Identification and characterization of the nano-sized vesicles released by muscle cells
Open accessAbstract
Several cell types secrete small membranous vesicles that contain cell-specific collections of proteins, lipids, and genetic material. The function of these vesicles is to allow cell-to-cell signaling and the horizontal transfer of their cargo molecules. Here, we demonstrate that muscle cells secrete nano-sized vesicles and that their release increases during muscle differentiation. Analysis of these nanovesicles allowed us to characterize them as exosome-like particles and to define the potential role of the multifunctional protein Alix in their biogenesis.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Myotubes release small exosome-like vesicles (ELV-MT).
“Myotubes also release small ELVs (ELV-MT) (Figure 1D; Le Bihan et al., 2012; Romancino et al., 2013; Forterre et al., 2014a,b)”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Romancino et al., 2013
Loss of Alix protein involved in ILV biogenesis in MVBs resulted in alteration of membrane budding, a decrease in the number of ELV released, and modifications of ELV-MT composition.
“In their study, loss of Alix protein involved in ILV biogenesis in MVBs (Sun et al., 2015) resulted in alteration of membrane budding, a decrease in the number of ELV released and a modifications of ELV-MT composition”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Romancino et al., 2013
Muscle cells release extracellular vesicles into the extracellular milieu, which represent new paracrine and endocrine signals.
“During the last decade, it has been shown that muscle cells also release extracellular vesicles (EVs) into the extracellular milieu, which represent new paracrine and endocrine signals that have modified our conceptual basis to explain how muscles communicate to other organs (Guescini et al., 2010; Le Bihan et al., 2012; Romancino et al., 2013; Forterre et al., 2014a).”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Romancino et al., 2013
Alix protein level was significantly enriched in ELVs released from myotubes than from myoblasts.
“and that Alix protein level was significantly enriched in ELVs released from myotubes than from myoblasts (Romancino et al., 2013).”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Romancino et al., 2013
ELV-MB and ELV-MT may have different origins, and ELVs from myotubes would be produced mainly through budding of the plasma membrane.
“Romancino et al. (2013) have suggested that ELV-MB and ELV-MT may have different origins and that ELVs from MT would be produced mainly through the budding of the plasma membrane.”
From Skeletal Muscle-Released Extracellular Vesicles: State of the Art (2019) · cites this paper as Romancino et al., 2013
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Isolation and Characterization of Exosomes from Cell Culture Supernatants and Biological Fluids
Théry, C., Amigorena, S., Raposo, G., & Clayton, A. (2006) · Current Protocols in Cell Biology · doi:10.1002/0471143030.cb0322s30 · Cited by 5,766 · see citing works
Exosomes – vesicular carriers for intercellular communication
Simons, M., & Raposo, G. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.03.007 · Cited by 2,351 · see citing works
Syndecan–syntenin–ALIX regulates the biogenesis of exosomes
Baietti, M. F., Zhang, Z., Mortier, E., Melchior, A., Degeest, G., Geeraerts, A., Ivarsson, Y., Depoortere, F., Coomans, C., Vermeiren, E., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2502 · Cited by 1,899 · see citing works
Shedding microvesicles: artefacts no more
Cocucci, E., Racchetti, G., & Meldolesi, J. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.11.003 · Cited by 1,742 · see citing works
Vesiclepedia: A Compendium for Extracellular Vesicles with Continuous Community Annotation
Kalra, H., Simpson, R. J., Ji, H., Aikawa, E., Altevogt, P., Askenase, P., Bond, V. C., Borràs, F. E., Breakefield, X., Budnik, V., et al. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001450 · Cited by 1,367 · see citing works
Exosome Secretion: Molecular Mechanisms and Roles in Immune Responses
