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Open AccessArticle

Progressive and Coordinated Mobilization of the Skeletal Muscle Niche throughout Tissue Repair Revealed by Single-Cell Proteomic Analysis

1
Université Paris Est Creteil, INSERM, IMRB, F-94010 Creteil, France
2
EFS, IMRB, F-94010 Creteil, France
3
Sorbonne Université, UMS030 LUMIC, Plateforme CyPS, Hôpital Pitié-Salpêtrière, F-75013 Paris, France
4
ENVA, IMRB, F-94700 Maisons-Alfort, France
5
AP-HP, Hôpitaux Universitaires Henri Mondor & Centre de Référence des Maladies Neuromusculaires GNMH, F-94010 Creteil, France
*
Author to whom correspondence should be addressed.
Academic Editors: Gabriella Minchiotti, Annalisa Fico and Cord Brakebusch
Cells 2021, 10(4), 744; https://doi.org/10.3390/cells10040744
Received: 13 January 2021 / Revised: 2 March 2021 / Accepted: 22 March 2021 / Published: 28 March 2021
Background: Skeletal muscle is one of the only mammalian tissues capable of rapid and efficient regeneration after trauma or in pathological conditions. Skeletal muscle regeneration is driven by the muscle satellite cells, the stem cell population in interaction with their niche. Upon injury, muscle fibers undergo necrosis and muscle stem cells activate, proliferate and fuse to form new myofibers. In addition to myogenic cell populations, interaction with other cell types such as inflammatory cells, mesenchymal (fibroadipogenic progenitors—FAPs, pericytes) and vascular (endothelial) lineages are important for efficient muscle repair. While the role of the distinct populations involved in skeletal muscle regeneration is well characterized, the quantitative changes in the muscle stem cell and niche during the regeneration process remain poorly characterized. Methods: We have used mass cytometry to follow the main muscle cell types (muscle stem cells, vascular, mesenchymal and immune cell lineages) during early activation and over the course of muscle regeneration at D0, D2, D5 and D7 compared with uninjured muscles. Results: Early activation induces a number of rapid changes in the proteome of multiple cell types. Following the induction of damage, we observe a drastic loss of myogenic, vascular and mesenchymal cell lineages while immune cells invade the damaged tissue to clear debris and promote muscle repair. Immune cells constitute up to 80% of the mononuclear cells 5 days post-injury. We show that muscle stem cells are quickly activated in order to form new myofibers and reconstitute the quiescent muscle stem cell pool. In addition, our study provides a quantitative analysis of the various myogenic populations during muscle repair. Conclusions: We have developed a mass cytometry panel to investigate the dynamic nature of muscle regeneration at a single-cell level. Using our panel, we have identified early changes in the proteome of stressed satellite and niche cells. We have also quantified changes in the major cell types of skeletal muscle during regeneration and analyzed myogenic transcription factor expression in satellite cells throughout this process. Our results highlight the progressive dynamic shifts in cell populations and the distinct states of muscle stem cells adopted during skeletal muscle regeneration. Our findings give a deeper understanding of the cellular and molecular aspects of muscle regeneration. View Full-Text
Keywords: skeletal muscle; muscle stem cells; satellite cells; regeneration; muscle niche; CyTOF skeletal muscle; muscle stem cells; satellite cells; regeneration; muscle niche; CyTOF
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MDPI and ACS Style

Borok, M.; Didier, N.; Gattazzo, F.; Ozturk, T.; Corneau, A.; Rouard, H.; Relaix, F. Progressive and Coordinated Mobilization of the Skeletal Muscle Niche throughout Tissue Repair Revealed by Single-Cell Proteomic Analysis. Cells 2021, 10, 744. https://doi.org/10.3390/cells10040744

AMA Style

Borok M, Didier N, Gattazzo F, Ozturk T, Corneau A, Rouard H, Relaix F. Progressive and Coordinated Mobilization of the Skeletal Muscle Niche throughout Tissue Repair Revealed by Single-Cell Proteomic Analysis. Cells. 2021; 10(4):744. https://doi.org/10.3390/cells10040744

Chicago/Turabian Style

Borok, Matthew; Didier, Nathalie; Gattazzo, Francesca; Ozturk, Teoman; Corneau, Aurelien; Rouard, Helene; Relaix, Frederic. 2021. "Progressive and Coordinated Mobilization of the Skeletal Muscle Niche throughout Tissue Repair Revealed by Single-Cell Proteomic Analysis" Cells 10, no. 4: 744. https://doi.org/10.3390/cells10040744

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