Heterogeneity and interplay of the extracellular vesicle small RNA transcriptome and proteome
Open accessAbstract
Extracellular vesicles (EVs) mediate cell-to-cell communication by delivering or displaying macromolecules to their recipient cells. While certain broad-spectrum EV effects reflect their protein cargo composition, others have been attributed to individual EV-loaded molecules such as specific miRNAs. In this work, we have investigated the contents of vesicular cargo using small RNA sequencing of cells and EVs from HEK293T, RD4, C2C12, Neuro2a and C17.2. The majority of RNA content in EVs (49-96%) corresponded to rRNA-, coding- and tRNA fragments, corroborating with our proteomic analysis of HEK293T and C2C12 EVs which showed an enrichment of ribosome and translation-related proteins. On the other hand, the overall proportion of vesicular small RNA was relatively low and variable (2-39%) and mostly comprised of miRNAs and sequences mapping to piRNA loci. Importantly, this is one of the few studies, which systematically links vesicular RNA and protein cargo of vesicles. Our data is particularly useful for future work in unravelling the biological mechanisms underlying vesicular RNA and protein sorting and serves as an important guide in developing EVs as carriers for RNA therapeutics.
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Mitochondrial DNA, histones, and nuclear proteins were found in ELV-MB and ELV-MT.
“Interestingly, mitochondrial DNA (Guescini et al., 2010), histones, and nuclear proteins were also found in ELV-MB (Guescini et al., 2010; Forterre et al., 2014a; Sork et al., 2018) and ELV-MT (Le Bihan et al., 2012; Forterre et al., 2014a).”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Sork et al., 2018
Myoblasts produce small exosome-like vesicles (ELV-MB), likely reflecting the intense macromolecule/RNA/lipid turnover that occurs during cell proliferation.
“It has been described that myoblasts produce small ELVs (ELV-MB) (Guescini et al., 2010; Forterre et al., 2014a,b; Sork et al., 2018) likely reflecting the intense macromolecule/RNA/lipids turn-over that occurs during cell proliferation (Johnstone et al., 1991; Desdin-Mico and Mittelbrunn, 2017).”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Sork et al., 2018
Unlike miRNAs, there was no correlation between ELV-MB and cellular concentrations in myoblasts for piRNAs.
“Unlike miRNAs, there was no correlation between ELV-MB and cellular concentrations in myoblast for piRNAs (Sork et al., 2018).”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Sork et al., 2018
All studies reported that individual miRNAs deviate from the relationship: some miRNAs expressed in muscle cells were not detected in ELV-MB and/or ELV-MT; others were found at a higher rate in ELV-MB vs. myoblasts.
“Interestingly, all studies reported also that individual miRNAs deviate from this relationship, i.e., some miRNAs expressed in muscle cells were not detected in ELV-MB (Forterre et al., 2014b) and/or ELV-MT (Figure 6D; Forterre et al., 2014b); other were found at higher rate in ELV-MB vs. myoblasts [miR-451, miR-6239, miR-6,240, miR-6236, miR-144, miR-223, miR-5112, miR-3062, miR-142a, and miR-213”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Sork et al., 2018
C2C12 ELV-MB also contained tRNAs and Y RNA (mainly RNY1).
“C2C12 ELV-MB also contained tRNAs (Sork et al., 2018) and Y RNA (mainly RNY1) (Forterre et al., 2014b; Sork et al., 2018).”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Sork et al., 2018
In silico predictions of the most concentrated miRNAs in ELV-MB indicated that they could collectively regulate important cellular pathways for muscle physiology.
“In silico predictions of the most concentrated miRNAs in ELV-MB (Sork et al., 2018) indicated that they could collectively regulate important cellular pathways for muscle physiology, i.e., signaling pathways involved in the regulation of muscle mass (PI3K-Akt, insulin, MAPK, TGF-beta, proteolysis, and calcium), in the neuromuscular junction, in immune response, and in calcium signaling and cytoske”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Sork et al., 2018
Only the small RNA population has been further analyzed and was found highly enriched in piRNAs and miRNAs.
“Only the small RNA population has been further analyzed (Forterre et al., 2014b; Sork et al., 2018; Xu et al., 2018), and was found highly enriched in piRNAs and miRNAs (Figure 6B; Sork et al., 2018).”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Sork et al., 2018
C2C12 ELV-MB were enriched in small RNA subsets compared with C2C12 parental cells.
“In the case of SkM cells, it was shown that C2C12 ELV-MB were also enriched in small RNAs subsets compared with C2C12 parental cells (Figure 6A; Sork et al., 2018).”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Sork et al., 2018
For the majority of miRNAs, a good correlation was observed between miRNA levels in ELV-MB vs. myoblasts in two independent studies, and between ELVs released from myofibers vs. myofibers.
“For the majority of miRNAs, a good correlation was observed between miRNA levels in ELV-MB vs. MB in two independent studies (Forterre et al., 2014b; Sork et al., 2018), and between ELVs released from myofibers vs. myofibers (De Gasperi et al., 2017)”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Sork et al., 2018
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- Authors
- Sork, H., Corso, G., Krjutskov, K., Johansson, H. J., Nordin, J. Z., Wiklander, O. P. B., Lee, Y. X. F., Westholm, J. O., Lehtiö, J., Wood, M. J. A., Mäger, I., & EL Andaloussi, S.
- Affiliations
- Karolinska Institutet (SE)
- Science for Life Laboratory (SE)
- University of Oxford (GB)
- Stockholm University (SE)
- Corresponding author
- Sork, Helena
- Mäger, Imre
- ORCID
- Venue
- Scientific Reports
- Published
- 2018-07-17
- Volume
- 8
- Issue
- 1
- Pages
- 10813-10813
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC6050237
- OpenAlex
- W2875630158
- Cited by
- 140
- References
- 68
- Citations by year
- 2026: 11 · 2025: 15 · 2024: 15 · 2023: 22 · 2022: 21 · 2021: 22 · 2020: 20 · 2019: 12 · 2018: 2
- FWCI
- 4.98
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Työväentutkimus Vuosikirja (submittedVersion, other-oa)
- Funders
- Sihtasutus Archimedes
- Eesti Teadusagentuur
- Svenska Sällskapet för Medicinsk Forskning
- Karolinska Institutet
- Knut och Alice Wallenbergs Stiftelse
- Stockholms Läns Landsting
- Vetenskapsrådet
- Science for Life Laboratory
- Medical Research Council
- Biotechnology and Biological Sciences Research Council (BB/R021422/1)
- Uppsala Multidisciplinary Center for Advanced Computational Science
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Keywords
- extracellular vesicles, small RNA, microRNA, cell-to-cell communication, RNA therapeutics, vesicle heterogeneity, HEK293T cells, C2C12 myoblasts, N2a cells, C17.2 cells
- MeSH terms
- Extracellular Vesicles, Cell Line, Chromatography, High Pressure Liquid, Humans, RNA, Small Nuclear, Sequence Analysis, RNA, Proteome, RNA, Small Interfering, Tandem Mass Spectrometry, HEK293 Cells, Transcriptome
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