Heterogeneity of extracellular vesicles in porcine myoblasts regulates adipocyte differentiation.
Adipocytes
Heterogeneity
Porcine
Skeletal muscle stem cells
sEV
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
30 10 2024
30 10 2024
Historique:
received:
20
06
2024
accepted:
21
10
2024
medline:
31
10
2024
pubmed:
31
10
2024
entrez:
31
10
2024
Statut:
epublish
Résumé
The interactions between myogenic cells and adipocytes play an important role in improving carcass traits and the efficiency of energy utilization. However, there are few reports about the interaction between them mediated by small extracellular vesicles (sEV). In this study, sEV derived from porcine primary skeletal muscle stem cells (MuSCs) was found to be involved in the inhibition of porcine primary adipocyte viability, triglyceride content, Oil Red O enrichment and the expression of adipogenic genes. When the MuSCs were treated with insulin (INS) and oleic acid (OA), the effects of their secreted sEVs on adipose precursor cells were reversed, suggesting that the signaling effects of sEV are related to their own heterogeneity. Further by component heterogeneity analysis, miR-146a-5p was found to be enriched in sEVs of MuSCs and to regulate and suppress adipogenesis through its heterogeneity. This study provides an important mechanism and molecular target for small extracellular vesicles to regulate the interaction between muscle and adipose tissue and improve carcass traits at the intercellular level.
Identifiants
pubmed: 39478138
doi: 10.1038/s41598-024-77110-5
pii: 10.1038/s41598-024-77110-5
doi:
Substances chimiques
MicroRNAs
0
Insulin
0
Oleic Acid
2UMI9U37CP
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
26077Subventions
Organisme : National Natural Science Foundation of China
ID : 32072814
Informations de copyright
© 2024. The Author(s).
Références
Kaczmarska, K., Taylor, M., Piyasiri, U. & Frank, D. Flavor and metabolite profiles of meat, meat substitutes, and traditional plant-based high-protein food products available in Australia. Foods 10(4), 801 (2021).
pubmed: 33917948
pmcid: 8068397
doi: 10.3390/foods10040801
Wang, C. et al. Effectiveness and safety evaluation of graded levels of N-carbamylglutamate in growing-finishing pigs. Anim. Nutr. 10, 412–418 (2022).
pubmed: 36016840
pmcid: 9382136
doi: 10.1016/j.aninu.2022.04.012
Zhao, Y. et al. Dynamic transcriptome profiles of skeletal muscle tissue across 11 developmental stages for both Tongcheng and Yorkshire pigs. BMC Genom. 16(1), 377 (2015).
doi: 10.1186/s12864-015-1580-7
Dinh, C. H. et al. Bardoxolone methyl prevents fat deposition and inflammation in the visceral fat of mice fed a high-fat diet. Chem. Biol. Interact. 229, 1–8 (2015).
pubmed: 25637688
doi: 10.1016/j.cbi.2015.01.025
Liu, J. et al. Comprehensive evaluation of the metabolic effects of porcine CRTC3 overexpression on subcutaneous adipocytes with metabolomic and transcriptomic analyses. J. Anim. Sci. Biotechnol. 12(1), 19 (2021).
pubmed: 33653408
pmcid: 7927250
doi: 10.1186/s40104-021-00546-6
Wagner, J. et al. Functional aging in health and heart failure: The COmPLETE study. BMC Cardiovasc. Disord. 19(1), 180 (2019).
pubmed: 31362698
pmcid: 6664502
doi: 10.1186/s12872-019-1164-6
Wang, L., Xie, Y., Chen, W., Zhang, Y. & Zeng, Y. miR-34a regulates lipid droplet deposition in 3T3-L1 and C2C12 cells by targeting LEF1. Cells 12(1), 167 (2022).
pubmed: 36611960
pmcid: 9818453
doi: 10.3390/cells12010167
Maggiolino, A. et al. Dry-aged beef steaks: Effect of dietary supplementation with Pinustaeda hydrolyzed lignin on sensory profile, colorimetric and oxidative stability. Foods 10(5), 1080 (2021).
pubmed: 34068173
pmcid: 8152972
doi: 10.3390/foods10051080
Chen, C. et al. Prevotellacopri increases fat accumulation in pigs fed with formula diets. Microbiome 9(1), 175 (2021).
pubmed: 34419147
pmcid: 8380364
doi: 10.1186/s40168-021-01110-0
Wu, W. et al. Comprehensive transcriptomic view of the role of the LGALS12 gene in porcine subcutaneous and intramuscular adipocytes. BMC Genom. 20(1), 509 (2019).
doi: 10.1186/s12864-019-5891-y
Gonzalez-Gil, A. M. & Elizondo-Montemayor, L. The role of exercise in the interplay between myokines, hepatokines, osteokines, adipokines, and modulation of inflammation for energy substrate redistribution and fat mass loss: A review. Nutrients 12(6), 1899 (2020).
