The DOI matches its Crossref record; 49 of the 51 references it cites were found in a registry or an index.
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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THIS ARTICLE HAS BEEN RETRACTED Exercise induces interleukin‐8 expression in human skeletal muscle
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“Exosomes secreted from skeletal muscle, visceral adipose tissue, and hepatocytes can transfer functional proteins and RNA species that regulate the metabolic function of adjacent cells as well as remote tissues [34,35].”
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“Multiple cell types have been demonstrated to release vesicles into the extracellular medium, including mesenchymal cells, adipocytes, fibroblasts, immune cells, platelets, myoblasts and tumor cells (7-16).”
In vitro models of exosome biology and toxicology: New frontiers in biomedical research
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“In addition to RNA, genomic and mitochondrial DNA are also found in exosomes (Guescini et al., 2010; Thakur et al., 2014).”
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Smolina, N., Khudiakov, A. A., Knyazeva, A., Zlotina, A. M., Сухарева, К. С., Кондратов, К. А., Gogvadze, V. G., Zhivotovsky, B., Sejersen, T., & Kostareva, A. A. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.165745 · Cited by 44
Extracellular Vesicles in Oncology: from Immune Suppression to Immunotherapy
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“[52] Guescini M, Guidolin D, Vallorani L, Casadei L, Gioacchini AM, Tibollo P, et al.”
BackgroundCharacterization of nucleic acids from extracellular vesicle-enriched human sweat
Bart, G., Fischer, D., Samoylenko, A., Zhyvolozhnyi, A., Stehantsev, P., Miinalainen, I., Kaakinen, M., Nurmi, T., Singh, P., Harju-Baker, S., et al. (2021) · BMC Genomics · doi:10.1186/s12864-021-07733-9 · Cited by 44
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“In addition, our group demonstrated that muscle cells release EVs both in vitro [18] and in vivo [17].”
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Ofir‐Birin, Y., Heidenreich, M., & Regev‐Rudzki, N. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.03.004 · Cited by 41
“Interestingly, recent EVs studies in humans demonstrated that exosomal DNA represents the entire nuclear [51, 52] and mitochondrial [53, 54] genomes.”
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Exosomes and microRNAs as mediators of the exercise
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“The pioneering discovery made by Guescini et al. was a major breakthrough, as it was the first demonstration of skeletal muscle cells producing extracellular vesicles, including exosomes [175].”
Redox proteins are constitutively secreted by skeletal muscle
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Storci, G., Carolis, S. D., Olivieri, F., & Bonafè, M. (2018) · Seminars in Immunology · doi:10.1016/j.smim.2018.08.003 · Cited by 37
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Salivary Extracellular Vesicles: Biomarkers and Beyond in Human Diseases
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“Numerous studies have highlighted the potential of molecules in sEVs as promising biomarkers for various diseases.”
BackgroundDetection of DNA methylation of gastric juice-derived exosomes in gastric cancer
Yamamoto, H. (2014) · Integrative Molecular Medicine · doi:10.15761/imm.1000105 · Cited by 34
“GC is a heterogeneous disease with multiple environmental etiologies and alternative carcinogenic pathways [26].”
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“The findings that muscle cells release in vitro [83] and in vivo [84] exosomes containing miRNAs [84,85] are in agreement with the idea that EV-miRNAs can function as signaling molecules at the NMJ.”
ResultAnticoli, S., Aricò, E., Arenaccio, C., Manfredi, F., Chiozzini, C., Olivetta, E., Ferrantelli, F., Lattanzi, L., D’Urso, M. T., Proietti, E., et al. (2017) · Journal of Molecular Medicine · doi:10.1007/s00109-017-1617-2 · Cited by 34
“Exosomes are nanovesicles released by basically all eukaryotic cells, including muscle cells [3, 4].”
BackgroundMuscle and Adipose Tissue Communicate with Extracellular Vesicles
Rome, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137052 · Cited by 33
“In addition to RNA, the presence of mitochondrial DNA has been found in EVs released in vitro from differentiated murine yotubes [23] and from adipocytes [24].”
BackgroundMitochondrial Extracellular Vesicles: A Promising Avenue for Diagnosing and Treating Lung Diseases
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Extracellular Vesicles in Type 1 Diabetes: A Versatile Tool
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“detectable in body fluids including plasma, in which it is contained in extracellular vesicles (EVs) (Guescini et al., 2010; Meddeb et al., 2019; Thurairajah et al., 2018).”
BackgroundMiro proteins connect mitochondrial function and intercellular transport
Nahácka, Z., Zobalová, R., Dubisova, M., Rohlena, J., & Neužil, J. (2021) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2021.1925216 · Cited by 30
“However, genomic and mitochondrial DNA (mtDNA) have also been detected in these vesicles (Guescini et al. 2010a; Guescini et al. 2010b; Kahlert et al. 2014; Thakur et al. 2014).”
