Unexpected contribution of fibroblasts to muscle lineage as a mechanism for limb muscle patterning

Joana Esteves de Lima, Cédrine Blavet, Marie-Ange Bonnin, Estelle Hirsinger, Glenda Comai, Laurent Yvernogeau, Marie-Claire Delfini, Léa Bellenger, Sébastien Mella, Sonya Nassari, Catherine Robin, Ronen Schweitzer, Claire Fournier-Thibault, Thierry Jaffredo, Shahragim Tajbakhsh, Frédéric Relaix and Delphine Duprez ()
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Joana Esteves de Lima: Developmental Biology Laboratory, Institut Biologie Paris Seine, Sorbonne Université, CNRS, IBPS-UMR 7622
Cédrine Blavet: Developmental Biology Laboratory, Institut Biologie Paris Seine, Sorbonne Université, CNRS, IBPS-UMR 7622
Marie-Ange Bonnin: Developmental Biology Laboratory, Institut Biologie Paris Seine, Sorbonne Université, CNRS, IBPS-UMR 7622
Estelle Hirsinger: Developmental Biology Laboratory, Institut Biologie Paris Seine, Sorbonne Université, CNRS, IBPS-UMR 7622
Glenda Comai: Institut Pasteur, CNRS UMR 3738
Laurent Yvernogeau: Developmental Biology Laboratory, Institut Biologie Paris Seine, Sorbonne Université, CNRS, IBPS-UMR 7622
Marie-Claire Delfini: Developmental Biology Laboratory, Institut Biologie Paris Seine, Sorbonne Université, CNRS, IBPS-UMR 7622
Léa Bellenger: ARTbio Bioinformatics Platform, Inserm US 037
Sébastien Mella: Institut Pasteur, CNRS UMR 3738
Sonya Nassari: Developmental Biology Laboratory, Institut Biologie Paris Seine, Sorbonne Université, CNRS, IBPS-UMR 7622
Catherine Robin: University Medical Center Utrecht
Ronen Schweitzer: Research Division, Shriners Hospital for Children
Claire Fournier-Thibault: Developmental Biology Laboratory, Institut Biologie Paris Seine, Sorbonne Université, CNRS, IBPS-UMR 7622
Thierry Jaffredo: Developmental Biology Laboratory, Institut Biologie Paris Seine, Sorbonne Université, CNRS, IBPS-UMR 7622
Shahragim Tajbakhsh: Institut Pasteur, CNRS UMR 3738
Frédéric Relaix: Univ Paris Est Creteil, INSERM, EnvA, EFS, AP-HP, IMRB
Delphine Duprez: Developmental Biology Laboratory, Institut Biologie Paris Seine, Sorbonne Université, CNRS, IBPS-UMR 7622

Nature Communications, 2021, vol. 12, issue 1, 1-17

Abstract: Abstract Positional information driving limb muscle patterning is contained in connective tissue fibroblasts but not in myogenic cells. Limb muscles originate from somites, while connective tissues originate from lateral plate mesoderm. With cell and genetic lineage tracing we challenge this model and identify an unexpected contribution of lateral plate-derived fibroblasts to the myogenic lineage, preferentially at the myotendinous junction. Analysis of single-cell RNA-sequencing data from whole limbs at successive developmental stages identifies a population displaying a dual muscle and connective tissue signature. BMP signalling is active in this dual population and at the tendon/muscle interface. In vivo and in vitro gain- and loss-of-function experiments show that BMP signalling regulates a fibroblast-to-myoblast conversion. These results suggest a scenario in which BMP signalling converts a subset of lateral plate mesoderm-derived cells to a myogenic fate in order to create a boundary of fibroblast-derived myonuclei at the myotendinous junction that controls limb muscle patterning.

Date: 2021
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DOI: 10.1038/s41467-021-24157-x

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