pubmed: 32604889
pmcid: 7353393
doi: 10.3390/nu12061899
Nigro, P. et al. Exercise training promotes sex-specific adaptations in mouse inguinal white adipose tissue. Diabetes 70(6), 1250–1264 (2021).
pubmed: 33563587
pmcid: 8275891
doi: 10.2337/db20-0790
Takahashi, H. et al. TGF-β2 is an exercise-induced adipokine that regulates glucose and fatty acid metabolism. Nat. Metab. 1(2), 291–303 (2019).
pubmed: 31032475
pmcid: 6481955
doi: 10.1038/s42255-018-0030-7
Pedersen, B. K. Muscle as a secretory organ. Compr. Physiol. 3(3), 1337–1362 (2013).
pubmed: 23897689
doi: 10.1002/cphy.c120033
Stanford, K. I. & Goodyear, L. J. Muscle-adipose tissue cross talk. Cold Spring Harb. Perspect. Med. 8(8), a029801 (2018).
pubmed: 28507197
pmcid: 5685935
doi: 10.1101/cshperspect.a029801
Ayer, J., Charakida, M., Deanfield, J. E. & Celermajer, D. S. Lifetime risk: Childhood obesity and cardiovascular risk. Eur. Heart J. 36(22), 1371–1376 (2015).
pubmed: 25810456
doi: 10.1093/eurheartj/ehv089
Salek-Maghsoudi, A. et al. Recent advances in biosensor technology in assessment of early diabetes biomarkers. Biosens. Bioelectron. 99, 122–135 (2018).
pubmed: 28750336
doi: 10.1016/j.bios.2017.07.047
Severinsen, M. C. K. & Pedersen, B. K. Muscle-organ crosstalk: The emerging roles of myokines. Endocr. Rev. 41(4), 594–609 (2020).
pubmed: 32393961
pmcid: 7288608
doi: 10.1210/endrev/bnaa016
Liu, J. et al. Integrative biology of extracellular vesicles in diabetes mellitus and diabetic complications. Theranostics 12(3), 1342–1372 (2022).
pubmed: 35154494
pmcid: 8771544
doi: 10.7150/thno.65778
Lemaire, Q. et al. Isolation of microglia-derived extracellular vesicles: Towards miRNA signatures and neuroprotection. J. Nanobiotechnol. 17(1), 119 (2019).
doi: 10.1186/s12951-019-0551-6
Farooq, A. U. et al. K-29 linked ubiquitination of Arrdc4 regulates its function in extracellular vesicle biogenesis. J. Extracell. Vesicles 11(2), e12188 (2022).
pubmed: 35106941
pmcid: 8807422
doi: 10.1002/jev2.12188
Chuo, S. T., Chien, J. C. & Lai, C. P. Imaging extracellular vesicles: Current and emerging methods. J. Biomed. Sci. 25(1), 91 (2018).
pubmed: 30580764
pmcid: 6304785
doi: 10.1186/s12929-018-0494-5
Han, C. et al. Single-vesicle imaging and co-localization analysis for tetraspanin profiling of individual extracellular vesicles. J. Extracell. Vesicles 10(3), e12047 (2021).
pubmed: 33456726
pmcid: 7797949
doi: 10.1002/jev2.12047
de Jong, O. G. et al. Drug Delivery with extracellular vesicles: From imagination to innovation. Acc. Chem. Res. 52(7), 1761–1770 (2019).
pubmed: 31181910
pmcid: 6639984
doi: 10.1021/acs.accounts.9b00109
Chen, J. et al. E2F1 regulates adipocyte differentiation and adipogenesis by activating ICAT. Cells 9(4), 1024 (2020).
pubmed: 32326181
pmcid: 7225968
doi: 10.3390/cells9041024
Li, W. et al. Comparative analysis of MicroRNA expression profiles between skeletal muscle-and adipose-derived exosomes in pig. Front. Genet. 12, 631230 (2021).
pubmed: 34135937
pmcid: 8202525
doi: 10.3389/fgene.2021.631230
Qin, M. et al. Skeletal muscle-derived exosomal miR-146a-5p inhibits adipogenesis by mediating muscle-fat axis and targeting GDF5-PPARγ signaling. Int. J. Mol. Sci. 24(5), 4561 (2023).
pubmed: 36901991
pmcid: 10003660
doi: 10.3390/ijms24054561
Lee, S. H. et al. The influence of pork quality traits and muscle fiber characteristics on the eating quality of pork from various breeds. Meat Sci. 90(2), 284–291 (2012).
pubmed: 21840135
doi: 10.1016/j.meatsci.2011.07.012
Li, H. et al. Effects of ractopamine administration and castration method on muscle fiber characteristics and sensory quality of the longissimus muscle in two Piétrain pig genotypes. Meat Sci. 102, 27–34 (2015).
