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Reduced efficiency, but increased fat oxidation, in mitochondria from human skeletal muscle after 24-h ultraendurance exercise.
Swedish School of Sport and Health Sciences, GIH, Department of Sport and Health Sciences, Research group for Mitokondriell funktion och metabolisk kontroll.ORCID iD: 0000-0001-9526-2967
Swedish School of Sport and Health Sciences, GIH, Department of Sport and Health Sciences, Research group for Mitokondriell funktion och metabolisk kontroll.
Swedish School of Sport and Health Sciences, GIH, Department of Sport and Health Sciences, Research group for Mitokondriell funktion och metabolisk kontroll.
Swedish School of Sport and Health Sciences, GIH, Department of Sport and Health Sciences, Research group for Mitokondriell funktion och metabolisk kontroll.
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2007 (English)In: Journal of applied physiology, ISSN 8750-7587, E-ISSN 1522-1601, Vol. 102, no 5, 1844-1849 p.Article in journal (Refereed) Published
Abstract [en]

The hypothesis that ultraendurance exercise influences muscle mitochondrial function has been investigated. Athletes in ultraendurance performance performed running, kayaking, and cycling at 60% of their peak O(2) consumption for 24 h. Muscle biopsies were taken preexercise (Pre-Ex), postexercise (Post-Ex), and after 28 h of recovery (Rec). Respiration was analyzed in isolated mitochondria during state 3 (coupled to ATP synthesis) and state 4 (noncoupled respiration), with fatty acids alone [palmitoyl carnitine (PC)] or together with pyruvate (Pyr). Electron transport chain activity was measured with NADH in permeabilized mitochondria. State 3 respiration with PC increased Post-Ex by 39 and 41% (P < 0.05) when related to mitochondrial protein and to electron transport chain activity, respectively. State 3 respiration with Pyr was not changed (P > 0.05). State 4 respiration with PC increased Post-Ex but was lower than Pre-Ex at Rec (P < 0.05 vs. Pre-Ex). Mitochondrial efficiency [amount of added ADP divided by oxygen consumed during state 3 (P/O ratio)] decreased Post-Ex by 9 and 6% (P < 0.05) with PC and PC + Pyr, respectively. P/O ratio remained reduced at Rec. Muscle uncoupling protein 3, measured with Western blotting, was not changed Post-Ex but tended to decrease at Rec (P = 0.07 vs. Pre-Ex). In conclusion, extreme endurance exercise decreases mitochondrial efficiency. This will increase oxygen demand and may partly explain the observed elevation in whole body oxygen consumption during standardized exercise (+13%). The increased mitochondrial capacity for PC oxidation indicates plasticity in substrate oxidation at the mitochondrial level, which may be of advantage during prolonged exercise.

Place, publisher, year, edition, pages
2007. Vol. 102, no 5, 1844-1849 p.
National Category
Physiology
Identifiers
URN: urn:nbn:se:gih:diva-838DOI: 10.1152/japplphysiol.01173.2006PubMedID: 17234801OAI: oai:DiVA.org:gih-838DiVA: diva2:174853
Projects
Physiology of Adventure Racing
Available from: 2010-06-17 Created: 2009-02-25 Last updated: 2017-08-18Bibliographically approved
In thesis
1. Effects of endurance exercise on mitochondrial efficiency, uncoupling and lipid oxidation in human skeletal muscle
Open this publication in new window or tab >>Effects of endurance exercise on mitochondrial efficiency, uncoupling and lipid oxidation in human skeletal muscle
2006 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

During the last years the importance of muscle mitochondria, and mitochondrial function, not only for performance but also for health has been highlighted. The main function of the mitochondria is to produce ATP by oxidative phosphorylation (coupled respiration). In skeletal muscle a substantial part of the energy is lost in non-coupled reactions, it has been estimated that non-coupled respiration accounts for as much as 20-25% of the total energy expenditure. It is now almost 10 years since the discovery of uncoupling protein 3 (UCP3), but the functional role of UCP3 in non-coupled respiration is not completely understood. The aim of this thesis was to investigate mitochondrial efficiency (P/O ratio), mitochondrial fat oxidation, non-coupled respiration (state 4) and protein expression of UCP3 in response to exercise and training in human skeletal muscle.

In study I eight healthy subjects endurance trained for 6 weeks and 9 subjects performed one exercise session (75 min). In the cycling efficiency study II, and in the study on mitochondrial lipid oxidation III, 9 healthy trained and 9 healthy untrained men participated. In study IV mitochondrial function and reactive oxygen species (ROS) production was studied in 9 elite athletes after extreme exercise, 24 hours of cycling, running and paddling.

Endurance training increased whole body oxygen uptake (VO2 peak) by 24% and muscle citrate synthase (CS) activity (marker of mitochondrial volume) by 47% (P< 0.05), but non-coupled respiration and UCP3 adjusted for mitochondrial volume were reduced (P< 0.05). One session of exercise did not affect non-coupled respiration or UCP3.

Cycling efficiency (expressed as work efficiency) was inversely related to protein expression of UCP3 (r= 0.57) and correlated to type 1 fibers (r= 0.58). Work efficiency was not influenced by training status or correlated to mitochondrial efficiency. UCP3 was 52% higher in the untrained men (P< 0.05). Mitochondrial capacity for fat oxidation was not influenced by training status, but related to fiber type composition. The hypothesis that mitochondrial fat oxidation is related to whole body lipid oxidation during low-intensity exercise was confirmed (r= 0.62).

Mitochondrial capacity for fat oxidation increased after 24 hours of exercise, whereas mitochondrial efficiency (P/O ratio) decreased. P/O ratio remained reduced also after 28 hours of recovery. Formation of ROS by isolated mitochondria increased after exercise. Non-coupled respiration (state 4), however, decreased and UCP3 tended to be reduced after recovery from ultra-endurance exercise (P= 0.07).

In conclusion: UCP3 does not follow exercise induced mitochondrial biogenesis. UCP3 is reduced by endurance training and lower in trained men compared with untrained men. Non-coupled respiration, measured in isolated mitochondria was reduced by endurance training and reduced after recovery from ultra-endurance exercise, but similar in trained and untrained men. In these studies UCP3 and non-coupled respiration follow the same pattern but are not correlated. Further studies are needed to understand the complex role of UCP3 in skeletal muscle metabolism.

Place, publisher, year, edition, pages
Department of Physiology and Pharmacology, Karolinska Institutet, 2006
Identifiers
urn:nbn:se:gih:diva-13 (URN)91-7357-059-1 (ISBN)
Public defence
2007-01-19, Aulan, GIH, 09:00 (English)
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Supervisors
Available from: 2007-01-25 Created: 2007-01-25 Last updated: 2011-05-05

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