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Oxidative and glycolytic skeletal muscle-derived exosomes selectively coated miRNAs and participate in regulating myoblast proliferation and differentiation mediated by miR-4331-3p

ABSTRACT: The phenotypic characteristics and meat quality of skeletal muscle are collectively determined by the muscle cells, other cellular groups within it, and their intricate interactions with the extracellular microenvironment. Exosomes have the capacity to influence the development and microenvironment of skeletal muscle, thus playing a crucial role in its differentiation and maturation. In this study, we conducted an initial evaluation of the muscle fiber phenotypes in glycolytic skeletal muscle (Longissimus dorsi, HC-L) and oxidative skeletal muscle (Psoas major, HC-P) of Hechuan black pigs. The results revealed significant differences in terms of muscle fiber diameter, density, and type phenotypes (P<0.05). Subsequently, we isolated and identified exosomes derived from skeletal muscle (SKM-Exos). Co-culture experiments with myoblasts demonstrated that SKM-Exos can promote both myoblast proliferation and differentiation. Furthermore, sequencing analysis confirmed that miRNAs present in SKM-Exos are selectively coated miRNAs. It is noteworthy that the expression of miR-4331-3p was notably higher in SKM-Exos compared to its derived skeletal muscles. It was significantly elevated in the SKM-Exos of HC-L when compared to those of HC-P, and have interactions with the differentially expressed genes between HC-L and HC-P. Interestingly enough, miR-4331-3p has been shown to enhance myoblast proliferation while inhibiting the differentiation process. By investigating the interaction between SKM-Exos, their derived miRNAs, and myoblasts, this study elucidated the molecular mechanism underlying the regulation of muscle fiber differentiation by SKM-Exos and provided valuable insights into the intricate molecular processes involved in meat formation.

ORGANISM(S): Sus scrofa

PROVIDER: GSE269386 | GEO | 2026/06/07

REPOSITORIES: GEO

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Project description:Myoblasts are critical progenitor cells for the prenatal formation of skeletal muscle (SkM) as well as in postnatal repair of SkM. This study examined the epigenomics and transcriptomics of human myoblasts vs. those of diverse other cell and tissue types from both global genomic and single-gene perspectives. Using enzymatic methyl-seq (EM-seq) and whole-genome bisulfite sequencing (WGBS) of myoblast DNA and available WGBS profiles of other cell cultures, we determined myoblast differentially methylated regions (DMRs). We also examined several DMRs in reporter gene assays. Among the unusual findings was the positive association of promoter-adjacent hypermethylation in myoblasts with transcription turn-on for some genes (e.g., SIM2 and TWIST1), but at down-modulated levels. In contrast, some genes, like the brain-specific OLIG2, were silent and embedded in repressed chromatin in myoblasts and many diverse cell populations but displayed myoblast-specific hypermethylated promoters. OLIG2 exhibited binding of the myogenic MYOD transcription factor in its vicinity. One OLIG2-downstream MYOD+ site overlapped enhancer chromatin in myotubes. These findings suggest that OLIG2 silencing only by repressive chromatin is insufficient in myoblasts without the addition of DNA hypermethylation. The numerous hypomethylated DMRs at enhancer chromatin in myoblasts were bound by MYOD much more frequently than by CTCF. Combined with previous studies, our results suggest a more prevalent role for MYOD than for CTCF in organizing transcription-enhancing chromatin interactions at hypomethylated regions. We also found that myoblast-hypomethylated enhancer chromatin enriched in H3K36me3 was much more likely to be associated with genes preferentially expressed in myoblasts than were such regions without H3K36me3 enrichment. Therefore, there may be a special role in gene upregulation for the regional combination of DNA hypomethylation with H3K27ac, H3K4me1, and H3K36me3 enrichment. The unusual relationships between epigenetics and gene expression that we observed need further study in the SkM lineage to better understand fine-tuning of muscle differentiation and diseases.

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Oxidative and glycolytic skeletal muscle-derived exosomes selectively coated miRNAs and participate in regulating myoblast proliferation and differentiation mediated by miR-4331-3p

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