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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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 Guescini et al., 2010
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 Guescini et al., 2010
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 Guescini et al., 2010
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“Recently, it has been demonstrated that muscle cells secrete nanoparticles with exosomal properties.(29,30) Because exosomes released from donor cells can be taken up by recipient cells, where an array of biological processes, including cell proliferation and differentiation, can be affected,(31,32) we examined whethe…”
BackgroundMalaria parasite DNA-harbouring vesicles activate cytosolic immune sensors
Sisquella, X., Ofir‐Birin, Y., Pimentel, M. A., Cheng, L., Karam, P. A., Sampaio, N. G., Penington, J. S., Connolly, D. J., Giladi, T., Scicluna, B. J., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-02083-1 · Cited by 192 · see citing works
Kucharzewska, P., & Belting, M. (2013) · Journal of Extracellular Vesicles · doi:10.3402/jev.v2i0.20304 · Cited by 183 · see citing works
“In addition, both exosomes and SMVs have been shown to enclose mitochondrial DNA (44,45).”
Aswad, H., Forterre, A., Wiklander, O. P. B., Vial, G., Danty-Berger, E., Jalabert, A., Lamazière, A., Meugnier, E., Pesenti, S., Ott, C., et al. (2014) · Diabetologia · doi:10.1007/s00125-014-3337-2 · Cited by 185 · see citing works
“Muscles of HP- and SD-fed mice were incubated ex vivo for 24 h in serum-free medium and exosomes released into the CM during this time period were extracted by filtration and ultracentrifugation [5, 14, 23] (ESM Fig.”
MethodDiscovery of Double-Stranded Genomic DNA in Circulating ExosomesPreprint
Kalluri, R., & LeBleu, V. S. (2016) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2016.81.030932 · Cited by 185 · see citing works
“Exosomes were reported to contain mitochondrial DNA (from culture supernatant of myoblasts [Guescini et al. 2010]) and chromosomal DNA (vide infra).”
BackgroundJalabert, A., Vial, G., Guay, C., Wiklander, O. P. B., Nordin, J. Z., Aswad, H., Forterre, A., Meugnier, E., Pesenti, S., Regazzi, R., et al. (2016) · Diabetologia · doi:10.1007/s00125-016-3882-y · Cited by 177 · see citing works
Forterre, A. V., Jalabert, A., Berger, E., Baudet, M., Chikh, K., Errazuriz-Cerda, E., Larichaudy, J. D., Chanon, S., Weiss‐Gayet, M., Hesse, A.-M., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0084153 · Cited by 176 · see citing works
“Among the 163 proteins previously identified in ELVs released from C2C12 myoblasts using a similar proteomic analysis [23], 71 were also included in our list of 334 proteins from ELV-MB (Table S2), leaving 263 that had not formally been associated with C2C12 myoblast ELVs.”
InfluentialAdvances in the understanding of mitochondrial DNA as a pathogenic factor in inflammatory diseases
Boyapati, R. K., Tamborska, A., Dorward, D. A., & Ho, G. (2017) · F1000Research · doi:10.12688/f1000research.10397.1 · Cited by 169 · see citing works
Mitochondrial DNA in extracellular vesicles declines with age
Lazo, S., Hooten, N. N., Green, J., Eitan, E., Mode, N. A., Liu, Q., Zonderman, A. B., Ezike, N., Mattson, M. P., Ghosh, P., et al. (2020) · Aging Cell · doi:10.1111/acel.13283 · Cited by 161 · see citing works
“Recent data indicate that ccf-mtDNA can be detected in EVs derived from myoblasts, astrocytes and glioblastoma cells grown in vitro and also in plasma EVs from women with hormonal therapy-resistant breast cancer (Guescini et al., 2010a; Guescini, Guidolin, et al., 2010; Sansone et al., 2017).”
BackgroundBae, J. H., Jo, S. I., Kim, S. J., Lee, J. M., Jeong, J. H., Kang, J. S., Cho, N., Kim, S. S., Lee, E. Y., & Moon, J. (2019) · Cells · doi:10.3390/cells8040328 · Cited by 162 · see citing works
Mitochondrial Dysfunction and Aging: Insights from the Analysis of Extracellular Vesicles
Picca, A., Guerra, F., Calvani, R., Bucci, C., Monaco, M. R. L., Bentivoglio, A. R., Coelho‐Júnior, H. J., Landi, F., Bernabei, R., & Marzetti, E. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20040805 · Cited by 159 · see citing works
“Mitochondrial mtDNA (mtDNA) fragments have been identified within the exosomal cargo in astrocytes and myoblasts [46,47].”
BackgroundExtracellular vesicles as emerging targets in cancer: Recent development from bench to bedside
Wu, K., Xing, F., Wu, S.-Y., & Watabe, K. (2017) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2017.10.001 · Cited by 157 · see citing works
“Nat Immunol, 3(12), 1156-62 (2002) doi:10.”
InfluentialBryzgunova, O. E., Zaripov, M. M., Skvortsova, T. E., Lekchnov, E. A., Grigor’eva, A. E., Zaporozhchenko, I. A., Morozkin, E. S., Ryabchikova, E. I., Yurchenko, Y. B., Voitsitskiy, V. E., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157566 · Cited by 155 · see citing works
“Besides, mitochondrial DNA was found in exosomes from C2C12 myoblasts [51], glioblastoma cells and astrocytes [52].”
