Single-cell analysis of the muscle stem cell hierarchy identifies heterotypic communication signals involved in skeletal muscle regeneration
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Abstract
Abstract Muscle stem cells (MuSCs) are an essential adult stem cell population with the capacity to self-renew and regenerate muscle tissue. Functionally heterogeneous subpopulations of MuSCs have been identified based on their expression of myogenic regulatory factors and surface markers. However, a unified organization of muscle stem and progenitor cells and their subpopulations remains unresolved. Here, we performed temporal analysis of skeletal muscle regeneration using single-cell RNA-sequencing (scRNA-seq) of myotoxin-injured adult mouse hindlimb muscles. We generated over 34,000 single-cell transcriptomes spanning four muscle regeneration time-points and identified 15 distinct cell types, including a heterogeneous population of MuSCs and progenitor cells. Our analysis provides a hierarchical map of myogenic cell populations and identifies stage-specific regulatory programs that govern their contributions to muscle regeneration. In this transcriptomic atlas, we observed cell type-specific regenerative dynamics, exemplified by waves of transient amplification and diversification of multiple immune cell types and, subsequently, myogenic cells. Unbiased trajectory inference organized the myogenic cell populations within the atlas into a continuum, consisting of a hierarchy of quiescent MuSCs, cycling progenitors, committed myoblasts, and terminally differentiated myocytes. This myogenic trajectory matched prior understanding and also revealed that MuSC stages are defined by synchronous changes in regulatory factors, cell cycle-associated, and surface receptor gene expression. Lastly, we analyzed the transcriptomic atlas to identify over 100 candidate heterotypic communication signals between myogenic and non-myogenic cell populations, including many involving the fibroblast growth factor (FGF), Notch, and Syndecan receptor families and their associated ligands. Syndecan receptors were implicated in a large fraction of these cell communication interactions and were observed to exhibit transcriptional heterogeneity within the myogenic continuum. Using multiparameter mass cytometry (CyTOF), we confirmed that cycling MuSCs exhibit diversified Syndecan-1/2 expression, which suggests that dynamic alterations in Syndecan signaling interactions may coordinate stage-specific myogenic cell fate regulation. This scRNA-seq reference atlas provides a resolved hierarchical organization of myogenic subpopulations as a resource to investigate cell-cell interactions that regulate myogenic stem and progenitor cell fates in muscle regeneration.
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Our data are consistent with previous reports of decreased Pax7 with activation at the ensemble level, when considering only the mean expression of Pax7 at the quiescent and activated time points.
“Our data are consistent with previous reports of decreased Pax7 with activation at the ensemble level (Cornelison and Wold, 1997; De Micheli et al., 2020; Dell'Orso et al., 2019), when we consider only the mean expression of Pax7 at the quiescent and activated time points (Fig. S3C).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as De Micheli et al., 2020
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- Authors
- De Micheli, A. J., Laurilliard, E. J., Heinke, C. L., Ravichandran, H., Fraczek, P., Soueid-Baumgarten, S., De Vlaminck, I., Elemento, O., & Cosgrove, B. D.
- Affiliations
- Cornell University (US)
- Weill Cornell Medicine (US)
- Corresponding author
- Cosgrove, Benjamin D.
- ORCID
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2020-03
- Volume
- 30
- Issue
- 10
- Pages
- 3583-3595.e5
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC7091476
- OpenAlex
- W3011739739
- Cited by
- 373
- References
- 61
- Citations by year
- 2026: 35 · 2025: 55 · 2024: 72 · 2023: 65 · 2022: 70 · 2021: 46 · 2020: 28 · 2019: 2
- FWCI
- 17.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (R00AG042491, R01AG058630, 1DP2AI138242)
- US Department of Education (P200A150273)
- Glenn Medical Research Foundation and American Federation for Aging Research Grant for Junior Faculty
- Cornell Engineering Learning Initiatives Undergraduate Research Award
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- muscle stem cells, skeletal muscle regeneration, paracrine signaling, muscle progenitor cells, syndecans, FGF2, TGF-β1, RSPO3, ligand-receptor interactions, single-cell transcriptome atlas
- MeSH terms
- RNA-Seq, Animals, Cell Communication, Gene Expression Regulation, Ligands, Mice, Inbred C57BL, Models, Biological, Receptors, Cell Surface, Regeneration, Stem Cells, Signal Transduction, Muscle, Skeletal, Paracrine Communication, Muscle Development, Cell Proliferation, Adipogenesis, Syndecans, Single-Cell Analysis
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