, 25 rue du Dr. Roux, Institut Pasteur, 75015 Paris, France
2UMR CNRS 3738, Institut Pasteur, Paris, France
3Sorbonne Universités, Complexité du Vivant, F-75005, Paris, France
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Alexandre Grimaldi
1Stem Cells & Development Unit, 25 rue du Dr. Roux, Institut Pasteur, 75015 Paris, France
2UMR CNRS 3738, Institut Pasteur, Paris, France
3Sorbonne Universités, Complexité du Vivant, F-75005, Paris, France
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Priscilla Thomas Lopes
1Stem Cells & Development Unit, 25 rue du Dr. Roux, Institut Pasteur, 75015 Paris, France
2UMR CNRS 3738, Institut Pasteur, Paris, France
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Melania Murolo
1Stem Cells & Development Unit, 25 rue du Dr. Roux, Institut Pasteur, 75015 Paris, France
2UMR CNRS 3738, Institut Pasteur, Paris, France
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Brendan Evano
1Stem Cells & Development Unit, 25 rue du Dr. Roux, Institut Pasteur, 75015 Paris, France
2UMR CNRS 3738, Institut Pasteur, Paris, France
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  • ORCID record for Brendan Evano
Stamatia Gioftsidi
4Université Paris-Est, 77420, Champs-sur-Marne, France
5Freie Universität Berlin, 14195, Berlin, Germany
6Inserm, IMRB U955-E10, 94000, Créteil, France
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Vincent Laville
1Stem Cells & Development Unit, 25 rue du Dr. Roux, Institut Pasteur, 75015 Paris, France
2UMR CNRS 3738, Institut Pasteur, Paris, France
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Sebastian Mella
7Hub de Bioinformatique et Biostatistique, Cytométrie et Biomarqueurs, Institut Pasteur, 75015 Paris, France
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Shahragim Tajbakhsh
1Stem Cells & Development Unit, 25 rue du Dr. Roux, Institut Pasteur, 75015 Paris, France
2UMR CNRS 3738, Institut Pasteur, Paris, France
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  • ORCID record for Shahragim Tajbakhsh
  • For correspondence: comai@pasteur.fr
Glenda Comai
1Stem Cells & Development Unit, 25 rue du Dr. Roux, Institut Pasteur, 75015 Paris, France
2UMR CNRS 3738, Institut Pasteur, Paris, France
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  • ORCID record for Glenda Comai
  • For correspondence: comai@pasteur.fr
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Abstract

The muscle stem cell (MuSC) population is recognized as functionally heterogeneous. Cranial muscle stem cells, which originate from head mesoderm, can have greater proliferative capacity in culture and higher regenerative potential in transplantation assays when compared to those in the limb. The existence of such functional differences in phenotypic outputs remain unresolved as a comprehensive understanding of the underlying mechanisms is lacking. We addressed this issue using a combination of clonal analysis, live imaging, and scRNA-seq, identifying critical biological features that distinguish extraocular (EOM) and limb (Tibialis anterior, TA) MuSC populations. Time-lapse studies using a MyogenintdTomatoreporter showed that the increased proliferation capacity of EOM MuSCs is accompanied by a differentiation delay in vitro. Unexpectedly, in vitro activated EOM MuSCs expressed a large array of distinct extracellular matrix (ECM) components, growth factors, and signaling molecules that are typically associated with mesenchymal non-muscle cells. These unique features are regulated by a specific set of transcription factors that constitute a coregulating module. This transcription factor network, which includes Foxc1 as one of the major players, appears to be hardwired to EOM identity as it is present in quiescent adult MuSCs, in the activated counterparts during growth and retained upon passages in vitro. These findings provide insights into how high-performing MuSCs regulate myogenic commitment by active remodeling of their local environment.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵# Co-first authors

  • updated version with more functional data on Figure 7

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted May 22, 2023.
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Extraocular muscle stem cells exhibit distinct cellular properties associated with non-muscle molecular signatures
Daniela Di Girolamo, Maria Benavente-Diaz, Alexandre Grimaldi, Priscilla Thomas Lopes, Melania Murolo, Brendan Evano, Stamatia Gioftsidi, Vincent Laville, Sebastian Mella, Shahragim Tajbakhsh, Glenda Comai
bioRxiv 2023.03.10.532049; doi: https://doi.org/10.1101/2023.03.10.532049
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Extraocular muscle stem cells exhibit distinct cellular properties associated with non-muscle molecular signatures
Daniela Di Girolamo, Maria Benavente-Diaz, Alexandre Grimaldi, Priscilla Thomas Lopes, Melania Murolo, Brendan Evano, Stamatia Gioftsidi, Vincent Laville, Sebastian Mella, Shahragim Tajbakhsh, Glenda Comai
bioRxiv 2023.03.10.532049; doi: https://doi.org/10.1101/2023.03.10.532049

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