Transcriptome changes favoring intramuscular fat deposition in the longissimus muscle following castration of bulls1

Abstract

Castration increases intramuscular fat (IMF) deposition, improving beef quality in cattle. The present study was performed to determine the global transcriptome changes following castration of bulls and to identify genes associated with IMF deposition in the longissimus dorsi (LM) of Korean cattle. A customized bovine CombiMatrix oligonucleotide microarray was constructed, and transcriptome changes following castration were determined by microarray hybridization. Transcriptome comparison between bulls and steers indicated that 428 of 8,407 genes were differentially expressed in the LM by greater than two fold (P < 0.05). Gene expression profiling indicated alterations in several pathways, including adipogenesis, fatty acid oxidation, tricarboxylic acid (TCA) cycle, and oxidative phosphorylation (OP), following castration. Castration upregulated transcription of adipogenic perilipin 2 (PLIN2) and visfatin, lipogenic fatty acid synthase, fatty acid esterification 1-acylglycerol-3-phosphate O-acyltransferase 5, and many fatty acid oxidation-related genes. Many TCA cycle and OP genes were also transcriptionally upregulated. Correlation analysis indicated that the IMF content in the LM was highly correlated with mRNA levels of PLIN2 (r = 0.70, P < 0.001), adenosine triphosphatase (ATPase), H(+)-transporting, lysosomal 42 kDa, V1 subunit C1 (ATP6V1C1: r = 0.66, P < 0.001), and cytochrome c oxidase assembly homolog 11 (COX11: r = 0.72, P < 0.001) genes in a pooled animal group of steers plus bulls, and significant correlations in the steer-alone group were maintained in the 3 genes, PLIN2 (r = 0.47, P < 0.05), ATP6V1C1 (r = 0.50, P < 0.05), and COX11 (r = 0.60, P < 0.01). In conclusion, our study provided evidence that castration shifts transcription of lipid metabolism genes, favoring IMF deposition by increasing adipogenesis, lipogenesis, and triglyceride synthesis. This study also indicated that castration increases transcription of genes involved in fatty acid oxidation and subsequent energy production (TCA and OP genes). Our microarray analysis provided novel information that castration alters the transcriptome associated with lipid/energy metabolism, favoring IMF deposition in the LM.

Differential miRNA expression profiles in the longissimus dorsi muscle between intact and castrated male pigs

“…Previously, it was shown that castration of male rats increased body fat mass but reduced body lean mass (Jiao et al, 2009). Moreover, steers have lower skeletal muscle mass and higher lipid accumulation than intact bulls (Jeong et al, 2013). Similarly, in humans, men with testosterone deficiency show significant decreases in skeletal muscle mass and strength (Urban et al, 1995).…”

Integrated data mining of transcriptomic and proteomic datasets to predict the secretome of adipose tissue and muscle in ruminants

“…1) in order to propose a set of proteins putatively secreted by the adipose tissue and the skeletal muscle in ruminants. We used data from 24 publications reporting data from bovine [12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30] , ovine 18 , a free web service (www.proteinside.org) that (I) provides an overview of the biological information stored in public databases or provided by annotations according to the Gene Ontology (GO), (II) predicts proteins that are secreted to search for proteins that mediate signalization between cells or tissues, and (III) analyses protein-protein interactions to identify proteins contributing to a process or to visualize functional pathways. The "Gene Names" were thus submitted to ProteINSIDE to identify proteins putatively secreted by the adipose tissue, muscle or by both tissues (shared proteome) in ruminants.…”

Long non‐coding RNA analysis of muscular responses to testosterone deficiency in Huainan male pigs

“…Compared with control rats, body weight and lean mass decreased in castrated rats (Jiao et al 2009). Moreover, steers showed lower lean mass and higher intramuscular fat (IMF) deposition than that in bulls (Jeong et al 2013).…”

“…Compared with control rats, body weight and lean mass decreased in castrated rats (Jiao et al ). Moreover, steers showed lower lean mass and higher intramuscular fat (IMF) deposition than that in bulls (Jeong et al ). Recently, researchers have identified the mechanism underlying castration‐induced muscle reduction from transcriptome to miRNAs: in Korea cattle, castration altered the expression of genes participating in adipogenesis, fatty acid oxidation, tricarboxylic acid (TCA) cycle and oxidative phosphorylation (OP) pathway, these changes increased IMF deposition and beef quality (Jeong et al ).…”

“…Moreover, steers showed lower lean mass and higher intramuscular fat (IMF) deposition than that in bulls (Jeong et al ). Recently, researchers have identified the mechanism underlying castration‐induced muscle reduction from transcriptome to miRNAs: in Korea cattle, castration altered the expression of genes participating in adipogenesis, fatty acid oxidation, tricarboxylic acid (TCA) cycle and oxidative phosphorylation (OP) pathway, these changes increased IMF deposition and beef quality (Jeong et al ). It was reported that castration changed the expression files of miRNA in porcine LM, the seven differentially expressed miRNAs were involved in the regulation of skeletal muscle and fat metabolism (Cai et al ).…”