BackgroundSudakov, N. P., Popkova, T. P., Katyshev, A. I., Гольдберг, О. А., Nikiforov, S. B., Пушкарев, Б. Г., Клименков, И. В., Lepekhova, S. A., Апарцин, К. А., Nevinsky, G. A., et al. (2015) · Biochemistry (Moscow) · doi:10.1134/s000629791510020x · Cited by 27
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“Guescini et al. demonstrated that also skeletal muscle cells release small vesicles of 50–80 nm in diameter: they carry mitochondrial DNA (mtDNA) and signaling proteins, and regulate the communication processes within skeletal muscles and between skeletal muscles and other organs [19].”
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BackgroundMelatonin behavior in restoring chemical damaged C2C12 myoblasts
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Diversity of Intercellular Communication Modes: A Cancer Biology Perspective
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“, 2014), mitochondrial DNAs (mtDNAs) (Guescini et al., 2010), and single-stranded DNAs (ssDNAs) (Balaj et al.”
Mas‐Bargues, C., Sanz‐Ros, J., Romero-García, N., Huete-Acevedo, J., Dromant, M., & Borrás, C. (2023) · Redox Biology · doi:10.1016/j.redox.2023.102668 · Cited by 25
Aas, V., Øvstebø, R., Brusletto, B. S., Aspelin, T., Trøseid, A. S., Qureshi, S., Eid, D. S. O., Olstad, O. K., Nyman, T. A., & Haug, K. B. F. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1143966 · Cited by 25
“EVs have been isolated and characterized from murine skeletal muscle cells (C2C12 cells) (Guescini et al., 2010) and primary human myoblasts and myotubes (Le Bihan et al.”
BackgroundHanson, B., Vorobieva, I., Zheng, W., Conceição, M., Lomonosova, Y. N., Mäger, I., Puri, P., Andaloussi, S. E., Wood, M. J. A., & Roberts, T. C. (2023) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2023.07.005 · Cited by 24
The mesmiRizing complexity of microRNAs for striated muscle tissue engineering
Quattrocelli, M., & Sampaolesi, M. (2015) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.04.011 · Cited by 24
Non-canonical retinoid signaling in neural development, regeneration and synaptic function
Piazza, A., Carlone, R. L., & Spencer, G. E. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1371135 · Cited by 24
The Relationship between Exosomes and Cancer: Implications for Diagnostics and Therapeutics
Weston, W. W., Ganey, T. M., & Temple, H. T. (2019) · BioDrugs · doi:10.1007/s40259-019-00338-5 · Cited by 24
Lombardo, M., Aiello, G., Fratantonio, D., Karav, S., & Baldelli, S. (2024) · Nutrients · doi:10.3390/nu16183097 · Cited by 24
“…development, including insulin-like growth factor-1 (IGF-1), TGF-β 3, vascular endothelial growth factor, and fibroblast growth factor 2 (FGF2) [45]. essential factors for muscle development, including insulin-like growth factor-1 (IGF-1) TGF-β 3, vascular endothelial growth factor, and…”
BackgroundWang, M., Wang, W., Chopp, M., Zhang, Z. G., & Zhang, Y. (2025) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x251338971 · Cited by 26
“29 EV-mt-DNA transfer as a pathogenic factor in disease Due to the absence of histone protection and direct exposure to ROS, mt-DNA is more prone to mutations nuclear DNA.”
Fernández‐Rhodes, M., Adlou, B., Williams, S., Lees, R., Peacock, B., Aubert, D., Jalal, A. R., Lewis, M. P., & Davies, O. G. (2023) · Journal of Extracellular Biology · doi:10.1002/jex2.85 · Cited by 22
“Historically, EVs were first isolated in SM studies from undifferentiated C2C12 cells by Guescini et al., who predicted their role in the modulation of IGF-1 signalling and intra-and inter-organ communication through proteomic analysis (Guescini et al., 2010).”
BackgroundMethodInfluentialEpigenetic Reprogramming of Muscle Progenitors: Inspiration for Clinical Therapies
Consalvi, S., Sandonà, M., & Saccone, V. (2015) · Stem Cells International · doi:10.1155/2016/6093601 · Cited by 21
“However several studies reporting muscle-exosomes are emerging [98–100].”
