High-intensity training induces non-stoichiometric changes in the mitochondrial proteome of human skeletal muscle without reorganisation of respiratory chain content

Granata, Cesare; Caruana, Nikeisha J.; Botella, Javier; Jamnick, Nicholas A.; Huynh, Kevin; Kuang, Jujiao; Janssen, Hans A.; Reljić, Boris; Mellett, Natalie A.; Laskowski, Adrienne; Stait, Tegan; Frazier, Ann E; Coughlan, Melinda T.; Meikle, Peter J.; Thorburn, David R.; Stroud, David A.; Bishop, David J.

doi:10.1038/s41467-021-27153-3

Cited by 58 publications

(48 citation statements)

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“…Nine healthy male participants ( Table 1 ) completed 20 days of twice-a-day high-intensity interval training (HIIT) as part of a larger study design, as previously published [ 32 , 33 ]. The exercise sessions consisted of 7 to 10 4-min intervals at a starting intensity of 50% of the power output between the lactate threshold and peak power in the GXT.…”

Section: Methodsmentioning

confidence: 99%

Exercise and Training Regulation of Autophagy Markers in Human and Rat Skeletal Muscle

Botella

Jamnick

Granata

et al. 2022

IJMS

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Autophagy is a key intracellular mechanism by which cells degrade old or dysfunctional proteins and organelles. In skeletal muscle, evidence suggests that exercise increases autophagosome content and autophagy flux. However, the exercise-induced response seems to differ between rodents and humans, and little is known about how different exercise prescription parameters may affect these results. The present study utilised skeletal muscle samples obtained from four different experimental studies using rats and humans. Here, we show that, following exercise, in the soleus muscle of Wistar rats, there is an increase in LC3B-I protein levels immediately after exercise (+109%), and a subsequent increase in LC3B-II protein levels 3 h into the recovery (+97%), despite no change in Map1lc3b mRNA levels. Conversely, in human skeletal muscle, there is an immediate exercise-induced decrease in LC3B-II protein levels (−24%), independent of whether exercise is performed below or above the maximal lactate steady state, which returns to baseline 3.5 h following recovery, while no change in LC3B-I protein levels or MAP1LC3B mRNA levels is observed. SQSTM1/p62 protein and mRNA levels did not change in either rats or humans following exercise. By employing an ex vivo autophagy flux assay previously used in rodents we demonstrate that the exercise-induced decrease in LC3B-II protein levels in humans does not reflect a decreased autophagy flux. Instead, effect size analyses suggest a modest-to-large increase in autophagy flux following exercise that lasts up to 24 h. Our findings suggest that exercise-induced changes in autophagosome content markers differ between rodents and humans, and that exercise-induced decreases in LC3B-II protein levels do not reflect autophagy flux level.

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Section: Methodsmentioning

confidence: 99%

Exercise and Training Regulation of Autophagy Markers in Human and Rat Skeletal Muscle

Botella

Jamnick

Granata

et al. 2022

IJMS

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“…Exercise is a powerful stimulus affecting skeletal muscle, leading to improvements in cardiovascular function, mitochondrial content and function, and whole-body metabolism ( Bishop et al, 2019 ; Cornelissen & Smart, 2013 ; Granata et al, 2021 ; Lavie et al, 2015 ; Philippou et al, 2019 ). The molecular basis of skeletal muscle adaptations to exercise fundamentally involve modified protein content and enzyme activity, mediated by an array of pre- and post-transcriptional processes, as well as translational and post-translational control ( Egan, Hawley & Zierath, 2016 ; Egan & Zierath, 2013 ).…”

Section: Introductionmentioning

confidence: 99%

Interpretation of exercise-induced changes in human skeletal muscle mRNA expression depends on the timing of the post-exercise biopsies

