Profiling of ob/ob mice skeletal muscle exosome-like vesicles demonstrates combined action of miRNAs, proteins and lipids to modulate lipid homeostasis in recipient cells.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
03 11 2021
Historique:
received: 23 04 2021
accepted: 15 10 2021
entrez: 4 11 2021
pubmed: 5 11 2021
medline: 28 1 2022
Statut: epublish

Résumé

We have determined the lipid, protein and miRNA composition of skeletal muscle (SkM)-released extracellular vesicles (ELVs) from Ob/ob (OB) vs wild-type (WT) mice. The results showed that atrophic insulin-resistant OB-SkM released less ELVs than WT-SkM, highlighted by a RAB35 decrease and an increase in intramuscular cholesterol content. Proteomic analyses of OB-ELVs revealed a group of 37 proteins functionally connected, involved in lipid oxidation and with catalytic activities. OB-ELVs had modified contents for phosphatidylcholine (PC 34-4, PC 40-3 and PC 34-0), sphingomyelin (Sm d18:1/18:1) and ceramides (Cer d18:1/18:0) and were enriched in cholesterol, likely to alleviated intracellular accumulation. Surprisingly many ELV miRNAs had a nuclear addressing sequence, and targeted genes encoding proteins with nuclear activities. Interestingly, SkM-ELV miRNA did not target mitochondria. The most significant function targeted by the 7 miRNAs altered in OB-ELVs was lipid metabolism. In agreement, OB-ELVs induced lipid storage in recipient adipocytes and increased lipid up-take and fatty acid oxidation in recipient muscle cells. In addition, OB-ELVs altered insulin-sensitivity and induced atrophy in muscle cells, reproducing the phenotype of the releasing OB muscles. These data suggest for the first time, a cross-talk between muscle cells and adipocytes, through the SkM-ELV route, in favor of adipose tissue expansion.

Identifiants

pubmed: 34732797
doi: 10.1038/s41598-021-00983-3
pii: 10.1038/s41598-021-00983-3
pmc: PMC8566600
doi:

Substances chimiques

Lipids 0
MicroRNAs 0
Muscle Proteins 0
Proteome 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

21626

Subventions

Organisme : Agence Nationale de la Recherche
ID : ANR-10-INBS-08
Organisme : Agence Nationale de la Recherche
ID : ANR ZENITH n°45000260
Organisme : ANR
ID : ANR-17-EURE-0003

Informations de copyright

© 2021. The Author(s).

Références

Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14440-5
pubmed: 11717410
J Lipid Res. 2018 Dec;59(12):2255-2261
pubmed: 29678958
J Extracell Vesicles. 2019 Dec 19;9(1):1703244
pubmed: 32002167
Prenat Diagn. 2005 Nov;25(11):1000-6
pubmed: 16231320
Cancer Res. 2016 Jul 15;76(14):4051-7
pubmed: 27216185
PLoS One. 2007 Sep 05;2(9):e851
pubmed: 17786222
Nat Cell Biol. 2007 Jun;9(6):654-9
pubmed: 17486113
Cold Spring Harb Perspect Biol. 2013 Oct 01;5(10):a016816
pubmed: 24086044
RNA Biol. 2010 Sep-Oct;7(5):606-14
pubmed: 20864815
Prostaglandins Leukot Essent Fatty Acids. 2011 Jan-Feb;84(1-2):7-11
pubmed: 21109411
Nat Cell Biol. 2008 Dec;10(12):1470-6
pubmed: 19011622
Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17615-22
pubmed: 19822761
Theranostics. 2018 Mar 8;8(8):2171-2188
pubmed: 29721071
Diabetologia. 2016 May;59(5):1049-58
pubmed: 26852333
Int J Mol Sci. 2021 Feb 11;22(4):
pubmed: 33670146
Cytokine Growth Factor Rev. 2017 Feb;33:73-82
pubmed: 27765498
Prog Lipid Res. 2017 Apr;66:30-41
pubmed: 28342835
J Biol Chem. 2010 Jun 4;285(23):17442-52
pubmed: 20353945
Life Sci. 1987 Sep 7;41(10):1233-41
pubmed: 3041138
Science. 2007 Jan 5;315(5808):97-100
pubmed: 17204650
J Biol Chem. 1957 May;226(1):497-509
pubmed: 13428781
Cell Cycle. 2014;13(1):78-89
pubmed: 24196440
Springerplus. 2014 Oct 08;3:584
pubmed: 25332884
J Cell Biol. 2010 Apr 19;189(2):223-32
pubmed: 20404108
Front Immunol. 2014 Aug 20;5:403
pubmed: 25191326
J Diabetes Res. 2017;2017:1789395
pubmed: 28676863
Nat Commun. 2013;4:2980
pubmed: 24356509
RNA Biol. 2012 Mar;9(3):269-73
pubmed: 22336708
Gen Comp Endocrinol. 1971 Aug;17(1):164-82
pubmed: 5559131
Front Physiol. 2019 Aug 09;10:929
pubmed: 31447684
Bioinformatics. 2017 Jan 1;33(1):135-136
pubmed: 27605098
Proteomics. 2013 Aug;13(16):2419-23
pubmed: 23744604
Diabetologia. 1984 Sep;27(3):407-13
pubmed: 6238863
Science. 2012 May 18;336(6083):809-10
pubmed: 22605737
Obes Facts. 2018;11(4):294-305
pubmed: 30016792
Proc Natl Acad Sci U S A. 2006 Dec 12;103(50):18957-62
pubmed: 17135348
Diabetes. 2018 Nov;67(11):2377-2388
pubmed: 29720498
Front Cell Dev Biol. 2019 May 03;7:70
pubmed: 31131274
Int J Obes (Lond). 2005 Oct;29(10):1175-83
pubmed: 16030519
Adipocyte. 2019 Dec;8(1):83-97
pubmed: 30905315
Biochem J. 2001 Nov 15;360(Pt 1):143-50
pubmed: 11696001
EMBO J. 2011 Aug 31;30(17):3481-500
pubmed: 21878991
J Clin Invest. 2004 Jan;113(1):115-23
pubmed: 14702115
Biochem Biophys Res Commun. 2002 Mar 1;291(3):701-6
pubmed: 11855847
Cell Res. 2012 Mar;22(3):504-15
pubmed: 21862971
J Biol Chem. 2003 May 16;278(20):18063-8
pubmed: 12621037
EMBO J. 2002 Mar 15;21(6):1289-300
pubmed: 11889035
Cell. 2005 Dec 16;123(6):1133-46
pubmed: 16337999
Cell. 2004 Jan 23;116(2):281-97
pubmed: 14744438
Proteomics. 2018 Mar;18(5-6):e1700375
pubmed: 29350465
RNA. 2011 Apr;17(4):675-86
pubmed: 21363885
Prostaglandins Leukot Essent Fatty Acids. 2018 Sep;136:161-169
pubmed: 28110829
Diabetologia. 2014 Oct;57(10):2155-64
pubmed: 25073444
Bioinformatics. 2020 May 1;36(10):3148-3155
pubmed: 32096818
Traffic. 2008 Feb;9(2):230-50
pubmed: 17999726
Front Mol Neurosci. 2013 Nov 26;6:43
pubmed: 24324399

