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Volume 11
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10.3390/biom11081171
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Article

Characterization of the Skeletal Muscle Secretome Reveals a Role for Extracellular Vesicles and IL1α/IL1β in Restricting Fibro/Adipogenic Progenitor Adipogenesis

by
Simone Vumbaca
1,*,
Giulio Giuliani
1,
Valeria Fiorentini
1,
Flavia Tortolici
1,
Andrea Cerquone Perpetuini
1,
Federica Riccio
1,
Simona Sennato
2,
Cesare Gargioli
1,
Claudia Fuoco
1,*,
Luisa Castagnoli
1 and
Gianni Cesareni
1
1
Department of Biology, University of Rome Tor Vergata, Via delle Ricerca Scientifica 1, 00133 Rome, Italy
2
Sapienza Unit, Physics Department, Institute for Complex Systems (ISC), National Research Council, Sapienza University of Rome, P.le A. Moro 2, 00185 Rome, Italy
*
Authors to whom correspondence should be addressed.
Biomolecules 2021, 11(8), 1171; https://doi.org/10.3390/biom11081171
Submission received: 11 June 2021 / Revised: 1 August 2021 / Accepted: 5 August 2021 / Published: 8 August 2021
(This article belongs to the Special Issue State-of-the-Art of Myology in Italy 2020–2021)
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Abstract

Repeated mechanical stress causes injuries in the adult skeletal muscle that need to be repaired. Although muscle regeneration is a highly efficient process, it fails in some pathological conditions, compromising tissue functionality. This may be caused by aberrant cell–cell communication, resulting in the deposition of fibrotic and adipose infiltrates. Here, we investigate in vivo changes in the profile of skeletal muscle secretome during the regeneration process to suggest new targetable regulatory circuits whose failure may lead to tissue degeneration in pathological conditions. We describe the kinetic variation of expression levels of 76 secreted proteins during the regeneration process. In addition, we profile the gene expression of immune cells, endothelial cells, satellite cells, and fibro-adipogenic progenitors. This analysis allowed us to annotate each cell-type with the cytokines and receptors they have the potential to synthetize, thus making it possible to draw a cell–cell interaction map. We next selected 12 cytokines whose receptors are expressed in FAPs and tested their ability to modulate FAP adipogenesis and proliferation. We observed that IL1α and IL1β potently inhibit FAP adipogenesis, while EGF and BTC notably promote FAP proliferation. In addition, we characterized the cross-talk mediated by extracellular vesicles (EVs). We first monitored the modulation of muscle EV cargo during tissue regeneration. Using a single-vesicle flow cytometry approach, we observed that EVs differentially affect the uptake of RNA and proteins into their lumen. We also investigated the EV capability to interact with SCs and FAPs and to modulate their proliferation and differentiation. We conclude that both cytokines and EVs secreted during muscle regeneration have the potential to modulate adipogenic differentiation of FAPs. The results of our approach provide a system-wide picture of mechanisms that control cell fate during the regeneration process in the muscle niche.
Keywords: muscle regeneration; secretome; cytokine; extracellular vesicles; faps; adipogenesis muscle regeneration; secretome; cytokine; extracellular vesicles; faps; adipogenesis

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MDPI and ACS Style

Vumbaca, S.; Giuliani, G.; Fiorentini, V.; Tortolici, F.; Cerquone Perpetuini, A.; Riccio, F.; Sennato, S.; Gargioli, C.; Fuoco, C.; Castagnoli, L.; et al. Characterization of the Skeletal Muscle Secretome Reveals a Role for Extracellular Vesicles and IL1α/IL1β in Restricting Fibro/Adipogenic Progenitor Adipogenesis. Biomolecules 2021, 11, 1171. https://doi.org/10.3390/biom11081171

AMA Style

Vumbaca S, Giuliani G, Fiorentini V, Tortolici F, Cerquone Perpetuini A, Riccio F, Sennato S, Gargioli C, Fuoco C, Castagnoli L, et al. Characterization of the Skeletal Muscle Secretome Reveals a Role for Extracellular Vesicles and IL1α/IL1β in Restricting Fibro/Adipogenic Progenitor Adipogenesis. Biomolecules. 2021; 11(8):1171. https://doi.org/10.3390/biom11081171

Chicago/Turabian Style

Vumbaca, Simone, Giulio Giuliani, Valeria Fiorentini, Flavia Tortolici, Andrea Cerquone Perpetuini, Federica Riccio, Simona Sennato, Cesare Gargioli, Claudia Fuoco, Luisa Castagnoli, and et al. 2021. "Characterization of the Skeletal Muscle Secretome Reveals a Role for Extracellular Vesicles and IL1α/IL1β in Restricting Fibro/Adipogenic Progenitor Adipogenesis" Biomolecules 11, no. 8: 1171. https://doi.org/10.3390/biom11081171

APA Style

Vumbaca, S., Giuliani, G., Fiorentini, V., Tortolici, F., Cerquone Perpetuini, A., Riccio, F., Sennato, S., Gargioli, C., Fuoco, C., Castagnoli, L., & Cesareni, G. (2021). Characterization of the Skeletal Muscle Secretome Reveals a Role for Extracellular Vesicles and IL1α/IL1β in Restricting Fibro/Adipogenic Progenitor Adipogenesis. Biomolecules, 11(8), 1171. https://doi.org/10.3390/biom11081171

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