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C2C12 myoblasts release micro-vesicles containing mtDNA and proteins involved in signal transduction
Abstract
Micro-vesicles can be released by different cell types and operate as 'safe containers' mediating inter-cellular communication. In this work we investigated whether cultured myoblasts could release exosomes. The reported data demonstrate, for the first time, that C2C12 myoblasts release micro-vesicles as shown by the presence of two exosome markers (Tsg101 and Alix proteins). Using real-time PCR analysis it was shown that these micro-vesicles, like other cell types, carry mtDNA. Proteomic characterization of the released micro-vesicle contents showed the presence of many proteins involved in signal transduction. The bioinformatics assessment of the Disorder Index and Aggregation Index of these proteins suggested that C2C12 micro-vesicles mainly deliver the machinery for signal transduction to target cells rather than key proteins involved in hub functions in molecular networks. The presence of IGFBP-5 in the purified micro-vesicles represents an exception, since this binding protein can play a key role in the modulation of the IGF-1 signalling pathway. In conclusion, the present findings demonstrate that skeletal muscle cells release micro-vesicles, which probably have an important role in the communication processes within skeletal muscles and between skeletal muscles and other organs. In particular, the present findings suggest possible new diagnostic approaches to skeletal muscle diseases.
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“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 Guescini et al., 2010
In the citing paper
“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 Guescini et al., 2010
In the citing paper
“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 Guescini et al., 2010
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Rocha, K. C. E., Ying, W., & Olefsky, J. M. (2024) · Annual Review of Physiology · doi:10.1146/annurev-physiol-042222-024535 · Cited by 103
Extracellular Vesicles as Nanotherapeutics for Parkinson’s Disease
Leggio, L., Paternò, G., Vivarelli, S., L’Episcopo, F., Tirolo, C., Raciti, G., Pappalardo, F., Giachino, C., Caniglia, S., Serapide, M. F., et al. (2020) · Biomolecules · doi:10.3390/biom10091327 · Cited by 100
“In particular, EVs contain nucleic acids, both DNA (chromosomal or mitochondrial) [41,42] and RNAs (mRNAs, small ncRNAs, such as microRNAs etc.”
BackgroundMicrofluidics for detection of exosomes and microRNAs in cancer: State of the art
Mousavi, S. M., Mahdian, S. M. A., Ebrahimi, M. S., Taghizadieh, M., Vosough, M., Nahand, J. S., Hosseindoost, S., Vousooghi, N., Javar, H. A., Larijani, B. A., et al. (2022) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2022.04.011 · Cited by 100
“Recent studies have demonstrated that exosomes can also transmit mitochondrial and chromosomal DNA between different cell types.(73) Genetic materials, such as RNA and DNA molecules, can be transferred between neighboring or distant cells via exosomes.”
BackgroundExosomes and Extracellular RNA in Muscle and Bone Aging and Crosstalk
Qin, W., & Dallas, S. L. (2019) · Current Osteoporosis Reports · doi:10.1007/s11914-019-00537-7 · Cited by 99
Mitochondrial and metabolic alterations in cancer cells
Gregorio, J. D., Petricca, S., Iorio, R., Toniato, E., & Flati, V. (2022) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2022.151225 · Cited by 97
Functional transferred DNA within extracellular vesicles
Cai, J., Wu, G., José, P. A., & Zeng, C. (2016) · Experimental Cell Research · doi:10.1016/j.yexcr.2016.10.012 · Cited by 95
“provide evidence that glioblastoma, astrocyte, and myoblast cells release EVs, which carry mtDNA [28,29].”
Interorganelle Communication between Mitochondria and the Endolysosomal System
Soto‐Heredero, G., Baixauli, F., & Mittelbrunn, M. (2017) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2017.00095 · Cited by 98
“Exosomes contain genetic material, mostly non-coding RNA, but also mtDNA (Guescini et al., 2010a,b) (Figure 2).”