Auteurs

Audrey Jalabert (A)

CarMeN Laboratory (INSERM 1060, INRAE 1397, INSA), Lyon-Sud Faculty of Medicine, University of Lyon, Oullins, France.

Laura Reininger (L)

UMR DIATHEC, EA 7294, Centre Européen d'Etude du Diabète, Université de Strasbourg, Strasbourg, France.

Emmanuelle Berger (E)

CarMeN Laboratory (INSERM 1060, INRAE 1397, INSA), Lyon-Sud Faculty of Medicine, University of Lyon, Oullins, France.
UMR Ecologie Microbienne Lyon (LEM), CNRS 5557, INRAE 1418, University of Lyon, VetAgro Sup, Villeurbanne, France.

Yohann Coute (Y)

Univ. Grenoble-Alpes, Inserm, CEA, UMR BioSanté U1292, CNRS CEA FR2048, Grenoble, France.

Emmanuelle Meugnier (E)

CarMeN Laboratory (INSERM 1060, INRAE 1397, INSA), Lyon-Sud Faculty of Medicine, University of Lyon, Oullins, France.

Alexis Forterre (A)

CarMeN Laboratory (INSERM 1060, INRAE 1397, INSA), Lyon-Sud Faculty of Medicine, University of Lyon, Oullins, France.
UMR DIATHEC, EA 7294, Centre Européen d'Etude du Diabète, Université de Strasbourg, Strasbourg, France.

Elizabeth Errazuriz-Cerda (E)

CIQLE, Claude Bernard Lyon 1 University, Lyon, France.

Alain Geloen (A)

CarMeN Laboratory (INSERM 1060, INRAE 1397, INSA), Lyon-Sud Faculty of Medicine, University of Lyon, Oullins, France.
UMR Ecologie Microbienne Lyon (LEM), CNRS 5557, INRAE 1418, University of Lyon, VetAgro Sup, Villeurbanne, France.

Myriam Aouadi (M)

Centre for Infectious Medicine, Department of Medicine, Karolinska Institutet, Huddinge, Sweden.

Karim Bouzakri (K)

UMR DIATHEC, EA 7294, Centre Européen d'Etude du Diabète, Université de Strasbourg, Strasbourg, France.

Jennifer Rieusset (J)

CarMeN Laboratory (INSERM 1060, INRAE 1397, INSA), Lyon-Sud Faculty of Medicine, University of Lyon, Oullins, France.

Sophie Rome (S)

CarMeN Laboratory (INSERM 1060, INRAE 1397, INSA), Lyon-Sud Faculty of Medicine, University of Lyon, Oullins, France. srome@univ-lyon1.fr.
Institut of Functional Genomic, ENS-Lyon, University of Lyon, CNRS 5242, INRAE Lyon, France. srome@univ-lyon1.fr.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH