MicroRNA-mRNA regulatory networking fine-tunes the porcine muscle fiber type, muscular mitochondrial respiratory and metabolic enzyme activities

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.

Genetic architecture and regulatory impact on hepatic microRNA expression linked to immune and metabolic traits

“…miR-34a is an obesity-associated miRNA that attenuates metabolic hormone function [ 39 , 40 ]. It is upregulated in the Doroc pig and Göttingen Minipig obesity model [ 41 , 42 ]. In other cases, miR-34a expression has been found to be increased in human patients with liver disease and in a rat liver fibrosis model [ 43 , 44 ].…”

“…Interestingly, high-phosphorus diets enhance energy metabolism through the utilization of free fatty acids released via lipolysis of white adipose tissue [ 59 ]. Accordingly, our previous study showed that miR-34a and miR-708 are upregulated in Duroc pigs, which are more obese than Pietrain [ 42 ]. This information links miR-34a to IP and TCHO, providing evidence of a functional link between IP, energy metabolism, genetic regulation of miRNA 34a and GALP.…”

Genome-Wide Association of Myoglobin Concentrations in Pork Loins

“…This gene has been shown to be highly associated with slowtwitch and fast-twitch oxidative fibers (Liu et al, 2016). ADAM metallopeptidase domain 12 (ADAM12), a candidate in SSC 14_146 Mb has been shown to have higher expression in slow-oxidative muscle fibers in cattle (Coles et al, 2014).…”

Identification of the Key Molecular Drivers of Phosphorus Utilization Based on Host miRNA-mRNA and Gut Microbiome Interactions

“…MiRNAs also play important roles in bone metabolism, bone-related diseases, and bone cell development and function [13][14][15][16]. Previous studies demonstrated that mRNA-miRNA regulatory networks affect different phenotypes, including endometrial receptivity in cattle, divergent muscle properties such as muscle fiber type, metabolic enzyme activity, and ATP production both in vivo pigs and in vitro in cell culture [17][18][19]. In the context of PU, the miRNA(s) involved and the role of host miRNA-mRNA and microbiota interactions remain unclear.…”