Endurance exercise training and high-fat diet differentially affect composition of diacylglycerol molecular species in rat skeletal muscle - PubMed (original) (raw)

Endurance exercise training and high-fat diet differentially affect composition of diacylglycerol molecular species in rat skeletal muscle

Noriaki Kawanishi et al. Am J Physiol Regul Integr Comp Physiol. 2018.

Abstract

Insulin resistance of peripheral muscle is implicated in the etiology of metabolic syndrome in obesity. Although accumulation of glycerolipids, such as triacylglycerol and diacylglycerol (DAG), in muscle contributes to insulin resistance in obese individuals, endurance-trained athletes also have higher glycerolipid levels but normal insulin sensitivity. We hypothesized that the difference in insulin sensitivity of skeletal muscle between athletes and obese individuals stems from changes in fatty acid composition of accumulated lipids. Here, we evaluated the effects of intense endurance exercise and high-fat diet (HFD) on the accumulation and composition of lipid molecular species in rat skeletal muscle using a lipidomic approach. Sprague-Dawley female rats were randomly assigned to three groups and received either normal diet (ND) in sedentary conditions, ND plus endurance exercise training, or HFD in sedentary conditions. Rats were fed ND or HFD between 4 and 12 wk of age. Rats in the exercise group ran on a treadmill for 120 min/day, 5 days/wk, for 8 wk. Soleus muscle lipidomic profiles were obtained using liquid chromatography/tandem mass spectrometry. Total DAG levels, particularly those of palmitoleate-containing species, were increased in muscle by exercise training. However, whereas the total DAG level in the muscle was also increased by HFD, the levels of DAG molecular species containing palmitoleate were decreased by HFD. The concentration of phosphatidylethanolamine molecular species containing palmitoleate was increased by exercise but decreased by HFD. Our results indicate that although DAG accumulation was similar levels in trained and sedentary obese rats, specific changes in molecular species containing palmitoleate were opposite.

Keywords: athlete’s paradox; diacylglycerol; skeletal muscle.

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Figures

Fig. 1.

Effects of endurance exercise training and high-fat diet (HFD) on maximal oxygen uptake and peroxisome proliferator-activated receptor-γ coactivator (PGC-1) protein expression in skeletal muscle. A: maximal oxygen uptake of normal diet (ND) plus sedentary (ND/Sed) rats, ND plus endurance exercise-training (ND/Ex) rats, and HFD plus sedentary (HFD/Sed) rats. B: relative protein levels of PGC-1 in soleus muscle of ND/Sed rats, ND/Ex rats, and HFD/Sed rats. Data are presented as means ± SE. *P < 0.05 compared with the ND/Sed rats by Dunnett’s multiple comparison test.

Fig. 2.

Effects of endurance exercise training and high-fat diet (HFD) on diacylglyceride (DAG) content in skeletal muscle. A: total DAG content in soleus muscle of normal (ND) plus sedentary (ND/Sed) rats, ND plus endurance exercise-training (ND/Ex) rats, and HFD plus sedentary (HFD/Sed) rats. B: heat map showing the fold change of DAG molecular species content in soleus muscle of ND/Ex and HFD/Sed rats in comparison to the corresponding values in ND/Sed rats. C: relative levels of DAG molecular species in soleus muscle of ND/Sed rats, ND/Ex rats, and HFD/Sed rats. Data are presented as mean ± SE. *P < 0.05 compared with the ND/Sed rats by Dunnett’s multiple comparison test.

Fig. 3.

Effects of endurance exercise training and high-fat diet (HFD) on triacylglyceride (TAG) content in skeletal muscle. A: total TAG content in soleus muscle of normal diet ND) plus sedentary (ND/Sed) rats, ND plus endurance exercise-training (ND/Ex) rats, and HFD plus sedentary (HFD/Sed) rats. B: heat map showing the fold change of TAG molecular species content in soleus muscle of ND/Ex and HFD/Sed rats in comparison to the corresponding values in ND/Sed rats. C: relative levels of TAG molecular species in soleus muscle of ND/Sed rats, ND/Ex rats, and HFD/Sed rats. Data are presented as means ± SE. *P < 0.05 compared with the ND/Sed rats by Dunnett’s multiple comparison test.

Fig. 4.

Effects of endurance exercise training and high-fat diet (HFD) on phosphatidylethanolamine (PE) content in skeletal muscle. A: total PE content in soleus muscle of normal diet (ND) plus sedentary (ND/Sed) rats, ND plus endurance exercise-training (ND/Ex) rats, and HFD plus sedentary (HFD/Sed) rats. B: heat map showing the fold change of PE molecular species content in soleus muscle of ND/Ex and HFD/Sed rats in comparison to the corresponding values in ND/Sed rats. C: relative levels of PE molecular species in soleus muscle of ND/Sed rats, ND/Ex rats, and HFD/Sed rats. Data are presented as means ± SE. *P < 0.05 compared with the ND/Sed rats by Dunnett’s multiple comparison test.

Fig. 5.

Effects of endurance exercise training and high-fat diet (HFD) on phosphatidylcholine (PC) content in skeletal muscle. A: total PC content in soleus muscle of normal diet (ND) plus sedentary (ND/Sed) rats, ND plus endurance exercise training (ND/Ex) rats, and HFD plus sedentary (HFD/Sed) rats. B: relative levels of PC molecular species in soleus muscle of ND/Sed rats, ND/Ex rats, and HFD/Sed rats. Data are presented as means ± SE. *P < 0.05 compared with the ND/Sed rats by Dunnett’s multiple comparison test.

Fig. 6.

Effects of endurance exercise training and high-fat diet (HFD) on mRNA expression levels of monoacylglycerol acyltransferase (MGAT) and diacylglycerol acyltransferase (DGAT) genes in skeletal muscle. Relative mRNA levels of genes of MGAT and DGAT families in soleus muscle of normal diet (ND) plus sedentary (ND/Sed) rats, ND plus endurance exercise-training (ND/Ex) rats, and HFD plus sedentary (HFD/Sed) rats. Data are presented as means ± SE. *P < 0.05 compared with the ND/Sed rats by Dunnett’s multiple comparison test.

Fig. 7.

Effects of endurance exercise training and high-fat diet (HFD) on stearoyl-CoA desaturase 1 (SCD1) mRNA and protein expression in skeletal muscle. A: SCD1 mRNA levels in soleus muscle of normal diet (ND) plus sedentary (ND/Sed) rats, ND plus endurance exercise-training (ND/Ex) rats, and HFD plus sedentary (HFD/Sed) rats. B: SCD1 protein expression levels in soleus muscle of ND/Sed rats, ND/Ex rats, and HFD/Sed rats. Data are presented as means ± SE. *P < 0.05 compared with the ND/Sed rats by Dunnett’s multiple comparison test.

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Endurance exercise training and high-fat diet differentially affect composition of diacylglycerol molecular species in rat skeletal muscle - PubMed (original) (raw)