Exercise training modifies skeletal muscle clock gene expression but not 24‐hour rhythmicity in substrate metabolism of men with insulin resistance

Dec 5, 2023The Journal of physiology

Exercise changes muscle clock gene activity but not daily patterns of fuel use in men with insulin resistance

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Abstract

Exercise training for 12 weeks did not lead to changes in 24-hour substrate metabolism or energy expenditure in men with .

Insulin resistance is associated with reduced flexibility in whole-body substrate metabolism and disruptions in the skeletal muscle molecular circadian clock.
Exercise training improved body composition and exercise capacity without resulting in weight loss.
Plasma glucose levels decreased over 24 hours following exercise training, but free fatty acid and triacylglycerol levels remained unchanged.
Muscle expression exhibited changes particularly around the timing of exercise training, with some genes showing a time and exercise interaction.
Mitochondrial respiration increased after exercise training, yet did not show diurnal variation.
Future research should explore different exercise timings or alternative interventions to enhance metabolic flexibility in insulin-resistant individuals.

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Twenty-four hour rhythmicity in whole-body substrate metabolism, skeletal muscle expression and mitochondrial respiration is compromised upon . With exercise training known to ameliorate insulin resistance, our objective was to test if exercise training can reinforce diurnal variation in whole-body and skeletal muscle metabolism in men with insulin resistance. In a single-arm longitudinal design, 10 overweight and obese men with insulin resistance performed 12 weeks of recurrently in the afternoon (between 14.00 and 18.00 h) and were tested pre- and post-exercise training, while staying in a metabolic research unit for 2 days under free-living conditions with regular meals. On the second days, indirect calorimetry was performed at 08.00, 13.00, 18.00, 23.00 and 04.00 h, muscle biopsies were taken from the vastus lateralis at 08.30, 13.30 and 23.30 h, and blood was drawn at least bi-hourly over 24 h. Participants did not lose body weight over 12 weeks, but improved body composition and exercise capacity. Exercise training resulted in reduced 24-h plasma glucose levels, but did not modify free fatty acid and triacylglycerol levels. Diurnal variation of muscle clock gene expression was modified by exercise training with period genes showing an interaction (time × exercise) effect and reduced mRNA levels at 13.00 h. Exercise training increased mitochondrial respiration without inducing diurnal variation. Twenty-four-hour substrate metabolism and energy expenditure remained unchanged. Future studies should investigate alternative exercise strategies or types of interventions (e.g. diet or drugs aiming at improving insulin sensitivity) for their capacity to reinforce diurnal variation in substrate metabolism and mitochondrial respiration. KEY POINTS: Insulin resistance is associated with blunted 24-h flexibility in whole-body substrate metabolism and skeletal muscle mitochondrial respiration, and disruptions in the skeletal muscle molecular circadian clock. We hypothesized that exercise training modifies 24-h rhythmicity in whole-body substrate metabolism and diurnal variation in skeletal muscle molecular clock and mitochondrial respiration in men with insulin resistance. We found that metabolic inflexibility over 24 h persisted after exercise training, whereas mitochondrial respiration increased independent of time of day. Gene expression of Per1-3 and Rorα in skeletal muscle changed particularly close to the time of day at which exercise training was performed. These results provide the rationale to further investigate the differential metabolic impact of differently timed exercise to treat metabolic defects of insulin resistance that manifest at a particular time of day.

Key numbers

0.039

Decrease in 24-h Plasma Glucose Levels

Statistical significance for 24-h glucose levels post-training.

10%

Increase in Maximal Power Output

Maximal power output increased from pre- to post-exercise training.

64 ± 6 years

Participant Age

Mean age of participants in the study.

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Exercise training modifies skeletal muscle clock gene expression but not 24‐hour rhythmicity in substrate metabolism of men with insulin resistance

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