Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle

Author:

Picard Martin12,Gentil Benoit J.3,McManus Meagan J.2,White Kathryn4,St. Louis Kyle3,Gartside Sarah E.5,Wallace Douglas C.2,Turnbull Douglass M.167

Affiliation:

1. Mitochondrial Research Group, Institute for Ageing and Health, University of Newcastle, Newcastle upon Tyne, United Kingdom;

2. Center for Mitochondrial and Epigenomic Medicine, The Children's Hospital of Philadelphia and University of Pennsylvania, Department of Laboratory Medicine, Philadelphia, Pennsylvania;

3. Department of Neurology/Neurosurgery and Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada;

4. EM Research Services, University of Newcastle, Newcastle upon Tyne, United Kingdom;

5. Institute of Neuroscience, University of Newcastle, Newcastle upon Tyne, United Kingdom;

6. Newcastle University Centre for Brain Ageing and Vitality, Institute for Ageing and Health, University of Newcastle, Newcastle upon Tyne, United Kingdom; and

7. Wellcome Trust Centre for Mitochondrial Research, Institute for Ageing and Health, University of Newcastle, Newcastle upon Tyne, United Kingdom

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.

Publisher

American Physiological Society

Subject

Physiology (medical),Physiology

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