Adaptation of the transcriptional response to resistance exercise over 4 weeks of daily training

Viggars, Mark; Sutherland, Hazel; Lanmüller, Hermann; Schmoll, Martin; Bijak, Michaela; Jarvis, Jonathan C.

doi:10.1096/fj.202201418r

Cited by 18 publications

(39 citation statements)

References 72 publications

(161 reference statements)

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“…We recently reported that Myc induction specifically in muscle fibres is central to the acute mechanical loading‐induced transcriptome in the plantaris of young mice (Murach et al., 2022). A corroborating result in muscle tissue was reported with frequent resistance‐type training in rats (Viggars et al., 2022). Furthermore, the induction of Myc was recently linked to ‘biological immortality’ in hydrozoans (Pascual‐Torner et al., 2022).…”

Section: Introductionsupporting

confidence: 83%

A molecular signature defining exercise adaptation with ageing and in vivo partial reprogramming in skeletal muscle

Jones

Dimet²,

Haghani

et al. 2023

The Journal of Physiology

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Exercise promotes functional improvements in aged tissues, but the extent to which it simulates partial molecular reprogramming is unknown. Using transcriptome profiling from (1) a skeletal muscle‐specific in vivo Oct3/4, Klf4, Sox2 and Myc (OKSM) reprogramming‐factor expression murine model; (2) an in vivo inducible muscle‐specific Myc induction murine model; (3) a translatable high‐volume hypertrophic exercise training approach in aged mice; and (4) human exercise muscle biopsies, we collectively defined exercise‐induced genes that are common to partial reprogramming. Late‐life exercise training lowered murine DNA methylation age according to several contemporary muscle‐specific clocks. A comparison of the murine soleus transcriptome after late‐life exercise training to the soleus transcriptome after OKSM induction revealed an overlapping signature that included higher JunB and Sun1. Also, within this signature, downregulation of specific mitochondrial and muscle‐enriched genes was conserved in skeletal muscle of long‐term exercise‐trained humans; among these was muscle‐specific Abra/Stars. Myc is the OKSM factor most induced by exercise in muscle and was elevated following exercise training in aged mice. A pulse of MYC rewired the global soleus muscle methylome, and the transcriptome after a MYC pulse partially recapitulated OKSM induction. A common signature also emerged in the murine MYC‐controlled and exercise adaptation transcriptomes, including lower muscle‐specific Melusin and reactive oxygen species‐associated Romo1. With Myc, OKSM and exercise training in mice, as well habitual exercise in humans, the complex I accessory subunit Ndufb11 was lower; low Ndufb11 is linked to longevity in rodents. Collectively, exercise shares similarities with genetic in vivo partial reprogramming. Key points Advances in the last decade related to cellular epigenetic reprogramming (e.g. DNA methylome remodelling) toward a pluripotent state via the Yamanaka transcription factors Oct3/4, Klf4, Sox2 and Myc (OKSM) provide a window into potential mechanisms for combatting the deleterious effects of cellular ageing. Using global gene expression analysis, we compared the effects of in vivo OKSM‐mediated partial reprogramming in skeletal muscle fibres of mice to the effects of late‐life murine exercise training in muscle. Myc is the Yamanaka factor most induced by exercise in skeletal muscle, and so we compared the MYC‐controlled transcriptome in muscle to Yamanaka factor‐mediated and exercise adaptation mRNA landscapes in mice and humans. A single pulse of MYC is sufficient to remodel the muscle methylome. We identify partial reprogramming‐associated genes that are innately altered by exercise training and conserved in humans, and propose that MYC contributes to some of these responses.

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Section: Introductionsupporting

confidence: 83%

A molecular signature defining exercise adaptation with ageing and in vivo partial reprogramming in skeletal muscle

Jones

Dimet²,

Haghani

et al. 2023

The Journal of Physiology

View full text Add to dashboard Cite

show abstract

“…Muscle adaptations are thought to stem from the molecular response to each exercise session (Perry et al ., 2010; Viggars et al ., 2023), which when repeated over time leads to phenotypical differences (Chapman et al ., 2020). Our results show that a single extensive resistance exercise session in strength athletes, leads to mild changes in mitochondrial morphological variables, in the SS and to a lower extent in the SMF, associated with mitochondrial stress (Figure 6).…”

Section: Discussionmentioning

confidence: 99%

“…Phenotypical adaptations following months or years of training stem from the accumulative effect of repeated exercise over time (Perry et al ., 2010; Viggars et al ., 2023). The acute molecular cascade initiated following an acute resistance exercise bout involves the upregulation of a large number of genes including ribosomal and myogenic pathways that will support the increased synthesis of myofibrillar proteins (Bamman et al ., 2018).…”

Section: Introductionmentioning

confidence: 99%

Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes

Botella

Schytz

Pehrson

et al. 2023

Preprint

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Mitochondria are the cellular organelles responsible for resynthesising the majority of ATP. In skeletal muscle, there is an increased ATP turnover during resistance exercise to sustain the energetic demands of muscle contraction. Despite this, little is known regarding the mitochondrial characteristics of chronically strength-trained individuals and any potential pathways regulating the strength-specific mitochondrial remodelling. Here, we investigated the mitochondrial structural characteristics in skeletal muscle of strength athletes and age-matched untrained controls. The mitochondrial pool in strength athletes was characterised by increased mitochondrial cristae density, decreased mitochondrial size, and increased surface-to-volume ratio, despite similar mitochondrial volume density. We also provide a fibre-type and compartment specific assessment of mitochondria morphology in human skeletal muscle, which reveals across groups a compartment-specific influence on mitochondrial morphology that is largely independent of fibre-type. Furthermore, we show that resistance exercise leads to signs of mild mitochondrial stress, without an increase in the number of damaged mitochondria. Using publicly available transcriptomic data we show that acute resistance exercise increases the expression of markers of mitochondrial biogenesis, fission, and mitochondrial unfolded protein responses (UPRmt). Further, we observed an enrichment of the UPRmt in the basal transcriptome of strength-trained individuals. Together, these findings show that strength athletes possess a unique mitochondrial remodelling, which minimises the space required for mitochondria. We propose that the concurrent activation of markers of mitochondrial biogenesis and mitochondrial remodelling pathways (fission and UPRmt) with resistance exercise may be partially responsible for the observed mitochondrial phenotype of strength athletes.

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“…Phenotypical adaptations following months or years of training stem from the cumulative effect of repeated exercise over time (Perry et al., 2010; Viggars et al., 2023). The acute molecular cascade initiated following an acute resistance exercise bout involves the upregulation of a large number of genes including ribosomal and myogenic pathways that will support the increased synthesis of myofibrillar proteins (Bamman et al., 2018).…”

Section: Introductionmentioning

confidence: 99%

Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes

Botella

Schytz

Pehrson

et al. 2023

The Journal of Physiology

View full text Add to dashboard Cite

show abstract

Adaptation of the transcriptional response to resistance exercise over 4 weeks of daily training

Cited by 18 publications

References 72 publications

A molecular signature defining exercise adaptation with ageing and in vivo partial reprogramming in skeletal muscle

A molecular signature defining exercise adaptation with ageing and in vivo partial reprogramming in skeletal muscle

Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes

Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes

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