Emerging role of extracellular vesicles in the regulation of skeletal muscle adaptation
Vechetti, I. J. (2019) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00914.2018 · Cited by 21
Agnati, L. F., Guidolin, D., Leo, G., Guescini, M., Pizzi, M., Stocchi, V., Spano, P., Ghidoni, R., Ciruela, F., Genedani, S., et al. (2011) · Journal of Receptors and Signal Transduction · doi:10.3109/10799893.2011.599393 · Cited by 20
“Furthermore, as shown below, data will be here reported showing that at least some components of signalosomes (in particular GPCRs) can be transferred from cell to cell thanks to the roamer-type of VT (10,73,74).”
BackgroundConkright, W. R., Beckner, M. E., Sahu, A., Mi, Q., Clemens, Z. J., Lovalekar, M. T., Flanagan, S. D., Martin, B. J., Ferrarelli, F., Ambrosio, F., et al. (2022) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00664.2021 · Cited by 20
Seewald, L. A., Sabino, I., Montney, K. L., & Delco, M. L. (2023) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2023.03.013 · Cited by 19
Murata, A., Akiyama, H., Honda, H., & Shimizu, K. (2023) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2023.06.054 · Cited by 19
Bolumar, D., Moncayo, J., González-Fernández, J., Ochando, A., Moreno, I., Monteagudo, A., Marin, C., Diez, A., Fabra, P., Checa, M. Á., et al. (2023) · eLife · doi:10.7554/elife.88008 · Cited by 19
Vann, C. G., Zhang, X., Khodabukus, A., Orenduff, M. C., Chen, Y., Corcoran, D. L., Truskey, G. A., Bursac, N., & Kraus, V. B. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.937899 · Cited by 18
“Importantly, emerging research in muscle-derived extracellular vesicles (EVs), which carry proteins, lipids, mRNAs and microRNAs (miRs), has provided further insight into mechanisms of crosstalk between muscle and other tissues (Guescini et al., 2010; Forterre et al., 2014; Yoon et al., 2014; Rome et al., 2019).”
BackgroundNext Stage Approach to Tissue Engineering Skeletal Muscle
Reid, G., Magarotto, F., Marsano, A., & Pozzobon, M. (2020) · Bioengineering · doi:10.3390/bioengineering7040118 · Cited by 18
Sutton, E. R., & Pekovic‐Vaughan, V. (2025) · Antioxidants · doi:10.3390/antiox14091132 · Cited by 20
“Mitochondrial DNA was found to be taken up into exosomes and released into extracellular medium of C2C12 cell cultures [23].”
MiRNAs: A Powerful Tool in Deciphering Gynecological Malignancies
Duică, F., Condrat, C. E., Dănilă, C. A., Boboc, A. E., Radu, M. R., Xiao, J., Li, X., Creţoiu, S. M., Suciu, N., Crețoiu, D., et al. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.591181 · Cited by 17
“miRNAs are small non-coding RNA molecules that function as post-transcriptional regulators of gene expressions (5, 22, 23).”
BackgroundAn Exploration of Molecular Correlates Relevant to Radiation Combined Skin-Burn Trauma
Islam, A., Ghimbovschi, S. D., Zhai, M., & Swift, J. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134827 · Cited by 17
“Alix, Resistin, and TSG101 serum exosome protein markers [16,17] were detected using mouse primary anti– Alix,–Resistin, and–TSG101 antibodies (Santa Cruz Biotechnology Inc.”
MethodBydak, B., Pierdoná, T. M., Seif, S., Sidhom, K., Obi, P. O., Labouta, H. I., Gordon, J. W., & Saleem, A. (2022) · Membranes · doi:10.3390/membranes12050464 · Cited by 15
“2 μm filtration have reported average myoblast-EV size ranges between 50 and 100 nm [63,64].”
BackgroundMethodNon-bone-derived exosomes: a new perspective on regulators of bone homeostasis
Wang, P., Shao, W., Li, Z., Wang, B., Lv, X., Huang, Y., & Feng, Y. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-023-01431-7 · Cited by 19
“In 2010, Guescini et al. first reported the production of exosomes by C2C12 myoblasts [185], and subsequent studies demonstrated that exosomes derived from C2C12 myoblasts can activate the β-catenin pathway through miR-27a-3p, thereby promoting osteogenic differentiation of MC3T3-E1 cells [186].”
BackgroundIn situ hybridization to detect DNA amplification in extracellular vesicles
Casadei, L., Sarchet, P., de Faria, F. C. C., Calore, F., Nigita, G., Tahara, S., Cascione, L., Wabitsch, M., Hornicek, F. J., Grignol, V. P., et al. (2022) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12251 · Cited by 16
“MitochondrialDNAhas also been found in EVs (Guescini et al., 2010), and the effect of mtDNA transfer as an oncogenic signal has been investigated (Sansone et al.”
