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Exercise training improves mitochondrial respiration and is associated with an altered intramuscular phospholipid signature in women with obesity
MRC/Wits Developmental Pathways for Health Research Unit, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa; Division of Exercise Science and Sports Medicine, Department of Human Biology, University of Cape Town, Cape Town, South Africa.
Division of Exercise Science and Sports Medicine, Department of Human Biology, University of Cape Town, Cape Town, South Africa; Non-communicable Diseases Research Unit, South African Medical Research Council, Cape Town, South Africa.
Umeå University, Faculty of Medicine, Department of Public Health and Clinical Medicine, Section of Sustainable Health. Hainan Tropical Ocean University, Sanya, Hainan, China.ORCID iD: 0000-0002-3075-1804
Center for Healthy Aging, Department of Biomedical Sciences, Copenhagen University, Copenhagen, Denmark; Clinical Research Centre, Medical University of Bialystok, Bialystok, Poland.
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2021 (English)In: Diabetologia, ISSN 0012-186X, E-ISSN 1432-0428, Vol. 64, no 7, p. 1642-1659Article in journal (Refereed) Published
Abstract [en]

Aims/hypothesis: We sought to determine putative relationships among improved mitochondrial respiration, insulin sensitivity and altered skeletal muscle lipids and metabolite signature in response to combined aerobic and resistance training in women with obesity.

Methods: This study reports a secondary analysis of a randomised controlled trial including additional measures of mitochondrial respiration, skeletal muscle lipidomics, metabolomics and protein content. Women with obesity were randomised into 12 weeks of combined aerobic and resistance exercise training (n = 20) or control (n = 15) groups. Pre- and post-intervention testing included peak oxygen consumption, whole-body insulin sensitivity (intravenous glucose tolerance test), skeletal muscle mitochondrial respiration (high-resolution respirometry), lipidomics and metabolomics (mass spectrometry) and lipid content (magnetic resonance imaging and spectroscopy). Proteins involved in glucose transport (i.e. GLUT4) and lipid turnover (i.e. sphingomyelin synthase 1 and 2) were assessed by western blotting.

Results: The original randomised controlled trial showed that exercise training increased insulin sensitivity (median [IQR]; 3.4 [2.0–4.6] to 3.6 [2.4–6.2] x10−5 pmol l−1 min−1), peak oxygen consumption (mean ± SD; 24.9 ± 2.4 to 27.6 ± 3.4 ml kg−1 min−1), and decreased body weight (84.1 ± 8.7 to 83.3 ± 9.7 kg), with an increase in weight (pre intervention, 87.8± 10.9 to post intervention 88.8 ± 11.0 kg) in the control group (interaction p < 0.05). The current study shows an increase in mitochondrial respiration and content in response to exercise training (interaction p < 0.05). The metabolite and lipid signature at baseline were significantly associated with mitochondrial respiratory capacity (p < 0.05) but were not associated with whole-body insulin sensitivity or GLUT4 protein content. Exercise training significantly altered the skeletal muscle lipid profile, increasing specific diacylglycerol(32:2) and ceramide(d18:1/24:0) levels, without changes in other intermediates or total content of diacylglycerol and ceramide. The total content of cardiolipin, phosphatidylcholine (PC) and phosphatidylethanolamine (PE) increased with exercise training with a decrease in the PC:PE ratios containing 22:5 and 20:4 fatty acids. These changes were associated with content-driven increases in mitochondrial respiration (p < 0.05), but not with the increase in whole-body insulin sensitivity or GLUT4 protein content. Exercise training increased sphingomyelin synthase 1 (p < 0.05), with no change in plasma-membrane-located sphingomyelin synthase 2.

Conclusions/interpretation: The major findings of our study were that exercise training altered specific intramuscular lipid intermediates, associated with content-driven increases in mitochondrial respiration but not whole-body insulin sensitivity. This highlights the benefits of exercise training and presents putative target pathways for preventing lipotoxicity in skeletal muscle, which is typically associated with the development of type 2 diabetes.

Place, publisher, year, edition, pages
Springer, 2021. Vol. 64, no 7, p. 1642-1659
Keywords [en]
Acylcarnitines, Aerobic and resistance training, Cardiolipins, Cardiorespiratory fitness, Ectopic fat, Mitochondrial biogenesis, Obesity, Phospholipid hydrolysis, Sphingomyelin, Triacylglycerol
National Category
Sport and Fitness Sciences Endocrinology and Diabetes
Identifiers
URN: urn:nbn:se:umu:diva-182159DOI: 10.1007/s00125-021-05430-6ISI: 000633274200001PubMedID: 33770195Scopus ID: 2-s2.0-85103352083OAI: oai:DiVA.org:umu-182159DiVA, id: diva2:1546305
Available from: 2021-04-21 Created: 2021-04-21 Last updated: 2023-03-24Bibliographically approved

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Zeng, YingxuHauksson, JonOlsson, TommyChorell, Elin

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