Time course analysis reveals gene-specific transcript and protein kinetics of adaptation to short-term aerobic exercise training in human skeletal muscle

PLoS One. 2013 Sep 12;8(9):e74098. doi: 10.1371/journal.pone.0074098. eCollection 2013.

Abstract

Repeated bouts of episodic myofibrillar contraction associated with exercise training are potent stimuli for physiological adaptation. However, the time course of adaptation and the continuity between alterations in mRNA expression and protein content are not well described in human skeletal muscle. Eight healthy, sedentary males cycled for 60 min at 80% of peak oxygen consumption (VO2peak) each day for fourteen consecutive days, resulting in an increase in VO2peak of 17.5±3.8%. Skeletal muscle biopsies were taken at baseline, and on the morning following (+16 h after exercise) the first, third, seventh, tenth and fourteenth training sessions. Markers of mitochondrial adaptation (Cyt c and COXIV expression, and citrate synthase activity) were increased within the first week of training, but the mtDNA/nDNA ratio was unchanged by two weeks of training. Accumulation of PGC-1α and ERRα protein during training suggests a regulatory role for these factors in adaptations of mitochondrial and metabolic gene expression. A subset of genes were transiently increased after one training session, but returned to baseline levels thereafter, which is supportive of the concept of transcriptional capacity being particularly sensitive to the onset of a new level of contractile activity. Thus, gene-specific temporal patterns of induction of mRNA expression and protein content are described. Our results illustrate the phenomenology of skeletal muscle plasticity and support the notion that transcript level adjustments, coupled to accumulation of encoded protein, underlie the modulation of skeletal muscle metabolism and phenotype by regular exercise.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological*
  • Adult
  • Biomarkers
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Exercise*
  • Gene Expression Regulation
  • Humans
  • Kinetics
  • Male
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Muscle, Skeletal / metabolism*
  • Oxygen Consumption
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Proteome*
  • RNA-Binding Proteins
  • Time Factors
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcription, Genetic
  • Transcriptome*
  • Young Adult

Substances

  • Biomarkers
  • Carrier Proteins
  • PPARGC1A protein, human
  • PPARGC1B protein, human
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Proteome
  • RNA-Binding Proteins
  • Transcription Factors

Grants and funding

This work was supported by a grant from Dublin City University (DJOG), the Irish Research Council for Science, Engineering and Technology (DJOG) and the European Foundation for the Study of Diabetes/Novo Nordisk European Clinical Research Programme in Adolescents with Type 2 Diabetes (DJOG), the Strategic Research Program in Diabetes at Karolinska Institutet (JRZ), Swedish Research Council (JRZ), and the European Research Council Advanced Grant Ideas Programme (JRZ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.