BackgroundHigh passage numbers induce resistance to apoptosis in C2C12 muscle cells
Pronsato, L., la Colla, A. B., Ronda, A. C., Milanesi, L. M., Boland, R., & Vasconsuelo, A. (2013) · Biocell · doi:10.32604/biocell.2013.37.001 · Cited by 15
“Since it has been shown that C2C12 cells are able to release micro-vesicles containing mtDNA (Guescini et al., 2010), we postulated that the loss of mtDNA in h-C2C12 cells could be consequence of the continuous release of microvesicles during passages.”
BackgroundInter-Cellular Transport of Ran GTPase
Khuperkar, D., Helen, M., Magre, I., & Joseph, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125506 · Cited by 15
Plasma mitochondrial DNA is associated with extrapulmonary sarcoidosis
Ryu, C., Brandsdorfer, C., Adams, T. S., Hu, B., Kelleher, D. W., Yaggi, M., Manning, E. P., Walia, A., Reeves, B. C., Pan, H., et al. (2019) · European Respiratory Journal · doi:10.1183/13993003.01762-2018 · Cited by 15
Characteristics and Changes of DNA in Extracellular Vesicles
Chang, X., Fang, L., Bai, J., & Wang, Z. (2020) · DNA and Cell Biology · doi:10.1089/dna.2019.5005 · Cited by 15
“Guescini et al. (2010) and Michele et al. (2010) indicated that mtDNA, besides dsDNA, were also contained in microvesicles released from C2C12 myoblast cells and in exosomes released from glioblastoma and astrocyte.”
Chen, X., Song, X., Li, J., Wang, J., Yan, Y., & Yang, F. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01640-8 · Cited by 14
“C2C12 myoblasts, an extensively studied skeletal muscle cell line [25, 26], can secrete EVs into the culture media [27–29].”
BackgroundThe Emergent Landscape of Detecting EGFR Mutations Using Circulating Tumor DNA in Lung Cancer
Huang, W.-L., Wei, F., Wong, D. T., Lin, C., & Su, W. (2015) · BioMed Research International · doi:10.1155/2015/340732 · Cited by 14
“Recent investigations provide further evidence that EVs carry not only proteins, mRNA, microRNA, mitochondrial DNA [12], and single-stranded DNA, but also large fragments (>10 kb) of double-stranded carrying mutated KRAS, p53 and EGFR sequences [13, 14].”
BackgroundMammes, A., Pasquier, J., Mammes, O., Conti, M., Douard, R., & Loric, S. (2021) · World Journal of Gastrointestinal Oncology · doi:10.4251/wjgo.v13.i11.1561 · Cited by 16
Therapeutic application of extracellular vesicles in acute and chronic renal injury
Rovira, J., Diekmann, F., Campistol, J. M., & Ramírez-Bajo, M. J. (2017) · Nefrología (English Edition) · doi:10.1016/j.nefroe.2017.03.004 · Cited by 14
Zhang, J., Gao, Y., & Yan, J. (2024) · Metabolites · doi:10.3390/metabo14020088 · Cited by 15
“Following the initial discovery of EV secretion by C2C12 myoblasts [126], subsequent studies have revealed that muscle cells at various developmental stages, including myotubes and muscle progenitors, also possess this capability.”
BackgroundUso terapéutico de las vesículas extracelulares en insuficiencia renal aguda y crónica
Rovira, J., Diekmann, F., Campistol, J. M., & Ramírez-Bajo, M. J. (2016) · Nefrología · doi:10.1016/j.nefro.2016.04.006 · Cited by 14
McGivney, B. A., Griffin, M. E., Gough, K. F., McGivney, C. L., Browne, J. A., Hill, E. W., & Katz, L. M. (2017) · BMC Veterinary Research · doi:10.1186/s12917-017-1277-z · Cited by 13
“It has been hypothesised that skeletal muscle may contribute to changes in differentially expressed (DE) ci-miRNAs in response to exercise training by releasing exosomes into plasma [15, 16], supporting the possibility that DE plasma ci-miRNAs could be used to assess adaptive training responses of skeletal muscle.”
BackgroundThe Role of Myokines in Liver Diseases
Nishikawa, H., Kim, S. K., & Asai, A. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26031043 · Cited by 12
The Role of Tumor-Derived Vesicles in the Regulation of Antitumor Immunity
Ukrainskaya, V. M., Rubtsov, Y. P., Knorre, V. D., Maschan, M. A., Gabibov, A. G., & Stepanov, A. V. (2019) · Acta Naturae · doi:10.32607/20758251-2019-11-4-33-41 · Cited by 12
Exosomes as intercellular communication messengers for cardiovascular and cerebrovascular diseases
Deftu, A. T., Radu, B. M., Crețoiu, D., Deftu, A., Creţoiu, S. M., & Xiao, J. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816053-4.00009-2 · Cited by 12
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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