Superior mitochondrial adaptations in human skeletal muscle after interval compared to continuous single-leg cycling matched for total work

Abstract

Key points: A classic unresolved issue in human integrative physiology involves the role of exercise intensity, duration and volume in regulating skeletal muscle adaptations to training. We employed counterweighted single-leg cycling as a unique within-subject model to investigate the role of exercise intensity in promoting training-induced increases in skeletal muscle mitochondrial content. Six sessions of high-intensity interval training performed over 2 weeks elicited greater increases in citrate synthase maximal activity and mitochondrial respiration compared to moderate-intensity continuous training matched for total work and session duration. These data suggest that exercise intensity, and/or the pattern of contraction, is an important determinant of exercise-induced skeletal muscle remodelling in humans.

Abstract: We employed counterweighted single-leg cycling as a unique model to investigate the role of exercise intensity in human skeletal muscle remodelling. Ten young active men performed unilateral graded-exercise tests to measure single-leg V̇O2, peak and peak power (Wpeak ). Each leg was randomly assigned to complete six sessions of high-intensity interval training (HIIT) [4 × (5 min at 65% Wpeak and 2.5 min at 20% Wpeak )] or moderate-intensity continuous training (MICT) (30 min at 50% Wpeak ), which were performed 10 min apart on each day, in an alternating order. The work performed per session was matched for MICT (143 ± 8.4 kJ) and HIIT (144 ± 8.5 kJ, P > 0.05). Post-training, citrate synthase (CS) maximal activity (10.2 ± 0.8 vs. 8.4 ± 0.9 mmol kg protein-1 min-1 ) and mass-specific [pmol O2 •(s•mg wet weight)-1 ] oxidative phosphorylation capacities (complex I: 23.4 ± 3.2 vs. 17.1 ± 2.8; complexes I and II: 58.2 ± 7.5 vs. 42.2 ± 5.3) were greater in HIIT relative to MICT (interaction effects, P < 0.05); however, mitochondrial function [i.e. pmol O2 •(s•CS maximal activity)-1 ] measured under various conditions was unaffected by training (P > 0.05). In whole muscle, the protein content of COXIV (24%), NDUFA9 (11%) and mitofusin 2 (MFN2) (16%) increased similarly across groups (training effects, P < 0.05). Cytochrome c oxidase subunit IV (COXIV) and NADH:ubiquinone oxidoreductase subunit A9 (NDUFA9) were more abundant in type I than type II fibres (P < 0.05) but training did not increase the content of COXIV, NDUFA9 or MFN2 in either fibre type (P > 0.05). Single-leg V̇O2, peak was also unaffected by training (P > 0.05). In summary, single-leg cycling performed in an interval compared to a continuous manner elicited superior mitochondrial adaptations in human skeletal muscle despite equal total work.

Keywords: exercise intensity; high-intensity interval training; muscle fibre.

© 2016 The Authors. The Journal of Physiology © 2016 The Physiological Society.

Figures

Figure 1. Representative western blot images for whole muscle and pooled type I and type II muscle fibres

Samples from pre‐ and post‐training muscle biopsies collected from the MICT and HIIT groups at rest were run on the same gels. Whole muscle (W) samples were run on separate gels from type I and type II muscle fibres (I and II). Protein content was normalized to total protein loaded in each lane, although only a representative image of the actin band is displayed. A calibration curve (e.g. 1, 2, 4, 8 μl) comprised of pooled (P) whole muscle samples was run on each gel. The presence and absence of MHCI and MHCIIa were used to confirm the purity of pooled muscle fibre types. [Colour figure can be viewed at wileyonlinelibrary.com]

Figure 2. Maximal CS activity in resting skeletal muscle biopsies in response to six sessions of MICT (white bars) and HIIT (black bars)

The bars represent the mean data pre‐ and post‐training, whereas individual data are displayed as grey lines. Symbols indicate a significant difference from the within‐group, pre‐training mean (§) and a significant difference between groups at the post‐training mean (†). Error bars represent the SEM (n = 9 subjects).

Figure 3. Mass‐specific and mitochondria‐specific J O2 in resting permeabilized muscle fibres in response to six sessions of MICT (white bars) and HIIT (black bars)

Bars in (A), (C) and (E) show the mean values for mass‐specific PCI, PCI&CII and E respectively, whereas the bars in (B), (D) and (F) show the mean values for mitochondria‐specific PCI, PCI&CII and E, respectively. Individual subjects are shown as grey lines. Symbols indicate a significant effect of group (#), a significant difference from the within‐group, pre‐training mean (§) and a significant difference between groups at the post‐training mean (†). Error bars represent the SEM (n = 8 subjects).

Figure 4. Protein content in resting whole muscle samples, pooled type I muscle fibres and pooled type II muscle fibres in response to six sessions of MICT (white bars) and HIIT (black bars)

COXIV (A–C), NDUFA9 (D–F) and MFN2 (G–I) are displayed separately. Whole muscle samples were normalized to the pre‐training MICT samples, whereas pooled muscle fibres were normalised to the pre‐training, type I fibre, MICT samples. Symbols indicate a significant main effect of training (*); and a significant fibre‐type difference (‡). Representative blots are displayed in Fig. 1. Error bars represent the SEM (n = 10 subjects).