BackgroundDiagnostic and therapeutic potentials of exosomes in CNS diseases
Kawiková, I., & Askenase, P. W. (2014) · Brain Research · doi:10.1016/j.brainres.2014.09.070 · Cited by 144 · see citing works
Hudson, M. B., Woodworth-Hobbs, M. E., Zheng, B., Rahnert, J. A., Blount, M. A., Gooch, J. L., Searles, C. D., & Price, S. R. (2014) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00266.2013 · Cited by 137 · see citing works
“In 2010, it was reported that C2C12 myotubes release exosomes, but there was no attempt to measure or identify the encapsulated microRNAs (11).”
Li, Y., & Yao, H. (2016) · British Journal of Pharmacology · doi:10.1111/bph.13518 · Cited by 138 · see citing works
Mechanisms of mitochondrial DNA escape and its relationship with different metabolic diseases
Pérez-Treviño, P., Velasquez-Esparza, M. M., & Garcı́a, N. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.165761 · Cited by 134 · 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
“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).”
Exosome-mediated communication in the ovarian follicle
Pietro, C. D. (2016) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-016-0657-9 · Cited by 136 · see citing works
Small extracellular vesicles in cancer
Abhange, K. K., Makler, A., Wen, Y., Ramnauth, N., Mao, W., Asghar, W., & Wan, Y. (2021) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.03.015 · Cited by 130 · 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
Identification and characterization of the nano-sized vesicles released by muscle cells
Romancino, D. P., Paterniti, G., Campos, Y., De Luca, A., Di Felice, V., d'Azzo, A., & Bongiovanni, A. (2013) · FEBS Letters · doi:10.1016/j.febslet.2013.03.012 · Cited by 120 · 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.”
The influence of tumour-derived extracellular vesicles on local and distal metastatic dissemination
Nogués, L., Benito‐Martín, A., Hergueta‐Redondo, M., & Peinado, H. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.11.012 · Cited by 116 · see citing works
“The isolation of exoDNA and exoRNA in combination with circulating free DNA might offer a more reliable and sensitive screening tool to detect specific mutations.”
BackgroundInfluentialStem cell-derived exosomes: roles in stromal remodeling, tumor progression, and cancer immunotherapy
Fatima, F., & Nawaz, M. (2015) · Chinese journal of cancer · doi:10.1186/s40880-015-0051-5 · Cited by 108 · see citing works
MitoEVs: A new player in multiple disease pathology and treatment
Zhou, X., Liu, S., Lu, Y., Wan, M., Cheng, J., & Liu, J. (2023) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12320 · Cited by 113 · see citing works
Li, J., Zhang, Y., Dong, P.-Y., Yang, G.-M., & Gurunathan, S. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115087 · Cited by 111 · see citing works
The bright and dark side of extracellular vesicles in the senescence-associated secretory phenotype
Wallis, R., Mizen, H., & Bishop, C. L. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111263 · Cited by 107 · see citing works
“Furthermore, mitochondrial DNA (mtDNA) has been identified in EVs isolated from astrocytes (Guescini and Genedani, 2010) and myoblasts (Guescini and Guidolin, 2010) suggesting that mitochondrial components may be removed via a vesicular route.”
BackgroundSandonà, M., Pietro, L. D., Esposito, F., Ventura, A., Silini, A. R., Parolini, O., & Saccone, V. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.652970 · Cited by 108 · see citing works
“Subsequent characterization studies identified this fraction as EVs, which are lipid endogenous nanoparticles that mediate the transfer of their content across cellular boundaries (Guescini et al., 2010; Andaloussi et al., 2013; Romancino et al., 2013; Forterre et al., 2014).”
BackgroundMechanical overload‐induced muscle‐derived extracellular vesicles promote adipose tissue lipolysis
Vechetti, I. J., Peck, B. D., Wen, Y., Walton, R. G., Valentino, T. R., Alimov, A. P., Dungan, C. M., Pelt, D. W. V., von Walden, F., Alkner, B. A., et al. (2021) · The FASEB Journal · doi:10.1096/fj.202100242r · Cited by 105 · see citing works
Ye, W., Tang, X., Yang, Z., Liu, C., Zhang, X., Jin, J., & Lyu, J. (2017) · Molecular Immunology · doi:10.1016/j.molimm.2017.03.011 · Cited by 104 · see citing works
Wang, W., Li, M., Chen, Z., Xu, L., Chang, M., Wang, K., Deng, C., Gu, Y., Zhou, S., Shen, Y., et al. (2022) · Biochemical Pharmacology · doi:10.1016/j.bcp.2022.114954 · Cited by 107 · see citing works
Exosome-Mediated Impact on Systemic Metabolism
Rocha, K. C. E., Ying, W., & Olefsky, J. M. (2024) · Annual Review of Physiology · doi:10.1146/annurev-physiol-042222-024535 · Cited by 103 · see citing works
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 · see citing works
“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 99 · see citing works
“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 93 · see citing works
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 93 · see citing works
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 93 · see citing works
“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 92 · see citing works
“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 93 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 82 · see citing works
“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 85 · see citing works
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 82 · see citing works
“[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 79 · see citing works
“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 79 · see citing works
“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 80 · see citing works
“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 · see citing works
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 · 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
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 · see citing works
“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 77 · see citing works
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 · see citing works
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 · see citing works
Karnas, E., Dudek, P., & Zuba‐Surma, E. K. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1120175 · Cited by 73 · see citing works
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 · see citing works
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 71 · see citing works
“…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 · see citing works
“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 · see citing works
“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 62 · see citing works
“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 · see citing works
“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 · see citing works
“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 60 · see citing works
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 58 · see citing works
“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 · see citing works
“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., & Camussi, G. (2019) · American Journal of Physiology - Cell Physiology · doi:10.1152/ajpcell.00129.2019 · Cited by 43 · see citing works
“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 56 · see citing works
“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
- 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
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 ›
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