Abstract
We aimed to understand the roles of miRNAs in the muscle tissue maturation and those of circulating microRNAs (c-miRNAs) in beef production of Japanese Black (JB) cattle (Wagyu), a breed with genetically background of superior intermuscular fat depot, by comparing different feeding conditions (indoor grain-feeding vs. grazing on pasture). The cattle at 18 months old were assigned to pasture feeding or conventional indoor grain feeding conditions for 5 months. Microarray analysis of c-miRNAs from the plasma extracellular vesicles led to the detection of a total of 202 bovine miRNAs in the plasma, including 15 miRNAs that differed between the feeding conditions. Validation of the microarray results by qPCR showed that the circulating miR-10b level in the grazing cattle was upregulated compared to that of the grain-fed cattle. In contrast, the levels of miR-17-5p, miR-19b, miR-29b, miR-30b-5p, miR-98, miR-142-5p, miR-301a, miR-374b, miR-425-5p, and miR-652 were lower in the grazing cattle than in the grain-fed cattle. Bioinformatic analysis indicated that the predicted target genes of those c-miRNAs were enriched in gene ontology terms associated with blood vessel morphogenesis, plasma membrane, focal adhesion, endocytosis, collagen, ECM-receptor interaction, and phosphorylation. In the grazing cattle, the elevation of miR-10b expression in the plasma was coincident with its elevation in the longissimus lumborum (LL) muscle. Expression of bovine-specific miR-2478, the most plasma-enriched miRNA, tended to be also upregulated in the muscle but not in the plasma. Furthermore, grazing caused the downregulated mRNA expression of predicted miR-10b and/or miR-2478 target genes, such as DNAJB2, PTEN, and SCD1. Thus, the feeding system used for JB cattle affected the c-miRNAs that could be indicators of grain feeding. Among these, miR-10b expression was especially associated with feeding-induced changes and with the expression of the potential target genes responsible for glucose homeostasis and intramuscular fat depot in the LL muscle of JB cattle.
Highlights
MicroRNAs are highly conserved, noncoding small RNAs that regulate the expression of target genes in various biological processes in plants and animals [1]
Circulating miRNA profile of plasma extracellular vesicles in Japanese Black (JB) cattle To profile c-miRNAs of JB cattle fed under two different systems, we conducted microarray analysis using plasma EV precipitates prepared by ultracentrifugation
Our previous studies revealed that skeletal muscle-specific miRNAs, namely miR-1, miR-133a/b, miR-206, miR-208a/ b, miR-496, and miR-499, were abundant in the muscles of JB cattle [4], whereas none of them was detected in the plasma profiles except for a modest miR-486 content [24]
Summary
MicroRNAs (miRNAs) are highly conserved, noncoding small RNAs that regulate the expression of target genes in various biological processes in plants and animals [1]. To better understand the meat quality traits of domestic animals, skeletal muscle miRNAs have been profiled in investigations into how distinct muscle properties are specified. Some muscle miRNAs are differently expressed between muscle types [3,4] or tissues [5,6] in cattle and pigs. Since muscle physiological property determined by the muscle type have impacts on meat quality [8,9,10], potential association of miRNAs with muscle gene expression and mat quality have been focused recently [11,12,13]. Transcriptomic miRNA analyses in mammalian adipose tissue have unveiled their roles in fat accumulation. When primary cultured porcine adipocytes are exposed to miR-130b-enriched micro-vesicles, peroxisome proliferator-activated receptor γ (PPARG) expression is downregulated [19]
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