pubmed: 25529286
doi: 10.1016/j.meatsci.2014.10.027
Chai, C. et al. Metabolic circuit involving free fatty acids, microRNA 122, and triglyceride synthesis in liver and muscle tissues. Gastroenterology 153(5), 1404–1415 (2017).
pubmed: 28802563
doi: 10.1053/j.gastro.2017.08.013
Senol-Cosar, O. et al. Tenomodulin promotes human adipocyte differentiation and beneficial visceral adipose tissue expansion. Nat. Commun. 7, 10686 (2016).
pubmed: 26880110
pmcid: 4757769
doi: 10.1038/ncomms10686
Shirvani, H. & Arabzadeh, E. Metabolic cross-talk between skeletal muscle and adipose tissue in high-intensity interval training vs. Moderate-intensity continuous training by regulation of PGC-1α. Eat Weight Disord. 25(1), 17–24 (2020).
pubmed: 29480414
doi: 10.1007/s40519-018-0491-4
Li, Y. et al. Myokine IL-15 regulates the crosstalk of co-cultured porcine skeletal muscle satellite cells and preadipocytes. Mol. Biol. Rep. 41(11), 7543–7553 (2014).
pubmed: 25098601
doi: 10.1007/s11033-014-3646-z
Yan, J., Gan, L., Yang, H. & Sun, C. The proliferation and differentiation characteristics of co-cultured porcine preadipocytes and muscle satellite cells in vitro. Mol. Biol. Rep. 40(4), 3197–3202 (2013).
pubmed: 23271122
doi: 10.1007/s11033-012-2395-0
Choi, S. H. et al. Co-culture of bovine muscle satellite cells with preadipocytes increases PPARγ and C/EBPβ gene expression in differentiated myoblasts and increases GPR43 gene expression in adipocytes. J. Nutr. Biochem. 24(3), 539–543 (2013).
pubmed: 22748806
doi: 10.1016/j.jnutbio.2012.01.015
Smith, G. I. et al. Influence of adiposity, insulin resistance, and intrahepatic triglyceride content on insulin kinetics. J. Clin. Invest. 130(6), 3305–3314 (2020).
pubmed: 32191646
pmcid: 7260030
doi: 10.1172/JCI136756
Taniguchi, A. et al. Remnant-like particle cholesterol, triglycerides, and insulin resistance in nonobese Japanese type 2 diabetic patients. Diabetes Care. 23(12), 1766–1769 (2000).
pubmed: 11128349
doi: 10.2337/diacare.23.12.1766
Wu, S. et al. In vitro inhibition of lipid accumulation induced by oleic acid and in vivo pharmacokinetics of chitosan microspheres (CTMS) and chitosan-capsaicin microspheres (CCMS). Food Nutr. Res. 61(1), 1331658 (2017).
pubmed: 28659743
pmcid: 5475299
doi: 10.1080/16546628.2017.1331658
Labbaye, C. & Testa, U. The emerging role of MIR-146A in the control of hematopoiesis, immune function and cancer. J. Hematol. Oncol. 5, 13 (2012).
pubmed: 22453030
pmcid: 3342163
doi: 10.1186/1756-8722-5-13
Nunes, A. D. C. et al. miR-146a-5p modulates cellular senescence and apoptosis in visceral adipose tissue of long-lived Ames dwarf mice and in cultured pre-adipocytes. Geroscience 44(1), 503–518 (2022).
pubmed: 34825304
doi: 10.1007/s11357-021-00490-3
Sun, Y. et al. miR-146a-5p acts as a negative regulator of TGF-β signaling in skeletal muscle after acute contusion. Acta Biochim. Biophys. Sin. 49(7), 628–634 (2017).
pubmed: 28510617
doi: 10.1093/abbs/gmx052
Wu, D. et al. miR-146a-5p inhibits TNF-α-induced adipogenesis via targeting insulin receptor in primary porcine adipocytes. J. Lipid Res. 57(8), 1360–1372 (2016).
pubmed: 27324794
pmcid: 4959853
doi: 10.1194/jlr.M062497
Zhang, Q., Cai, R., Tang, G., Zhang, W. & Pang, W. MiR-146a-5p targeting SMAD4 and TRAF6 inhibits adipogenensis through TGF-β and AKT/mTORC1 signal pathways in porcine intramuscular preadipocytes. J. Anim. Sci. Biotechnol. 12(1), 12 (2021).
pubmed: 33531066
pmcid: 7856799
doi: 10.1186/s40104-020-00525-3
Wang, Y. et al. MiR-146a-5p, targeting ErbB4, promotes 3T3-L1 preadipocyte differentiation through the ERK1/2/PPAR-γ signaling pathway. Lipids Health Dis. 21(1), 54 (2022).
pubmed: 35705996
pmcid: 9202118
doi: 10.1186/s12944-022-01662-6