BackgroundEffects of exercise on exosome release and cargo in in vivo and ex vivo models: A systematic review
Estébanez, B., Jiménez‐Pavón, D., Huang, C., Cuevas, M. J., & González‐Gallego, J. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.30094 · Cited by 94
“Regardless of the sample sizes in both studies (n = 9 and n = 18), the different technique, SEC (Lovett et al., 2018) versus ultracentrifugation (Guescini et al., 2010) were utilized to isolate exosomes.”
BackgroundMethodResultMitochondrial oxidative phosphorylation in cutaneous melanoma
Kumar, P. R., Moore, J. A., Bowles, K. M., Rushworth, S. A., & Moncrieff, M. D. (2020) · British Journal of Cancer · doi:10.1038/s41416-020-01159-y · Cited by 92
Exosomes: the ideal nanovectors for biodelivery
Fais, S., Logozzi, M., Lugini, L., Federici, C., Azzarito, T., Zarovni, N., & Chiesi, A. (2012) · Biological Chemistry · doi:10.1515/hsz-2012-0236 · Cited by 90
Non-coding RNAs in Exosomes: New Players in Cancer Biology
Silva, M. G., & Melo, S. A. (2015) · Current Genomics · doi:10.2174/1389202916666150707154719 · Cited by 86
Hogan, S. E., Rodriguez, M. P., Cheadle, J. B., Glenn, R. A., Medrano, C., Petersen, T. H., & Ilagan, R. M. (2019) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00058.2018 · Cited by 83
“We and others have shown that exosomes contain mitochondrial proteins, mtDNA, and mitochondrial genes (19, 30, 62).”
BackgroundAnnibalini, G., Lucertini, F., Agostini, D., Vallorani, L., Gioacchini, A. M., Barbieri, E., Guescini, M., Casadei, L., Passalia, A., Sal, M. D., et al. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/3937842 · Cited by 89
Guescini, M., Leo, G., Genedani, S., Carone, C., Pederzoli, F., Ciruela, F., Guidolin, D., Stocchi, V., Mantuano, M., Borroto‐Escuela, D. O., et al. (2012) · Experimental Cell Research · doi:10.1016/j.yexcr.2012.01.005 · Cited by 80
“[44] M.”
BackgroundThe Pleiotropic Effect of Physical Exercise on Mitochondrial Dynamics in Aging Skeletal Muscle
Barbieri, E., Agostini, D., Polidori, E., Potenza, L., Guescini, M., Lucertini, F., Annibalini, G., Stocchi, L., Santi, M. D., & Stocchi, V. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/917085 · Cited by 82
“Therefore, muscle cell changes associated with endocrine alterations andmitochondrial dysfunction require further attention.”
BackgroundWatanabe, S., Sudo, Y., Makino, T., Kimura, S., Tomita, K., Noguchi, M., Sakurai, H., Shimizu, M., Takahashi, Y., Sato, R., et al. (2022) · PNAS Nexus · doi:10.1093/pnasnexus/pgac173 · Cited by 81
“Although previous papers identified specific proteins as markers of SkM-EVs (ITGA7 (13) and SPARC (20)), the potential of SkM-EVs proteins to follow their trafficking in vivo has been poorly explored.”
BackgroundTumor-Derived Exosomes in Tumor-Induced Immune Suppression
Hao, Q., Wu, Y., Wu, Y., Wang, P., & Vadgama, J. V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031461 · Cited by 83
“Mitochondrial DNA (mtDNA) [71,72], single-stranded DNA (ssDNA) [73], and double-stranded DNA (dsDNA) [45,74,75] have been found in TEX.”
BackgroundNative and Bioengineered Exosomes for Ischemic Stroke Therapy
Khan, H. L., Pan, J., Li, Y.-F., Zhang, Z., & Yang, G. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.619565 · Cited by 79
Barbieri, E., Battistelli, M., Casadei, L., Vallorani, L., Piccoli, G., Guescini, M., Gioacchini, A. M., Polidori, E., Zeppa, S. D., Ceccaroli, P., et al. (2011) · Journal of Aging Research · doi:10.4061/2011/845379 · Cited by 78
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
Mesothelial-to-Mesenchymal Transition and Exosomes in Peritoneal Metastasis of Ovarian Cancer
Pascual‐Antón, L., Cardeñes, B., de la Cuesta, R. S., González‐Cortijo, L., López‐Cabrera, M., Cabañas, C., & Sandoval, P. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111496 · Cited by 74
“Moreover, single and double-stranded DNA [38], as well as mitochondrial DNA, are also contained in exosomes [39,40].”
BackgroundNew Perspectives on the Importance of Cell-Free DNA Biology
Bronkhorst, A. J., Ungerer, V., Oberhofer, A., Gabriel, S., Polatoglou, E., Randeu, H., Uhlig, C., Pfister, H., Mayer, Z., & Holdenrieder, S. (2022) · Diagnostics · doi:10.3390/diagnostics12092147 · Cited by 78
Genetically Engineered Cellular Membrane Vesicles as Tailorable Shells for Therapeutics
Ren, E., Liu, C., Lv, P., Wang, J., & Liu, G. (2021) · Advanced Science · doi:10.1002/advs.202100460 · Cited by 70
Bonito, P. D., Chiozzini, C., Arenaccio, C., Anticoli, S., Manfredi, F., Olivetta, E., Ferrantelli, F., Falcone, E., Ruggieri, A., & Federico, M. (2017) · International Journal of Nanomedicine · doi:10.2147/ijn.s131309 · Cited by 71
Karnas, E., Dudek, P., & Zuba‐Surma, E. K. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1120175 · Cited by 74
Standardization Approaches for Extracellular Vesicle Loading with Oligonucleotides and Biologics
Roerig, J., & Schulz‐Siegmund, M. (2023) · Small · doi:10.1002/smll.202301763 · Cited by 67
17β-Estradiol and testosterone in sarcopenia: Role of satellite cells
la Colla, A. B., Pronsato, L., Milanesi, L. M., & Vasconsuelo, A. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.07.011 · Cited by 73
“…by every cell type that has been examined, including tumour cells, reticulocytes, epithelial cells, neurons, muscle cells and Schwann cells (Guescini et al., 2010; LopezVerrilli et al., 2012; Smalheiser et al., 2007), and that they are found in most biological fluids (Simpson et al., 2008).”
Muscle cell communication in development and repair
Demonbreun, A. R., & McNally, E. M. (2017) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2017.03.008 · Cited by 64
“Proteins identified in exosomes derived from myoblasts and myotubes include myoferlin, annexins and the EHD proteins [41,48].”
Madison, R. D., McGee, C. A., Rawson, R., & Robinson, G. A. (2014) · Journal of Extracellular Vesicles · doi:10.3402/jev.v3.22865 · Cited by 64
“Recent reports have also suggested that this cell line, like most cell lines, secretes extracellular vesicles into the culture media (24).”
BackgroundExosomes: Nanocarriers of Biological Messages
Conigliaro, A., Fontana, S., Raimondo, S., & Alessandro, R. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-4397-0_2 · Cited by 63
“Authors finally speculated that mtDNA, shuttled among cells, could have physiological relevance in restoring the proper mtDNA or, conversely, favoring the spread of pathological phenotypes, such as skeletal muscle diseases [115].”
BackgroundDystrophin deficiency leads to disturbance of LAMP1-vesicle-associated protein secretion
Duguez, S., Duddy, W. J., Johnston, H., Lainé, J., Bihan, M. L., Brown, K. J., Bigot, A., Hathout, Y., Butler-Browne, G. S., & Partridge, T. A. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1248-2 · Cited by 60
“Secreted vesicles of various sizes and origins have been observed in tumor cells, endothelial cells, and immune response cells [45–48].”
BackgroundGuescini, 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
“Our and other reports opened up the possibility that EVs convey signalling molecules allowing for intercellular regulation of gene expression [5,25,36].”
BackgroundResultPneumolysin induced mitochondrial dysfunction leads to release of mitochondrial DNA
Nerlich, A. G., Mieth, M., Letsiou, E., Fatykhova, D., Zscheppang, K., Imai‐Matsushima, A., Meyer, T. F., Paasch, L., Mitchell, T. J., Tönnies, M., et al. (2018) · Scientific Reports · doi:10.1038/s41598-017-18468-7 · Cited by 61
Salivary Extracellular Vesicle-Associated exRNA as Cancer Biomarker
Chiabotto, G., Gai, C., Deregibus, M. C., & Camussi, G. (2019) · Cancers · doi:10.3390/cancers11070891 · Cited by 60
“Some studies indicate that genetic materials encapsulated in EV include mitochondrial [24,42] and genomic [22] DNAs.”
BackgroundVarela-Eirín, M., Varela-Vázquez, A., Mateos, M. R.-C., Vila‐Sanjurjo, A., Fonseca, E., Mascarenas, J. L., Vázquez, M. E., & Mayán, M. D. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2017.02.001 · Cited by 56
“In addition, mitochondrial DNA (mtDNA) has been found in the exosomes of astrocytes, myoblasts and glioblastoma cells [29-31].”
BackgroundRole of extracellular vesicles in stem cell biology
Bruno, S., Chiabotto, G., Favaro, E., Deregibus, M. C., & Camussi, G. (2019) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00129.2019 · Cited by 58
“In some cases, genomic (7) and mitochondrial (64, 65) DNAs have been found.”
Roles of Skeletal Muscle-Derived Exosomes in Organ Metabolic and Immunological Communication
Aoi, W., & Tanimura, Y. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.697204 · Cited by 57
“Interestingly, mitochondrial DNA was also shown to be taken up into exosomes and released into the extracellular medium in cultures of C2C12 cells (7).”
Background
Metadata
- Authors
- Guescini, M., Guidolin, D., Vallorani, L., Casadei, L., Gioacchini, A. M., Tibollo, P., Battistelli, M., Falcieri, E., Battistin, L., Agnati, L. F., & Stocchi, V.
- Affiliations
- University of Urbino (IT)
- University of Padua (IT)
- IRCCS San Camillo Hospital (IT)
- Corresponding author
- Guescini, M.
- Stocchi, V.
- ORCID
- Venue
- Experimental Cell Research
- Publisher
- Elsevier BV
- Published
- 2010-07
- Volume
- 316
- Issue
- 12
- Pages
- 1977-1984
- ISSN
- 0014-4827 (ISSN-L)
- OpenAlex
- W1981888677
- Cited by
- 294
- References
- 51
- Citations by year
- 2026: 2 · 2025: 16 · 2024: 21 · 2023: 33 · 2022: 27 · 2021: 27 · 2020: 32 · 2019: 25 · 2018: 9 · 2017: 29 · 2016: 14 · 2015: 20 · 2014: 17 · 2013: 12 · 2012: 5
- FWCI
- 2.87
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Experimental Cell Research (publishedVersion)
- PubMed (publishedVersion)
- CINECA IRIS Institutional Research information system (University of Urbino) (submittedVersion)
- Padua Research Archive (University of Padova) (submittedVersion)
- 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 › Cell Biology › Caveolin-1 and cellular processes
- Keywords
- exosomes, C2C12 myoblasts, mitochondrial DNA, signal transduction proteins, TSG101, Alix, IGFBP-5, IGF-1 signaling, intercellular communication, skeletal muscle, exosomal proteome, skeletal muscle disorders
- MeSH terms
- Tsg101 Protein, Animals, Calcium-Binding Proteins, Cells, Cultured, DNA-Binding Proteins, DNA, Mitochondrial, Insulin-Like Growth Factor I, Transcription Factors, Signal Transduction, Insulin-Like Growth Factor Binding Protein 5, Myoblasts, Skeletal, Microscopy, Electron, Transmission, Mice, Endosomal Sorting Complexes Required for Transport
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