Proteomic analysis of C2C12 myoblast and myotube exosome-like vesicles: a new paradigm for myoblast-myotube cross talk?

Exosomes are nanometer-sized microvesicles formed in multivesicular bodies (MVBs) during endosome maturation. Exosomes are released from cells into the microenvironment following fusion of MVBs with the plasma membrane. During the last decade, skeletal muscle-secreted proteins have been identified w...

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Autores principales: Alexis Forterre, Audrey Jalabert, Emmanuelle Berger, Mathieu Baudet, Karim Chikh, Elisabeth Errazuriz, Joffrey De Larichaudy, Stéphanie Chanon, Michèle Weiss-Gayet, Anne-Marie Hesse, Michel Record, Alain Geloen, Etienne Lefai, Hubert Vidal, Yohann Couté, Sophie Rome
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Publicado: Public Library of Science (PLoS) 2014
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spelling oai:doaj.org-article:f210e1372bcc484dbb2cd7b5d66fc38f2021-11-18T08:39:08ZProteomic analysis of C2C12 myoblast and myotube exosome-like vesicles: a new paradigm for myoblast-myotube cross talk?1932-620310.1371/journal.pone.0084153https://doaj.org/article/f210e1372bcc484dbb2cd7b5d66fc38f2014-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24392111/?tool=EBIhttps://doaj.org/toc/1932-6203Exosomes are nanometer-sized microvesicles formed in multivesicular bodies (MVBs) during endosome maturation. Exosomes are released from cells into the microenvironment following fusion of MVBs with the plasma membrane. During the last decade, skeletal muscle-secreted proteins have been identified with important roles in intercellular communications. To investigate whether muscle-derived exosomes participate in this molecular dialog, we determined and compared the protein contents of the exosome-like vesicles (ELVs) released from C2C12 murine myoblasts during proliferation (ELV-MB), and after differentiation into myotubes (ELV-MT). Using a proteomic approach combined with electron microscopy, western-blot and bioinformatic analyses, we compared the protein repertoires within ELV-MB and ELV-MT. We found that these vesicles displayed the classical properties of exosomes isolated from other cell types containing components of the ESCRT machinery of the MVBs, as well as numerous tetraspanins. Specific muscle proteins were also identified confirming that ELV composition also reflects their muscle origin. Furthermore quantitative analysis revealed stage-preferred expression of 31 and 78 proteins in ELV-MB and ELV-MT respectively. We found that myotube-secreted ELVs, but not ELV-MB, reduced myoblast proliferation and induced differentiation, through, respectively, the down-regulation of Cyclin D1 and the up-regulation of myogenin. We also present evidence that proteins from ELV-MT can be incorporated into myoblasts by using the GFP protein as cargo within ELV-MT. Taken together, our data provide a useful database of proteins from C2C12-released ELVs throughout myogenesis and reveals the importance of exosome-like vesicles in skeletal muscle biology.Alexis ForterreAudrey JalabertEmmanuelle BergerMathieu BaudetKarim ChikhElisabeth ErrazurizJoffrey De LarichaudyStéphanie ChanonMichèle Weiss-GayetAnne-Marie HesseMichel RecordAlain GeloenEtienne LefaiHubert VidalYohann CoutéSophie RomePublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 9, Iss 1, p e84153 (2014)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Alexis Forterre
Audrey Jalabert
Emmanuelle Berger
Mathieu Baudet
Karim Chikh
Elisabeth Errazuriz
Joffrey De Larichaudy
Stéphanie Chanon
Michèle Weiss-Gayet
Anne-Marie Hesse
Michel Record
Alain Geloen
Etienne Lefai
Hubert Vidal
Yohann Couté
Sophie Rome
Proteomic analysis of C2C12 myoblast and myotube exosome-like vesicles: a new paradigm for myoblast-myotube cross talk?
description Exosomes are nanometer-sized microvesicles formed in multivesicular bodies (MVBs) during endosome maturation. Exosomes are released from cells into the microenvironment following fusion of MVBs with the plasma membrane. During the last decade, skeletal muscle-secreted proteins have been identified with important roles in intercellular communications. To investigate whether muscle-derived exosomes participate in this molecular dialog, we determined and compared the protein contents of the exosome-like vesicles (ELVs) released from C2C12 murine myoblasts during proliferation (ELV-MB), and after differentiation into myotubes (ELV-MT). Using a proteomic approach combined with electron microscopy, western-blot and bioinformatic analyses, we compared the protein repertoires within ELV-MB and ELV-MT. We found that these vesicles displayed the classical properties of exosomes isolated from other cell types containing components of the ESCRT machinery of the MVBs, as well as numerous tetraspanins. Specific muscle proteins were also identified confirming that ELV composition also reflects their muscle origin. Furthermore quantitative analysis revealed stage-preferred expression of 31 and 78 proteins in ELV-MB and ELV-MT respectively. We found that myotube-secreted ELVs, but not ELV-MB, reduced myoblast proliferation and induced differentiation, through, respectively, the down-regulation of Cyclin D1 and the up-regulation of myogenin. We also present evidence that proteins from ELV-MT can be incorporated into myoblasts by using the GFP protein as cargo within ELV-MT. Taken together, our data provide a useful database of proteins from C2C12-released ELVs throughout myogenesis and reveals the importance of exosome-like vesicles in skeletal muscle biology.
format article
author Alexis Forterre
Audrey Jalabert
Emmanuelle Berger
Mathieu Baudet
Karim Chikh
Elisabeth Errazuriz
Joffrey De Larichaudy
Stéphanie Chanon
Michèle Weiss-Gayet
Anne-Marie Hesse
Michel Record
Alain Geloen
Etienne Lefai
Hubert Vidal
Yohann Couté
Sophie Rome
author_facet Alexis Forterre
Audrey Jalabert
Emmanuelle Berger
Mathieu Baudet
Karim Chikh
Elisabeth Errazuriz
Joffrey De Larichaudy
Stéphanie Chanon
Michèle Weiss-Gayet
Anne-Marie Hesse
Michel Record
Alain Geloen
Etienne Lefai
Hubert Vidal
Yohann Couté
Sophie Rome
author_sort Alexis Forterre
title Proteomic analysis of C2C12 myoblast and myotube exosome-like vesicles: a new paradigm for myoblast-myotube cross talk?
title_short Proteomic analysis of C2C12 myoblast and myotube exosome-like vesicles: a new paradigm for myoblast-myotube cross talk?
title_full Proteomic analysis of C2C12 myoblast and myotube exosome-like vesicles: a new paradigm for myoblast-myotube cross talk?
title_fullStr Proteomic analysis of C2C12 myoblast and myotube exosome-like vesicles: a new paradigm for myoblast-myotube cross talk?
title_full_unstemmed Proteomic analysis of C2C12 myoblast and myotube exosome-like vesicles: a new paradigm for myoblast-myotube cross talk?
title_sort proteomic analysis of c2c12 myoblast and myotube exosome-like vesicles: a new paradigm for myoblast-myotube cross talk?
publisher Public Library of Science (PLoS)
publishDate 2014
url https://doaj.org/article/f210e1372bcc484dbb2cd7b5d66fc38f
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