Effects of exercise-induced metabolic and mechanical loading on skeletal muscle mitochondrial function in male rats

Over the past decades, a growing interest in eccentric (ECC) exercise has emerged, but mitochondrial adaptations to ECC training remain poorly documented. Using an approach for manipulating mechanical and metabolic exercise power, we positioned that for the same metabolic power, training using concentric (CON) or ECC contractions would induce similar skeletal muscle mitochondrial adaptations. Sixty adult rats were randomly assigned to a control (CTRL) or three treadmill training groups running at 15 m·min^-1 for 45 min, 5 days weekly for 8 wk at targeted upward or downward slopes. Animals from the CON (+15%) and ECC30 (-30%) groups were trained at iso-metabolic power, whereas CON and ECC15 (-15%) exercised at iso-mechanical power. Assessments were made of vastus intermedius mitochondrial respiration (oxygraphy), enzymatic activities (spectrophotometry), and real-time qPCR for mRNA transcripts. Maximal rates of mitochondrial respiration were 14%-15% higher in CON and ECC30 compared with CTRL and ECC15. Apparent K_m for ADP for trained groups was 40%-66% higher than CTRL, with statistical significance reached for CON and ECC30. Complex I and citrate synthase activities were 1.6 (ECC15) to 1.8 (ECC30 and CON) times values of CTRL. Complex IV activity was higher than CTRL (P < 0.05) only for CON and ECC30. mRNA transcripts analyses showed higher TFAM, SLC25A4, CKMT2, and PPID in the ECC30 compared with CTRL. Findings confirm that training-induced skeletal muscle mitochondrial function adaptations are governed by the extent of metabolic overload irrespective of exercise modality. The distinctive ECC30 mRNA transcript pattern may reflect a cytoskeleton damage-repair or ECC adaptive cycle that differs from that of biogenesis.NEW & NOTEWORTHY Anticipating outcomes of eccentric versus concentric training is confounded by differences in mechanical efficiency. Our observations in groups of rats submitted to uphill and downhill running regimens inducing similar levels of metabolic demands or same external power outputs reaffirm that independent of modality, oxygen requirements and not external work governs skeletal muscle mitochondrial function adaptations.