Bobrie, A., Colombo, M., Raposo, G., & Théry, C. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01225.x · Cited by 1,102 · see citing works
Role of LBPA and Alix in Multivesicular Liposome Formation and Endosome Organization
Matsuo, H., Chevallier, J., Mayran, N., Le Blanc, I., Ferguson, C., Fauré, J., Blanc, N. S., Matile, S., Dubochet, J., Sadoul, R., et al. (2004) · Science · doi:10.1126/science.1092425 · Cited by 705 · see citing works
Gould, S. J., Booth, A. M., & Hildreth, J. E. K. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1831413100 · Cited by 638 · see citing works
Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane
Booth, A. M., Fang, Y., Fallon, J. K., Yang, J.-M., Hildreth, J. E. K., & Gould, S. J. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200508014 · Cited by 562 · see citing works
HIV Nef is Secreted in Exosomes and Triggers Apoptosis in Bystander CD4+ T Cells
Lenassi, M., Cagney, G., Liao, M., Vaupotič, T., Bartholomeeusen, K., Cheng, Y., Krogan, N. J., Plemenitaš, A., & Peterlin, B. M. (2009) · Traffic · doi:10.1111/j.1600-0854.2009.01006.x · Cited by 542 · see citing works
Tauro, B. J., Greening, D. W., Mathias, R. A., Mathivanan, S., Ji, H. L., & Simpson, R. J. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m112.021303 · Cited by 446 · see citing works
Higher-Order Oligomerization Targets Plasma Membrane Proteins and HIV Gag to Exosomes
Fang, Y., Wu, N., Gan, X., Yan, W., Morrell, J. C., & Gould, S. J. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050158 · Cited by 382 · see citing works
C2C12 myoblasts release micro-vesicles containing mtDNA and proteins involved in signal transduction
Guescini, M., Guidolin, D., Vallorani, L., Casadei, L., Gioacchini, A. M., Tibollo, P., Battistelli, M., Falcieri, E., Battistin, L., Agnati, L. F., et al. (2010) · Experimental Cell Research · doi:10.1016/j.yexcr.2010.04.006 · Cited by 294 · cited 1× · see citing works
“Recently, it has also been reported that a skeletal muscle cell line (C2C12) can release vesicles [4]; however, how muscle cells generate these vesicles and what their effectors are remain largely unknown.”
Protein Targeting to Exosomes/Microvesicles by Plasma Membrane Anchors
Shen, B., Wu, N., Yang, J.-M., & Gould, S. J. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.208660 · Cited by 283 · see citing works
The multiple personalities of Alix
Odorizzi, G. (2006) · Journal of Cell Science · doi:10.1242/jcs.03072 · Cited by 184 · see citing works
Structural Basis for Endosomal Targeting by the Bro1 Domain
Kim, J., Sitaraman, S., Hierro, A., Beach, B. M., Odorizzi, G., & Hurley, J. H. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.04.001 · Cited by 174 · see citing works
Alix regulates cortical actin and the spatial distribution of endosomes
Cabezas, A., Bache, K. G., Brech, A., & Stenmark, H. (2005) · Journal of Cell Science · doi:10.1242/jcs.02382 · Cited by 113 · see citing works
Ozz-E3, A Muscle-Specific Ubiquitin Ligase, Regulates β-Catenin Degradation during Myogenesis
Nastasi, T., Bongiovanni, A., Campos, Y., Männ, L., Toy, J. N., Bostrom, J., Rottier, R. J., Hahn, C. N., Conaway, J. W., Harris, A., et al. (2004) · Developmental Cell · doi:10.1016/s1534-5807(04)00020-6 · Cited by 91 · see citing works
Self-citationAlix Protein Is Substrate of Ozz-E3 Ligase and Modulates Actin Remodeling in Skeletal Muscle
Bongiovanni, A., Romancino, D. P., Campos, Y., Paterniti, G., Qiu, X., Moshiach, S., Felice, V. D., Vergani, N., Üstek, D., & d’Azzo, A. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.297036 · Cited by 35 · see citing works
Self-citationOzz-E3 Ubiquitin Ligase Targets Sarcomeric Embryonic Myosin Heavy Chain during Muscle Development
Campos, Y., Qiu, X., Zanoteli, E., Moshiach, S., Vergani, N., Bongiovanni, A., Harris, A., & d’Azzo, A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009866 · Cited by 28 · see citing works
Self-citationMembrane Curvature: The Power of Bananas, Zeppelins and Boomerangs
Cory, G. O. C., & Cullen, P. J. (2007) · Current Biology · doi:10.1016/j.cub.2007.04.015 · Cited by 17 · see citing works
