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Skeletal muscle mitochondria contain nuclear-encoded small and long RNA species prior to and following adaptation to exercise training in rats

ABSTRACT: Mitochondria import over 1000 proteins encoded by the nuclear genome, but the RNA contained within the organelle is generally thought to be only that which is transcribed from the mitochondrial genome. Recent evidence however suggests the presence of specific nuclear-encoded small- and long-non-coding RNAs (ncRNAs) in the mitochondrial matrix, hinting at a previously underappreciated level of subcellular, ncRNA-mediated regulation on mitochondrial function. The aim of this study was to characterise the population of RNAs contained within mitochondria isolated from rat skeletal muscle, and to investigate whether it was altered in response to endurance training, a potent metabolic stimulus that induces mitochondrial adaptations. Rats underwent four weeks of moderate intensity treadmill exercise training that induced typical adaptive responses at the transcriptome and functional levels in heart and skeletal muscle. Mitochondria from gastrocnemius skeletal muscle were isolated by immunoprecipitation, further purified, then sequenced to assess the mitochondrial transcriptome. Approximately 24 nuclear-encoded, coding or non-coding ‘long’ RNAs were detected in purified mitochondria, in addition to ~50 miRNAs with >100 normalised read counts. None were differentially expressed in the exercise vs control group at FDR < 0.05, but exploratory analyses (p<0.05) pointed towards 3 differentially regulated miRNAs in the mitochondria isolated from trained compared with sedentary muscle. In conclusion, we report the presence of a small population of nuclear-encoded long- and small RNAs in the mitochondria isolated from rat muscle tissue. Further research is required to investigate how these are imported into the mitochondria, and their role(s) in regulating exercise adaptations and mitochondrial biology

ORGANISM(S): Rattus norvegicus

PROVIDER: GSE267763 | GEO | 2025/06/27

REPOSITORIES: GEO

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Project description:Methods for studying mitochondrial adaptations in skeletal muscle have mostly used whole-muscle samples, where results may be confounded by the presence of a mixture of type I and II skeletal muscle fibres. In this project, we utilised the latest Mass spectrometry (MS) techniques to provide new insights into mitochondrial adaptations in type I and II fibres in response to two different types of training – moderate-intensity-continuous training (MICT) and sprint-interval training (SIT). An 8-week training intervention was undertaken by 23 men who performed either MICT or SIT. Single muscle fibres from skeletal muscle biopsies were collected at rest, before and after the 8 weeks of training, and pooled for subsequent MS analysis. A proteomic workflow was applied that permitted a three-tiered comparison and quantification of mitochondrial proteins in different fibre types. Our protocol includes tandem mass tag labelling for increased identification of low-abundant proteins. We quantified more than 45% of known mitochondrial proteins in skeletal muscle. When comparing type I to type II fibres,24 mitochondrial proteins were differentially expressed following MICT and 10 following SIT. These altered proteins were associated with known cellular pathways within the mitochondria, including oxidative phosphorylation, the TCA cycle and fatty acid oxidation. There were distinct trends for fibre-type-specific protein responses to different types of exercise training. Following MICT proteins mostly increased in abundance in type I fibres, without analogous changes observed following SIT. This greater upregulation of mitochondrial proteins observed following MICT, suggests exercise volume is a powerful stimulus for mitochondrial adaptations. This upregulation mostly seen in type I fibres is consistent with the predominate recruitment of this fibre type with MICT. When normalised to mitochondrial content further evidence to fibre-specific non-stoichiometrically induced increases in the expression of fatty acid mitochondrial proteins is presented, highlighting mitochondria as a pivotal subcellular site in facilitating substrate utilisation to increase ATP production in type I fibres. Conversely, the research suggests very high-intensity exercise training altered the systematic biogenesis of oxidative phosphorylation (OXPHOS) components, in particular complex IV subunits of the OXPHOS pathway. These results question the existing knowledge of fibre-type-specific changes to mitochondrial proteins in response to exercise training and provide a valuable contribution to understanding the mechanisms by which exercise helps to improve health and prevent disease.

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Skeletal muscle mitochondria contain nuclear-encoded small and long RNA species prior to and following adaptation to exercise training in rats

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