Sphingolipids in Extracellular Vesicles Released From the Skeletal Muscle Plasma Membrane Control Muscle Stem Cell Fate During Muscle Regeneration Article Swipe
Rhyma Hakkar
,
Caroline Brun
,
Pascal Leblanc
,
Emmanuelle Meugnier
,
Eric G. Berger
,
Olivier Blanc‐Brude
,
Stefano Tacconi
,
Audrey Jalabert
,
Laura Reininger
,
Sandra Pesenti
,
Catherine Calzada
,
Vincent Gache
,
Sara Vasan
,
Julien Pichon
,
Thibaut Larcher
,
Elizabeth Errazuriz-Cerda
,
C Cassin
,
Bong Hwan Sung
,
Alissa M. Weaver
,
Antonella Bongiovanni
,
Karl Rouger
,
Jean-Paul Paı̈s de Barros
,
Karim Bouzakri
,
Sophie Rome
·
YOU?
·
· 2025
· Open Access
·
· DOI: https://doi.org/10.1002/jev2.70164
YOU?
·
· 2025
· Open Access
·
· DOI: https://doi.org/10.1002/jev2.70164
Extracellular vesicles (EVs) represent a cytokine‐independent pathway though which skeletal muscle (SkM) cells influence the fate of neighbouring cells, thereby regulating SkM metabolic homeostasis and regeneration. Although SkM‐EVs are increasingly being explored as a therapeutic strategy to enhance muscle regeneration or to induce the myogenic differentiation of induced pluripotent stem cells (iPSCs), the mechanisms governing their release from muscle cells remain poorly described. Moreover, because muscle regeneration involves a tightly regulated inflammatory response it also important to determine how inflammation alters SkM‐EV cargo and function in order to design more effective EV‐based therapies. To address this knowledge gap, we isolated and characterized the large and small EVs (lEVs, sEVs) released from SkM cells under basal conditions and in response to TNF‐α, a well‐established inflammatory mediator elevated in both acute muscle injury and chronic inflammatory conditions such as type 2 diabetes. We then evaluated the regenerative roles of these EV subtypes in vivo using a mouse model of cardiotoxin‐induced muscle injury, with a specific focus on their bioactive sphingolipid content. Using transmission, scanning or cryo‐electron microscopy, lipidomic profiling and an adenoviral construct to express labelled CD63 in myotubes, we demonstrated that SkM cells release both sEVs and lEVs primarily from the plasma membrane. Notably, sEVs were generated from specialized membrane folds enriched in the EV markers ALIX (ALG‐2 interacting protein X) and TSG101, as well as lipid raft‐associated lipids. During regeneration, sEVs promoted M1 macrophage polarization and migration and muscle stem cell (MuSC) differentiation, thereby accelerating muscle repair. In contrast, lEVs inhibited and promoted MuSC proliferation and impaired the transition from the pro‐inflammatory to the anti‐inflammatory response, an essential step for promoting MuSC differentiation. Treatment of isolated muscle fibres with SkM‐EVs revealed that the distinct effects of sEVs and lEVs on MuSC behaviour and macrophage phenotype could be largely explained by differences in their lipid composition, particularly the ratio of sphingosine‐1‐phosphate (S1P) subspecies. However, TNF‐α exposure altered these ratios in sEVs and impaired their regenerative functions on MuSC and their effect on macrophage migration and polarization. These results demonstrate for the first time the importance of the sphingolipid content of EVs released by skeletal muscle in their regenerative function within muscle tissue, largely explained by their role as carriers of different subspecies of sphingosine‐1‐phosphate. This suggests that modulating the sphingolipid composition of EVs could be a viable strategy to enhance the regenerative potential of muscle tissue in addition to therapeutic interventions.
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- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.1002/jev2.70164
- https://onlinelibrary.wiley.com/doi/pdfdirect/10.1002/jev2.70164
- OA Status
- gold
- Cited By
- 3
- References
- 74
- OpenAlex ID
- https://openalex.org/W4414452965
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Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W4414452965Canonical identifier for this work in OpenAlex
- DOI
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https://doi.org/10.1002/jev2.70164Digital Object Identifier
- Title
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Sphingolipids in Extracellular Vesicles Released From the Skeletal Muscle Plasma Membrane Control Muscle Stem Cell Fate During Muscle RegenerationWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2025Year of publication
- Publication date
-
2025-09-01Full publication date if available
- Authors
-
Rhyma Hakkar, Caroline Brun, Pascal Leblanc, Emmanuelle Meugnier, Eric G. Berger, Olivier Blanc‐Brude, Stefano Tacconi, Audrey Jalabert, Laura Reininger, Sandra Pesenti, Catherine Calzada, Vincent Gache, Sara Vasan, Julien Pichon, Thibaut Larcher, Elizabeth Errazuriz-Cerda, C Cassin, Bong Hwan Sung, Alissa M. Weaver, Antonella Bongiovanni, Karl Rouger, Jean-Paul Paı̈s de Barros, Karim Bouzakri, Sophie RomeList of authors in order
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https://doi.org/10.1002/jev2.70164Publisher landing page
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https://onlinelibrary.wiley.com/doi/pdfdirect/10.1002/jev2.70164Direct link to full text PDF
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YesWhether a free full text is available
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goldOpen access status per OpenAlex
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https://onlinelibrary.wiley.com/doi/pdfdirect/10.1002/jev2.70164Direct OA link when available
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3Total citation count in OpenAlex
- Citations by year (recent)
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2025: 3Per-year citation counts (last 5 years)
- References (count)
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74Number of works referenced by this work
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