Increased intramuscular lipid synthesis and low saturation relate to insulin sensitivity in endurance-trained athletes

Abstract

Intramuscular triglyceride (IMTG) has received considerable attention as a potential mechanism promoting insulin resistance. Endurance-trained athletes have high amounts of IMTG but are insulin sensitive, suggesting IMTG content alone does not change insulin action. Recent data suggest increased muscle lipid synthesis protects against fat-induced insulin resistance. We hypothesized that rates of IMTG synthesis at rest would be increased in athletes compared with controls. Eleven sedentary men and 11 endurance-trained male cyclists participated in this study. An intravenous glucose tolerance test was performed to assess insulin action. After 3 days of dietary control and an overnight fast, [13C16]palmitate was infused at 0.0174 micromol.kg(-1).min(-1) for 4 h, followed by a muscle biopsy to measure isotope incorporation into IMTG and diacylglycerol. Compared with controls, athletes were twice as insulin sensitive (P=0.004) and had a significantly greater resting IMTG concentration (athletes: 20.4+/-1.6 microg IMTG/mg dry wt, controls: 14.5+/-1.8 microg IMTG/mg dry wt, P=0.04) and IMTG fractional synthesis rate (athletes: 1.56+/-0.37%/h, controls: 0.61+/-0.15%/h, P=0.03). Stearoyl-CoA desaturase 1 mRNA expression (P=0.02) and protein content (P=0.03) were also significantly greater in athletes. Diacylglycerol, but not IMTG, saturation was significantly less in athletes compared with controls (P=0.002). These data indicate endurance-trained athletes have increased synthesis rates of skeletal muscle IMTG and decreased saturation of skeletal muscle diacylglycerol. Increased synthesis rates are not due to recovery from exercise and are likely adaptations to chronic endurance exercise training.

Fig. 1.

Plasma palmitate enrichment over time during the last 30 min of the 4-h infusion in endurance-trained athletes and control subjects. Values are means ± SE. MPE, mole percent excess.

Fig. 2.

Intramuscular triglyceride concentration (IMTG; A) and fractional synthesis rate (FSR; B) in endurance-trained athletes and control subjects after an overnight fast at rest. Values are means ± SE. §P < 0.05, significantly different from control subjects.

Fig. 3.

IMTG (A), diacylglycerol (DAG; B), and phospholipid (C) %saturation and composition in endurance-trained athletes and control subjects after an overnight fast at rest. D: significant relationship between DAG %saturation and insulin sensitivity (Si). Values are means ± SE. §P < 0.05, significantly different from control subjects.

Fig. 4.

Skeletal muscle mRNA expression of stearoyl-CoA desaturase 1 (SCD1), diacylglycerol acyltransferase 1 (DGAT1), adipose triglyceride lipase (ATGL), sterol regulatory element binding protein 1c (SREBP1c), and peroxisome proliferator-activated receptor-α (PPAR-α) and -γ (PPAR-γ) in sedentary control subjects and endurance-trained athletes. RNA expression data were normalized to levels of ribosomal protein L13a and ubiquitin C using the comparative threshold cycle method. Values are means ± SE. §P < 0.05, significantly different from control subjects.

Fig. 5.

Protein content of SCD1 in endurance-trained athletes and sedentary control subjects. Values are means ± SE. §P < 0.05, significantly different from control subjects. AU, arbitrary units.