Characterization and functional analysis of extracellular vesicles and muscle-abundant miRNAs (miR-1, miR-133a, and miR-206) in C2C12 Myocytes and mdx mice
Open accessAbstract
Duchenne muscular dystrophy (DMD) is a progressive neuromuscular disorder. Here, we show that the CD63 antigen, which is located on the surface of extracellular vesicles (EVs), is associated with increased levels of muscle-abundant miRNAs, namely myomiRs miR-1, miR-133a, and miR-206, in the sera of DMD patients and mdx mice. Furthermore, the release of EVs from the murine myoblast C2C12 cell line was found to be modulated by intracellular ceramide levels in a Ca2+-dependent manner. Next, to investigate the effects of EVs on cell survival, C2C12 myoblasts and myotubes were cultured with EVs from the sera of mdx mice or C2C12 cells overexpressing myomiRs in presence of cellular stresses. Both the exposure of C2C12 myoblasts and myotubes to EVs from the serum of mdx mice, and the overexpression of miR-133a in C2C12 cells in presence of cellular stress resulted in a significant decrease in cell death. Finally, to assess whether miRNAs regulate skeletal muscle regeneration in vivo, we intraperitoneally injected GW4869 (an inhibitor of exosome secretion) into mdx mice for 5 and 10 days. Levels of miRNAs and creatine kinase in the serum of GW4869-treated mdx mice were significantly downregulated compared with those of controls. The tibialis anterior muscles of the GW4869-treated mdx mice showed a robust decrease in Evans blue dye uptake. Collectively, these results indicate that EVs and myomiRs might protect the skeletal muscle of mdx mice from degeneration.
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Blood ELVs play an important role in the regulation of myogenesis and muscle mass.
“thus suggesting an important role of blood ELVs on the regulation of myogenesis and muscle mass.”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Matsuzaka et al., 2016
Proliferation of C2C12 myoblasts is increased after 24 h of treatment with serum ELVs from mdx mice compared with ELV-depleted serum.
“proliferation of C2C12 myoblasts is increased after 24 h of treatment with serum ELVs from mice suffering from Duchenne muscular dystrophy (mdx mice) compared with ELV-depleted serum”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Matsuzaka et al., 2016
Intraperitoneal injections for 5-10 days of an inhibitor of ceramide synthesis improve muscle function and structure in mdx mice vs. untreated mdx animals.
“intraperitoneal injections for 5–10 days of an inhibitor of ceramide synthesis improved muscle function and structure in mdx mice vs. untreated mdx animals”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Matsuzaka et al., 2016
Modulation of ELV release might be a therapeutic approach to regulate deleterious organ cross-talks associated with the transfer of deleterious EV cargos.
“it is a proof-of-concept that modulation of ELV release might be a therapeutic approach to regulate deleterious organ cross-talks associated with the transfer of deleterious EV cargos”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Matsuzaka et al., 2016
Excessive concentration of circulating palmitate and saturated fatty acids associated with high-fat diet increases intra-muscular ceramides that regulate ELV release from muscle.
“It is likely that excessive concentration of circulating palmitate and saturated fatty acids associated with this specific high-fat diet had increased the concentration of intra-muscular ceramides that regulate ELV release from muscle”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Matsuzaka et al., 2016
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Skeletal Muscle-Released Extracellular Vesicles: State of the Art
Rome, S., Forterre, A., Mizgier, M. L., & Bouzakri, K. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00929 · Cited by 139 · see citing works
- Authors
- Matsuzaka, Y., Tanihata, J., Komaki, H., Ishiyama, A., Oya, Y., Rüegg, U., Takeda, S.-I., & Hashido, K.
- Affiliations
- National Center of Neurology and Psychiatry (JP)
- University of Geneva (CH)
- Corresponding author
- Hashido, Kazuo
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2016-12-15
- Volume
- 11
- Issue
- 12
- Pages
- e0167811
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5158003
- OpenAlex
- W2563686128
- Cited by
- 68
- References
- 67
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 7 · 2023: 12 · 2022: 13 · 2021: 5 · 2020: 7 · 2019: 10 · 2018: 4 · 2017: 2
- FWCI
- 2.77
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Intramural Research Grant (25-5) for Neurological and Psychiatric Disorders of NCNP
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Keywords
- extracellular vesicles, myomiRs, miR-1, miR-133a, miR-206, Duchenne muscular dystrophy, mdx mice, CD63, ceramide, calcium signaling, exosome secretion, GW4869, skeletal muscle regeneration, serum biomarkers
- MeSH terms
- Extracellular Vesicles, Animals, Cell Line, Mice, Inbred mdx, Muscle, Skeletal, Muscular Dystrophy, Duchenne, MicroRNAs, Mice
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