Raiborg, C., & Stenmark, H. (2011) · Science · doi:10.1126/science.1204208 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Théry, C., Witwer, K. W., Aikawa, E., Alcaraz, M. J., Anderson, J. D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., Atkin‐Smith, G. K., et al. (2018) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2018.1535750 · Cited by 11,099 · see citing works
Self-citationBiogenesis, Secretion, and Intercellular Interactions of Exosomes and Other Extracellular Vesicles
Colombo, M., Raposo, G., & Théry, C. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101512-122326 · Cited by 6,186 · see citing works
Biogenesis and secretion of exosomes
Kowal, J., Tkach, M., & Théry, C. (2014) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2014.05.004 · Cited by 1,781 · see citing works
The role of extracellular vesicles in skeletal muscle and systematic adaptation to exercise
Vechetti, I. J., Valentino, T., Mobley, C. B., & McCarthy, J. J. (2021) · The Journal of Physiology · doi:10.1113/jp278929 · Cited by 141 · see citing works
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
Systemic Nutrient and Stress Signaling via Myokines and Myometabolites
Rai, M., & Demontis, F. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021115-105305 · Cited by 123 · see citing works
Extracellular vesicles as personalized medicine
Beetler, D. J., Di Florio, D. N., Bruno, K. A., Ikezu, T., March, K. L., Cooper, L. T., Wolfram, J., & Fairweather, D. (2023) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2022.101155 · Cited by 101 · see citing works
Barone, R., Macaluso, F., Sangiorgi, C., Campanella, C., Marino Gammazza, A., Moresi, V., Coletti, D., Conway de Macario, E., Macario, A. J., Cappello, F., et al. (2016) · Scientific Reports · doi:10.1038/srep19781 · Cited by 86 · see citing works
De Gasperi, R., Hamidi, S., Harlow, L. M., Ksiezak-Reding, H., Bauman, W. A., & Cardozo, C. P. (2017) · Scientific Reports · doi:10.1038/s41598-017-13105-9 · Cited by 75 · see citing works
Guescini, M., Maggio, S., Ceccaroli, P., Battistelli, M., Annibalini, G., Piccoli, G., Sestili, P., & Stocchi, V. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18112488 · Cited by 59 · see citing works
Mantile, F., Kisovec, M., Adamo, G., Romancino, D. P., Hočevar, M., Božič, D., Bedina Zavec, A., Podobnik, M., Stoppelli, M. P., Kisslinger, A., et al. (2022) · Cancers · doi:10.3390/cancers14153700 · Cited by 18 · see citing works
Self-citation
- Authors
- Romancino, D. P., Paterniti, G., Campos, Y., De Luca, A., Di Felice, V., d'Azzo, A., & Bongiovanni, A.
- Affiliations
- Istituto di Biomedicina e di Immunologia Molecolare Alberto Monroy (IT)
- St. Jude Children's Research Hospital (US)
- Department of Experimental Biomedicine and Clinical Neurosciences (BIONEC), University of Palermo, Italy
- Department of Genetics, St. Jude Children's Research Hospital, Memphis, USA
- Corresponding author
- Bongiovanni, Antonella
- Venue
- FEBS Letters
- Publisher
- Wiley
- Published
- 2013-03-20
- Volume
- 587
- Issue
- 9
- Pages
- 1379-1384
- ISSN
- 0014-5793 (ISSN-L)
- 1873-3468
- PMC
- PMC4714929
- OpenAlex
- W2004252622
- Cited by
- 120
- References
- 22
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 6 · 2023: 8 · 2022: 19 · 2021: 18 · 2020: 12 · 2019: 12 · 2018: 7 · 2017: 11 · 2016: 4 · 2015: 7 · 2014: 5
- FWCI
- 2.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- FEBS Letters (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Nova Science Publishers (Nova Science Publishers, Inc.) (submittedVersion, other-oa)
- Funders
- American Lebanese Syrian Associated Charities (CA021765)
- National Institutes of Health (CA 021765)
- National Cancer Institute (CA021765, P30CA021765)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR049867, R01AR049867)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
- Keywords
- exosomes, muscle cells, myogenesis, Alix, vesicle biogenesis, extracellular vesicles, cell-to-cell signaling, membrane vesicles
- MeSH terms
- Animals, Calcium-Binding Proteins, Cell Differentiation, Cell Line, Cell Membrane, Muscle Cells, Nanostructures, Mice, Exosomes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
