Human skeletal muscle glycogen utilization in exhaustive exercise: role of subcellular localization and fibre type

Abstract

Non-technical summary During prolonged high-intensity exercise the main fuel for muscular work is glycogen, the storage form of glucose in skeletal muscle. The role of muscle glycogen in muscle function is best demonstrated by the inability to sustain prolonged high-intensity exercise when the glycogen stores are depleted. Despite this knowledge, the reason why muscle function is depressed when glycogen levels are low is still not known. We show that after prolonged exhaustive exercise the depletion of glycogen stores is dependent on its localization within the muscle cells. These results show that consideration of distinct localizations within the muscle cells may advance understanding of how and why low muscle glycogen content impairs muscle function.Abstract Although glycogen is known to be heterogeneously distributed within skeletal muscle cells, there is presently little information available about the role of fibre types, utilization and resynthesis during and after exercise with respect to glycogen localization. Here, we tested the hypothesis that utilization of glycogen with different subcellular localizations during exhaustive arm and leg exercise differs and examined the influence of fibre type and carbohydrate availability on its subsequent resynthesis. When 10 elite endurance athletes (22 ± 1 years, V O 2 max = 68 ± 5 ml kg −1 min −1 , mean ± SD) performed one hour of exhaustive arm and leg exercise, transmission electron microscopy revealed more pronounced depletion of intramyofibrillar than of intermyofibrillar and subsarcolemmal glycogen. This phenomenon was the same for type I and II fibres, although at rest prior to exercise, the former contained more intramyofibrillar and subsarcolemmal glycogen than the latter. In highly glycogen-depleted fibres, the remaining small intermyofibrillar and subsarcolemmal glycogen particles were often found to cluster in groupings. In the recovery period, when the athletes received either a carbohydrate-rich meal or only water the impaired resynthesis of glycogen with water alone was associated primarily with intramyofibrillar glycogen. In conclusion, after prolonged high-intensity exercise the depletion of glycogen is dependent on subcellular localization. In addition, the localization of glycogen appears to be influenced by fibre type prior to exercise, as well as carbohydrate availability during the subsequent period of recovery. These findings provide insight into the significance of fibre type-specific compartmentalization of glycogen metabolism in skeletal muscle during exercise and subsequent recovery.

IL-15Rα is a determinant of muscle fuel utilization, and its loss protects against obesity

“…Scale bar: 30 m. ****P Ͻ 0.0001, **P Ͻ 0.01, *P Ͻ 0.05. fatty acids. The application of an exercise-to-exhaustion protocol drastically reduces the intramuscular glycogen pools, leading to decreased glycolytic flux and low ATP synthesis (4,27). In this context, fatty acid oxidation is predominant (5,15,45) and becomes an essential fuel source for aerobic energy during the recovery phase (16).…”

“…Fatty acid oxidation plays an important role during prolonged exercise (45), marathon running or other endurance sports (5), and during postexercise recovery (16). In particular, after fatiguing conditions, triacylglycerol utilization increases to provide energy and to replenish the glycogen stores depleted during exercise (15,27). We designed an experimental protocol reproducing in vivo exercise-to-exhaustion in ex vivo EDL muscles, to promote FFA oxidation during the recovery phase.…”

Single fiber analyses of glycogen-related proteins reveal their differential association with glycogen in rat skeletal muscle

“…Thus compartmentalization is now thought to be a key feature in regulating glycogen metabolism and particle localization in skeletal muscle (21)(22)(23)27). To further this, we determined whether GBE, GS, GP, and GDE were located within the cytoplasm or bound somewhere within the fiber (e.g.. such as at a membrane, on glycogen or on contractile proteins) (15,17,19).…”

Muscle Glycogen Content Modifies SR Ca2+ Release Rate in Elite Endurance Athletes

“…SR Ca 2+ uptake rate. There is also evidence that the glycogen distribution in the muscle fiber is dependent on training status and exercise mode (28,30) and hence, it is difficult to quantify the effect of exercise on SR Ca 2+ uptake rate without considering individual and exercise factors. in SR vesicle Ca 2+ release occurred earlier after ingestion of a low CHO diet compared to the high CHO diet, indicating that total glycogen has a direct impact on SR Ca 2+ release.…”