Physical fitness and mitochondrial respiratory capacity in horse skeletal muscle.
Abstract: 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. Results: 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: 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.
Publication Date: 2012-04-18 PubMed ID: 22529950PubMed Central: PMC3329552DOI: 10.1371/journal.pone.0034890Google Scholar: Lookup
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Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This study investigated the relationship between physical fitness and mitochondrial respiratory capacity in horse skeletal muscle, demonstrating an increase in oxidative phosphorylation capacity with improved fitness and uncovering important insights about mitochondrial physiology in horses.
Research Methods
- The researchers used high-resolution respirometry, a method for measuring the rate of oxygen consumption, to study the mitochondrial physiology in horse muscle fibers.
- The team also used a method called multiple substrate-uncoupler-inhibitor titration protocol to effectively study mitochondria’s respiratory function.
- The study focused on small, permeabilized muscle fibres from the triceps brachii muscle of healthy horses in various fitness states, such as overweight, untrained, trained, and highly competitive horses.
Results
The researchers found that:
- The oxidative phosphorylation (the metabolic pathway that uses energy released by the oxidation of nutrients to produce adenosine triphosphate) capacity with combined Complex I and II substrate supply increased as the horses’ fitness improved.
- Regardless of the fitness level, the equine oxidative phosphorylation capacity was limited by just under 15% by the phosphorylation system – similar to human muscle mitochondria.
- In trained horses, when pyruvate was added to the substrate mixture, the oxidative phosphorylation capacity visibly increased.
- Relative to its maximum oxidative phosphorylation capacity, Complex I pathway capacities were notably less effective than the Complex II pathway.
- However, the performance of Complex I-linked oxidative phosphorylation, when powered by glutamate and malate, did improve relative to electron transfer system capacity as the physical fitness levels increased.
- The overall effectiveness of the Complex II pathway remained mostly constant throughout, regardless of increasing fitness levels.
Conclusions
- The study showed that with physical fitness, the apparent deficit of the Complex I pathway to the Complex II pathway was diminished, meaning the Complex I pathway’s capacity improved with fitness.
- The researchers concluded that the observation of a density-dependent increase in oxidative phosphorylation capacity, along with a density-independent quality increase in Complex I-linked respiratory capacity with increased fitness, suggests new understandings and perspectives on integrative and comparative mitochondrial respiratory physiology.
Cite This Article
APA
Votion DM, Gnaiger E, Lemieux H, Mouithys-Mickalad A, Serteyn D.
(2012).
Physical fitness and mitochondrial respiratory capacity in horse skeletal muscle.
PLoS One, 7(4), e34890.
https://doi.org/10.1371/journal.pone.0034890 Publication
Researcher Affiliations
- Equine European Centre of Mont-le-Soie, University of Liege, Vielsalm, Belgium. dominique.votion@ulg.ac.be
MeSH Terms
- Animals
- Electron Transport
- Electron Transport Complex I / metabolism
- Female
- Horses / physiology
- Mitochondria, Muscle / metabolism
- Muscle, Skeletal / metabolism
- Oxidative Coupling
- Oxidative Phosphorylation
Conflict of Interest Statement
The authors have read the journal's policy and have the following conflicts: Erich Gnaiger is founder and managing director of OROBOROS INSTRUMENTS, who helped this study with the loan of an apparatus (i.e. an Oxygraph-2k). There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLoS ONE policies on sharing data and materials.
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