Reduced efficiency, but increased fat oxidation, in mitochondria from human skeletal muscle after 24-h ultraendurance exercise

Abstract

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.

Measurement of β-oxidation capacity of biological samples by respirometry: a review of principles and substrates

“…For example, changes in ETS and OXPHOS capacities, which are observed after exercise training in muscle (16,73), implicate changes in substrate oxidation and ATP synthesis machinery, respectively, whereas an alteration in LEAK state implicates a change in proton conductance (8,22,52). The difference between ETS and OXPHOS capacities (ETS-OXPHOS) is called excess capacity and reveals the extent to which the phosphorylating system limits OXPHOS capacity (23).…”

High fatty acid oxidation capacity and phosphorylation control despite elevated leak and reduced respiratory capacity in northern elephant seal muscle mitochondria

“…Conversely, a similar oversupply of fatty-acid-derived reducing equivalents unmatched by ATP demand occurs transiently immediately following acute aerobic exercise, leading to brief periods of mitochondrial ROS release (Anderson et al, 2007). This 'physiological' ROS release triggers UCP3 activity/expression and induces respiratory uncoupling, which limits subsequent ROS emission during fatty-acid-supported respiration and enhances fatty acid OXPHOS capacity in muscle mitochondria (Pilegaard et al, 2000;Anderson et al, 2007;Fernstrom et al, 2007).…”

Mitochondrial Proteomics: From Structure to Function

“…However, it is important to observe that excessive ROS production can negatively influence exercise performance and can also lead to long-term health consequences (Bailey et al, 2004;Sahlin et al, 2010;Sun et al, 2010). The mechanism of increased ROS production during exercise is not totally clear, but experimental evidence suggests that mitochondria are the main source of ROS production during exercise (Di Meo & Venditti, 2001;Fernstrom et al, 2007). ROS levels are also described as depending on oxygen concentrations, and an additional electron accepted during energy production is used to create superoxide, a more reactive form of oxygen, which can be converted to hydrogen peroxide (H 2 O 2 ) (Sarsour et al, 2009).…”