Abstract
BackgroundMicroRNAs (miRNAs) are small non-coding RNAs that play critical roles in diverse biological processes via regulation of gene expression including in skeletal muscles. In the current study, miRNA expression profile was investigated in longissimus muscle biopsies of malignant hyperthermia syndrome-negative Duroc and Pietrain pigs with distinct muscle metabolic properties in order to explore the regulatory role of miRNAs related to mitochondrial respiratory activity and metabolic enzyme activity in skeletal muscle.ResultsA comparative analysis of the miRNA expression profile between Duroc and Pietrain pigs was performed, followed by integration with mRNA profiles based on their pairwise correlation and computational target prediction. The identified target genes were enriched in protein ubiquitination pathway, stem cell pluripotency and geranylgeranyl diphosphate biosynthesis, as well as skeletal and muscular system development. Next, we analyzed the correlation between individual miRNAs and phenotypical traits including muscle fiber type, mitochondrial respiratory activity, metabolic enzyme activity and adenosine phosphate concentrations, and constructed the regulatory miRNA-mRNA networks associated with energy metabolism. It is noteworthy that miR-25 targeting BMPR2 and IRS1, miR-363 targeting USP24, miR-28 targeting HECW2 and miR-210 targeting ATP5I, ME3, MTCH1 and CPT2 were highly associated with slow-twitch oxidative fibers, fast-twitch oxidative fibers, ADP and ATP concentration suggesting an essential role of the miRNA-mRNA regulatory networking in modulating the mitochondrial energy expenditure in the porcine muscle. In the identified miRNA-mRNA network, a tight relationship between mitochondrial and ubiquitin proteasome system at the level of gene expression was observed. It revealed a link between these two systems contributing to energy metabolism of skeletal muscle under physiological conditions.ConclusionsWe assembled miRNA-mRNA regulatory networks based on divergent muscle properties between different pig breeds and further with the correlation analysis of expressed genes and phenotypic measurements. These complex networks relate to muscle fiber type, metabolic enzyme activity and ATP production and may contribute to divergent muscle phenotypes by fine-tuning the expression of genes. Altogether, the results provide an insight into a regulatory role of miRNAs in muscular energy metabolisms and may have an implication on meat quality and production.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2850-8) contains supplementary material, which is available to authorized users.
Highlights
MicroRNAs are small non-coding RNAs that play critical roles in diverse biological processes via regulation of gene expression including in skeletal muscles
All the target genes were further analyzed with IPA to identify prominent functions and pathways that may contribute to divergent muscle metabolic properties between the two breed types
Duroc pigs are fattier and their skeletal muscle contains larger amount STO fibers which are generally associated with higher oxidative enzyme activities, mitochondrial respiratory activity and the storage of lipid to improve the tenderness and juiciness of the meat, whereas Pietrain pigs are more muscular and their muscles are more lean and contain higher percentage of FTG fibers which are associated with higher glycolytic enzyme activities [2, 18,19,20, 32, 33]
Summary
MicroRNAs (miRNAs) are small non-coding RNAs that play critical roles in diverse biological processes via regulation of gene expression including in skeletal muscles. MicroRNAs (miRNAs) are endogenous small non-coding RNAs ~22 nt in length that play critical roles in diverse biological processes via epigenetic regulation of gene expression. Since the critical roles of miRNAs such as myogenesis, adipogenesis and muscle development have been discovered in pig skeletal muscle [8,9,10,11], the understanding of the miRNA regulation in metabolic properties of skeletal muscle fibers could be key to improvement of meat quality [12]. MiR-696 regulates the fatty acid oxidation and mitochondrial biogenesis through targeting peroxisome proliferator-activated receptor-gamma coactivator-1alpha (PGC-1α) [17] With those miRNAs identified, the lack of a comprehensive and systematic miRNA profiling associated with energy metabolism of skeletal muscle remains unraveled
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