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Physical Fitness and Mitochondrial Respiratory Capacity in Horse Skeletal Muscle

BACKGROUND: Within the animal kingdom, horses are among the most powerful aerobic athletic mammals. Determination of muscle respiratory capacity and control improves our knowledge of mitochondrial physiology in horses and high aerobic performance in general. METHODOLOGY/PRINCIPAL FINDINGS: We applie...

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Autores principales: Votion, Dominique-Marie, Gnaiger, Erich, Lemieux, Hélène, Mouithys-Mickalad, Ange, Serteyn, Didier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3329552/
https://www.ncbi.nlm.nih.gov/pubmed/22529950
http://dx.doi.org/10.1371/journal.pone.0034890
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author Votion, Dominique-Marie
Gnaiger, Erich
Lemieux, Hélène
Mouithys-Mickalad, Ange
Serteyn, Didier
author_facet Votion, Dominique-Marie
Gnaiger, Erich
Lemieux, Hélène
Mouithys-Mickalad, Ange
Serteyn, Didier
author_sort Votion, Dominique-Marie
collection PubMed
description BACKGROUND: Within the animal kingdom, horses are among the most powerful aerobic athletic mammals. Determination of muscle respiratory capacity and control improves our knowledge of mitochondrial physiology in horses and high aerobic performance in general. METHODOLOGY/PRINCIPAL FINDINGS: We applied high-resolution respirometry and multiple substrate-uncoupler-inhibitor titration protocols to study mitochondrial physiology in small (1.0–2.5 mg) permeabilized muscle fibres sampled from triceps brachii of healthy horses. Oxidative phosphorylation (OXPHOS) capacity (pmol O(2)•s(−1)•mg(−1) wet weight) with combined Complex I and II (CI+II) substrate supply (malate+glutamate+succinate) increased from 77±18 in overweight horses to 103±18, 122±15, and 129±12 in untrained, trained and competitive horses (N = 3, 8, 16, and 5, respectively). Similar to human muscle mitochondria, equine OXPHOS capacity was limited by the phosphorylation system to 0.85±0.10 (N = 32) of electron transfer capacity, independent of fitness level. In 15 trained horses, OXPHOS capacity increased from 119±12 to 134±37 when pyruvate was included in the CI+II substrate cocktail. Relative to this maximum OXPHOS capacity, Complex I (CI)-linked OXPHOS capacities were only 50% with glutamate+malate, 64% with pyruvate+malate, and 68% with pyruvate+malate+glutamate, and ∼78% with CII-linked succinate+rotenone. OXPHOS capacity with glutamate+malate increased with fitness relative to CI+II-supported ETS capacity from a flux control ratio of 0.38 to 0.40, 0.41 and 0.46 in overweight to competitive horses, whereas the CII/CI+II substrate control ratio remained constant at 0.70. Therefore, the apparent deficit of the CI- over CII-linked pathway capacity was reduced with physical fitness. CONCLUSIONS/SIGNIFICANCE: The scope of mitochondrial density-dependent OXPHOS capacity and the density-independent (qualitative) increase of CI-linked respiratory capacity with increased fitness open up new perspectives of integrative and comparative mitochondrial respiratory physiology.
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spelling pubmed-33295522012-04-23 Physical Fitness and Mitochondrial Respiratory Capacity in Horse Skeletal Muscle Votion, Dominique-Marie Gnaiger, Erich Lemieux, Hélène Mouithys-Mickalad, Ange Serteyn, Didier PLoS One Research Article BACKGROUND: Within the animal kingdom, horses are among the most powerful aerobic athletic mammals. Determination of muscle respiratory capacity and control improves our knowledge of mitochondrial physiology in horses and high aerobic performance in general. METHODOLOGY/PRINCIPAL FINDINGS: We applied high-resolution respirometry and multiple substrate-uncoupler-inhibitor titration protocols to study mitochondrial physiology in small (1.0–2.5 mg) permeabilized muscle fibres sampled from triceps brachii of healthy horses. Oxidative phosphorylation (OXPHOS) capacity (pmol O(2)•s(−1)•mg(−1) wet weight) with combined Complex I and II (CI+II) substrate supply (malate+glutamate+succinate) increased from 77±18 in overweight horses to 103±18, 122±15, and 129±12 in untrained, trained and competitive horses (N = 3, 8, 16, and 5, respectively). Similar to human muscle mitochondria, equine OXPHOS capacity was limited by the phosphorylation system to 0.85±0.10 (N = 32) of electron transfer capacity, independent of fitness level. In 15 trained horses, OXPHOS capacity increased from 119±12 to 134±37 when pyruvate was included in the CI+II substrate cocktail. Relative to this maximum OXPHOS capacity, Complex I (CI)-linked OXPHOS capacities were only 50% with glutamate+malate, 64% with pyruvate+malate, and 68% with pyruvate+malate+glutamate, and ∼78% with CII-linked succinate+rotenone. OXPHOS capacity with glutamate+malate increased with fitness relative to CI+II-supported ETS capacity from a flux control ratio of 0.38 to 0.40, 0.41 and 0.46 in overweight to competitive horses, whereas the CII/CI+II substrate control ratio remained constant at 0.70. Therefore, the apparent deficit of the CI- over CII-linked pathway capacity was reduced with physical fitness. CONCLUSIONS/SIGNIFICANCE: The scope of mitochondrial density-dependent OXPHOS capacity and the density-independent (qualitative) increase of CI-linked respiratory capacity with increased fitness open up new perspectives of integrative and comparative mitochondrial respiratory physiology. Public Library of Science 2012-04-18 /pmc/articles/PMC3329552/ /pubmed/22529950 http://dx.doi.org/10.1371/journal.pone.0034890 Text en Votion et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Votion, Dominique-Marie
Gnaiger, Erich
Lemieux, Hélène
Mouithys-Mickalad, Ange
Serteyn, Didier
Physical Fitness and Mitochondrial Respiratory Capacity in Horse Skeletal Muscle
title Physical Fitness and Mitochondrial Respiratory Capacity in Horse Skeletal Muscle
title_full Physical Fitness and Mitochondrial Respiratory Capacity in Horse Skeletal Muscle
title_fullStr Physical Fitness and Mitochondrial Respiratory Capacity in Horse Skeletal Muscle
title_full_unstemmed Physical Fitness and Mitochondrial Respiratory Capacity in Horse Skeletal Muscle
title_short Physical Fitness and Mitochondrial Respiratory Capacity in Horse Skeletal Muscle
title_sort physical fitness and mitochondrial respiratory capacity in horse skeletal muscle
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3329552/
https://www.ncbi.nlm.nih.gov/pubmed/22529950
http://dx.doi.org/10.1371/journal.pone.0034890
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