Kuang

McGinley

Lee

et al. 2022

PeerJ

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Background Exercise elicits a range of adaptive responses in skeletal muscle, which include changes in mRNA expression. To better understand the health benefits of exercise training, it is important to investigate the underlying molecular mechanisms of skeletal muscle adaptation to exercise. However, most studies have assessed the molecular events at only a few time-points within a short time frame post-exercise, and the variations of gene expression kinetics have not been addressed systematically. Methods We assessed the mRNA expression of 23 gene isoforms implicated in the adaptive response to exercise at six time-points (0, 3, 9, 24, 48, and 72 h post exercise) over a 3-day period following a single session of high-intensity interval exercise. Results The temporal patterns of target gene expression were highly variable and the expression of mRNA transcripts detected was largely dependent on the timing of muscle sampling. The largest fold change in mRNA expression of each tested target gene was observed between 3 and 72 h post-exercise. Discussion and Conclusions Our findings highlight an important gap in knowledge regarding the molecular response to exercise, where the use of limited time-points within a short period post-exercise has led to an incomplete understanding of the molecular response to exercise. Muscle sampling timing for individual studies needs to be carefully chosen based on existing literature and preliminary analysis of the molecular targets of interest. We propose that a comprehensive time-course analysis on the exercise-induced transcriptional response in humans will significantly benefit the field of exercise molecular biology.

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“…In fact, bouts of recovery sleep are not always sufficient to mitigate the detrimental effects of sleep loss on metabolic health (22)(23)(24)(25). However, exercise improves glucose tolerance (26,27) and mitochondrial function (28)(29)(30)(31)(32), and can alter circadian rhythms (33,34). Data from our lab (utilising the same design as the present study) has also demonstrated that high-intensity interval (HIIE) exercise is able to mitigate the detrimental effects of sleep restriction (5 nights, 4 h TIB each night) on glucose tolerance, mitochondrial function, circadian rhythms, and both sarcoplasmic and myofibrillar protein synthesis (14,15,18).…”

Section: Introductionmentioning

confidence: 99%

The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males

et al. 2022

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BackgroundInadequate sleep is associated with many detrimental health effects, including increased risk of developing insulin resistance and type 2 diabetes. These effects have been associated with changes to the skeletal muscle transcriptome, although this has not been characterised in response to a period of sleep restriction. Exercise induces a beneficial transcriptional response within skeletal muscle that may counteract some of the negative effects associated with sleep restriction. We hypothesised that sleep restriction would down-regulate transcriptional pathways associated with glucose metabolism, but that performing exercise would mitigate these effects.Methods20 healthy young males were allocated to one of three experimental groups: a Normal Sleep (NS) group (8 h time in bed per night (TIB), for five nights (11 pm – 7 am)), a Sleep Restriction (SR) group (4 h TIB, for five nights (3 am – 7 am)), and a Sleep Restriction and Exercise group (SR+EX) (4 h TIB, for five nights (3 am – 7 am) and three high-intensity interval exercise (HIIE) sessions (performed at 10 am)). RNA sequencing was performed on muscle samples collected pre- and post-intervention. Our data was then compared to skeletal muscle transcriptomic data previously reported following sleep deprivation (24 h without sleep).ResultsGene set enrichment analysis (GSEA) indicated there was an increased enrichment of inflammatory and immune response related pathways in the SR group post-intervention. However, in the SR+EX group the direction of enrichment in these same pathways occurred in the opposite directions. Despite this, there were no significant changes at the individual gene level from pre- to post-intervention. A set of genes previously shown to be decreased with sleep deprivation was also decreased in the SR group, but increased in the SR+EX group.ConclusionThe alterations to inflammatory and immune related pathways in skeletal muscle, following five nights of sleep restriction, provide insight regarding the transcriptional changes that underpin the detrimental effects associated with sleep loss. Performing three sessions of HIIE during sleep restriction attenuated some of these transcriptional changes. Overall, the transcriptional alterations observed with a moderate period of sleep restriction were less evident than previously reported changes following a period of sleep deprivation.

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High-intensity training induces non-stoichiometric changes in the mitochondrial proteome of human skeletal muscle without reorganisation of respiratory chain content

Cited by 58 publications

References 100 publications

Exercise and Training Regulation of Autophagy Markers in Human and Rat Skeletal Muscle

Exercise and Training Regulation of Autophagy Markers in Human and Rat Skeletal Muscle

Interpretation of exercise-induced changes in human skeletal muscle mRNA expression depends on the timing of the post-exercise biopsies

The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males

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