Abstract

A unique property of mitochondria in mammalian cells is their ability to physically interact and undergo dynamic events of fusion/fission that remodel their morphology and possibly their function. In cultured cells, metabolic perturbations similar to those incurred during exercise influence mitochondrial fusion and fission processes, but it is unknown whether exercise acutely alters mitochondrial morphology and/or membrane interactions in vivo. To study this question, we subjected mice to a 3-h voluntarily exercise intervention following their normal physical activity patterns, and quantified mitochondrial morphology and membrane interactions in the soleus using a quantitative electron microscopy approach. A single exercise bout effectively decreased blood glucose (P < 0.05) and intramyocellular lipid content (P < 0.01), indicating increased muscle metabolic demand. The number of mitochondria spanning Z-lines and proportion of electron-dense contact sites (EDCS) between adjacent mitochondrial membranes were increased immediately after exercise among both subsarcolemmal (+116%, P < 0.05) and intermyofibrillar mitochondria (+191%, P < 0.001), indicating increased physical interactions. Mitochondrial morphology, and abundance of the mitochondrial pro-fusion proteins Mfn2 and OPA1 were unchanged. Collectively, these results support the notion that mitochondrial membrane dynamics are actively remodelled in skeletal muscle, which may be regulated by contractile activity and the metabolic state. Future studies are required to understand the implications of mitochondrial dynamics in skeletal muscle physiology during exercise and inactivity.

Highlights

  • IN RESPONSE TO CONTRACTION, skeletal muscle fibers undergo significant metabolic and molecular remodelling contributing to the health benefits of exercise [14]

  • Given that gene expression and hormonal mediators regulating cellular energy metabolism are under strong diurnal control [1, 17, 28], the timing of exercise interventions with the natural physical activity patterns of nocturnal laboratory animals appears essential to isolate the effect of physical activity

  • The ability of mitochondria to interact and fuse in skeletal muscle fibers is a relatively recently discovered property, and whether these processes are altered by exercise is unknown

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Summary

Introduction

IN RESPONSE TO CONTRACTION, skeletal muscle fibers undergo significant metabolic and molecular remodelling contributing to the health benefits of exercise [14]. These changes include but are not limited to translocation of glucose transporters (GLUT4) to the plasma membrane [32], allosteric activation of Ca2ϩ-sensitive mitochondrial dehydogenases [36], demethylation of mitochon-. Whether an acute bout of exercise can remodel mitochondrial membrane interactions or acutely alter mitochondrial morphology is unknown To study this question, key technical and physiological factors were considered. A quantitative high-resolution approach is required to resolve mitochondrial membrane interactions and compare key aspects of mitochondrial morphology [43]

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