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

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 characteris...

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Veröffentlicht in:The Journal of physiology 2023-07, Vol.601 (14), p.2899-2915
Hauptverfasser: Botella, Javier, Schytz, Camilla T., Pehrson, Thomas F., Hokken, Rune, Laugesen, Simon, Aagaard, Per, Suetta, Charlotte, Christensen, Britt, Ørtenblad, Niels, Nielsen, Joachim
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container_end_page 2915
container_issue 14
container_start_page 2899
container_title The Journal of physiology
container_volume 601
creator Botella, Javier
Schytz, Camilla T.
Pehrson, Thomas F.
Hokken, Rune
Laugesen, Simon
Aagaard, Per
Suetta, Charlotte
Christensen, Britt
Ørtenblad, Niels
Nielsen, Joachim
description 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. Key points Untrained individuals and strength athletes possess comparable skeletal muscle mitochondrial volume density. In contrast, strength athletes’ mitochondria are characterised by increased cristae density, decreased size and increased surface‐to‐volume ratio. Type I fibres have an increased number of mitochondrial profiles with minor differences in the mitochondrial morphological characteristics compared with type II fibres. The mitochondrial morphology is distinct across the subcellular compartments in both groups, with subsarcolemmal mitochondria being bigger
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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. Key points Untrained individuals and strength athletes possess comparable skeletal muscle mitochondrial volume density. In contrast, strength athletes’ mitochondria are characterised by increased cristae density, decreased size and increased surface‐to‐volume ratio. Type I fibres have an increased number of mitochondrial profiles with minor differences in the mitochondrial morphological characteristics compared with type II fibres. The mitochondrial morphology is distinct across the subcellular compartments in both groups, with subsarcolemmal mitochondria being bigger in size when compared with intermyofibrillar. Acute resistance exercise leads to signs of mild morphological mitochondrial stress accompanied by increased gene expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein response (UPRmt). figure legend Mitochondria are the cellular organelles responsible for resynthesising the majority of ATP. The present study aimed to investigate the mitochondrial structural characteristics of strength athletes when compared with age‐matched untrained individuals. Here we show that the mitochondria of strength athletes have an increased mitochondrial cristae density, an increased number of profiles and an increased surface‐to‐volume ratio; despite similar mitochondrial volumetric density. Furthermore, we show that human type I fibres, when compared with type II fibres, are characterised by an increased number of mitochondrial profiles without differences in their morphological characteristics. 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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. Key points Untrained individuals and strength athletes possess comparable skeletal muscle mitochondrial volume density. In contrast, strength athletes’ mitochondria are characterised by increased cristae density, decreased size and increased surface‐to‐volume ratio. Type I fibres have an increased number of mitochondrial profiles with minor differences in the mitochondrial morphological characteristics compared with type II fibres. The mitochondrial morphology is distinct across the subcellular compartments in both groups, with subsarcolemmal mitochondria being bigger in size when compared with intermyofibrillar. Acute resistance exercise leads to signs of mild morphological mitochondrial stress accompanied by increased gene expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein response (UPRmt). figure legend Mitochondria are the cellular organelles responsible for resynthesising the majority of ATP. The present study aimed to investigate the mitochondrial structural characteristics of strength athletes when compared with age‐matched untrained individuals. 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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. 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Here we show that the mitochondria of strength athletes have an increased mitochondrial cristae density, an increased number of profiles and an increased surface‐to‐volume ratio; despite similar mitochondrial volumetric density. Furthermore, we show that human type I fibres, when compared with type II fibres, are characterised by an increased number of mitochondrial profiles without differences in their morphological characteristics. 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subjects Adenosine Triphosphate - metabolism
Athletes
Biosynthesis
Cristae
cristae density
Gene expression
Humans
Mitochondria
Mitochondria - metabolism
Mitochondria, Muscle - metabolism
Morphology
Muscle contraction
Muscle, Skeletal - metabolism
Musculoskeletal system
Olympic weightlifting
Organelles
Phenotypes
Physical characteristics
Protein folding
resistance exercise
Skeletal muscle
strength
Transcriptomes
Transcriptomics
Unfolded Protein Response
title Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes
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