Time‐restricted feeding during the inactive phase abolishes the daily rhythm in mitochondrial respiration in rat skeletal muscle

Jan 15, 2022FASEB journal : official publication of the Federation of American Societies for Experimental Biology

Eating only during rest time removes daily rhythm of energy use in rat muscle

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Abstract

Rats fed during their inactive phase showed a significant disruption in mitochondrial respiration compared to those fed during their active phase.

Mitochondrial respiration exhibited a clear daily rhythm in rats with ad libitum feeding or those fed during the dark phase.
This rhythm was abolished in rats fed during the light phase, resulting in lower overall mitochondrial respiration over 24 hours.
Light-fed rats showed altered expression of genes related to mitochondrial growth and function.
Metabolomics analysis revealed that light-fed animals lost rhythmic levels of α-ketoglutarate and citric acid.
In contrast, lipidomics indicated an increase in rhythmic triglyceride levels in light-fed animals.
A mismatch was observed between expected and actual metabolic supply and demand in light-fed rats, potentially linking this to metabolic inflexibility.

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Shift-workers show an increased incidence of type 2 diabetes mellitus (T2DM). A possible mechanism is the disruption of the circadian timing of glucose homeostasis. Skeletal muscle mitochondrial function is modulated by the molecular clock. We used time-restricted feeding (TRF) during the inactive phase to investigate how mistimed feeding affects muscle mitochondrial metabolism. Rats on an ad libitum (AL) diet were compared to those that could eat only during the light (inactive) or dark (active) phase. Mitochondrial respiration, metabolic gene expressions, and metabolite concentrations were determined in the soleus muscle. Rats on AL feeding or dark-fed TRF showed a clear daily rhythm in muscle mitochondrial respiration. This rhythm in mitochondrial oxidative phosphorylation capacity was abolished in light-fed TRF animals and overall 24h respiration was lower. The expression of several genes involved in mitochondrial biogenesis and the fission/fusion machinery was altered in light-fed animals. Metabolomics analysis indicated that light-fed animals had lost rhythmic levels of α-ketoglutarate and citric acid. Contrastingly, lipidomics showed that light-fed animals abundantly gained rhythmicity in levels of triglycerides. Furthermore, while the RER shifted entirely with the food intake in the light-fed animals, many measured metabolic parameters (e.g., activity and mitochondrial respiration) did not strictly align with the shifted timing of food intake, resulting in a mismatch between expected metabolic supply/demand (as dictated by the circadian timing system and light/dark-cycle) and the actual metabolic supply/demand (as dictated by the timing of food intake). These data suggest that shift-work impairs mitochondrial metabolism and causes metabolic inflexibility, which can predispose to T2DM.

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Time‐restricted feeding during the inactive phase abolishes the daily rhythm in mitochondrial respiration in rat skeletal muscle

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