Training‐induced acceleration of O₂ uptake on‐kinetics precedes muscle mitochondrial biogenesis in humans

Abstract

New Findings r What is the central question of this study?A few weeks of endurance training accelerate the oxygen uptake (V O 2 ) on-kinetics in humans. The main aim of the present study was to determine whether the acceleration ofV O 2 onkinetics obtained by a short period of moderate-intensity training can be explained by an intensification of mitochondrial biogenesis. r What is the main finding and its importance?We demonstrated that 5 weeks of moderate-intensity training accelerates theV O 2 on-kinetics during moderate-intensity cycling in the absence of enhanced mitochondrial biogenesis or capillarization in the trained muscles. We postulate that in the early stages of training an intensification of 'parallel activation' of oxidative phosphorylation could account for the shortening of theV O 2 on-transient.The effects of 5 weeks of moderate-intensity endurance training on pulmonary oxygen uptake kinetics (V O 2 on-kinetics) were studied in 15 healthy men (mean ± SD: age 22.7 ± 1.8 years, body weight 76.4 ± 8.9 kg and maximalV O 2 46.0 ± 3.7 ml kg −1 min −1 ). Training caused a significant acceleration (P = 0.003) ofV O 2 on-kinetics during moderate-intensity cycling (time constant of the 'primary' component 30.0 ± 6.6 versus 22.8 ± 5.6 s before and after training, respectively) and a significant decrease (P = 0.04) in the amplitude of the primary component (837 ± 351 versus 801 ± 330 ml min −1 ). No changes in myosin heavy chain distribution, muscle fibre capillarization, level of peroxisome proliferator-activated receptor γ coactivator 1α and other markers of mitochondrial biogenesis (mitochondrial DNA copy number, cytochrome c and cytochrome oxidase subunit I contents) in the vastus lateralis were found after training. A significant downregulation in the content of the sarcoplasmic reticulum ATPase 2 (SERCA2; P = 0.03) and a tendency towards a decrease in SERCA1 (P = 0.055) was found after training. The decrease in SERCA1 was positively correlated (P = 0.05) with the training-induced decrease in the gain of theV O 2 on-kinetics ( V O 2 at steady state/ power output). In the early stage of training, the acceleration inV O 2 on-kinetics during moderate-intensity cycling can occur without enhanced mitochondrial biogenesis or changes in muscle myosin heavy chain distribution and

Exercise training in chronic heart failure: improving skeletal muscle O2transport and utilization

“…In healthy skeletal muscle, faster V O 2 kinetics after endurance exercise training results primarily from improved oxidative capacity and/or allosteric regulation of mitochondrial respiration (i.e., 1"parallel activation"; Refs. 18,35,36,86,133,207,221,222,242,338,339) (see also Figs. 6 and 7).…”

Slower V˙O2 Kinetics in Older Individuals

“…These rapid increases in vasodilatory responses to exercise have been also demonstrated in humans (77). In support of the idea that endothelium-mediated mechanisms rather than adaptations requiring a longer time frame (such as increases in mitochondrial content or structural changes within the vasculature) were responsible for the improved matching of O 2 delivery to O 2 utilization observed in the aforementioned training studies (57,58), recent data from Zoladz and colleagues (89) have shown that a faster adjustment in the V O 2 kinetics response precedes changes in mitochondrial biogenesis and increases in capillarization.…”

“…These considerable improvements in measures of vascularization and endothelium-dependent vasodilation would improve the surface area for O 2 exchange, which might contribute to absence of an ''overshoot'' in the normalized [HHb]/V O 2 ratio in the trained older compared with the untrained older men. Nevertheless, despite the suggestion that improved O 2 provision to the active tissues plays a critical role in controlling the faster V O 2 kinetics observed in trained older individuals, mechanisms of intracellular control discussed in this review (34,35,40,41,68,88,89) are also to be acknowledged as ''limiting'' factors determining the rate of adjustment of oxidative phosphorylation.…”

High‐intensity interval training alters ATP pathway flux during maximal muscle contractions in humans

“…Notably, several training studies have provided some evidence indicating that regulation of muscle oxidative metabolism may be altered before any apparent changes in mitochondrial capacity (Green et al 2009, Layec et al 2013, Phillips et al 1995, Zoladz et al 2013). Phillips et al.…”

“…Some results suggest that HIT may not promote a coordinated increase in all enzymes involved in a metabolic pathway (Burgomaster et al 2006, MacDougall et al 1998), while others indicate that alterations in regulation of oxidative phosphorylation may precede changes in oxidative capacity (Green et al 2009, Layec et al 2013, Phillips et al 1995, Zoladz et al 2013), which raises a question about the influence of this type of exercise training on overall pathway fluxes in vivo . In particular, there is controversy regarding the effects of sprint training on ATP pathway flux during muscular activity (Burgomaster et al 2006, Green et al 2009, Harmer et al 2000, Jacobs et al 1987, Nevill et al 1989, Sharp et al 1986).…”