Poster Presentation 26th Annual Lorne Proteomics Symposium 2021

Multi-Omic exploration of human skeletal muscle after endurance training identifies extensive mitochondrial biogenesis and remodelling. (#82)

Nikeisha J Caruana 1 2 , Cesare Granata 3 , Javier Botella 2 , Nicholas A Jamnick 2 , Kevin Huynh 4 , Jujiao Kuang 2 , Boris Reljic 1 , Hans A Janssen 2 , Adrienne Laskowski 3 5 , Tegan Stait 5 , Melinda T Coughlan 3 , Peter J Meikle 4 , David R Thorburn 5 , David A Stroud 1 , David Bishop 2
  1. Department of Biochemistry and Molecular Biology, Bio21, Parkville, Victoria, Australia
  2. Institute for Health and Sport, Victoria University, Melbourne, Victoria, Australia
  3. Department of Diabetes, Monash University, Melbourne, Victoria, Australia
  4. Metabolomics Laboratory, Baker Heart & Diabetes Institute, Melbourne, Victoria, Australia
  5. Murdoch Children's Research Institute, Royal Children's Hospital, Melbourne, Victoria, Australia

In addition to generating the bulk of cellular energy, mitochondria direct a vast array of biological functions essential for cellular homeostasis. Mutations affecting mitochondrial function and biogenesis can lead to a variety of pathological conditions that affect tissues of high energy demand, such as the skeletal muscle. A long-standing question in biology concerns the biogenesis of mitochondria in these tissues and its regulation in response to stress and the metabolic needs of the cellular environment. Increased need for mitochondrial energy, for example during times of increased muscle contraction, represents a major challenge to both these pathways, with exercise being arguably one of the most ‘natural’ perturbations experienced by our tissues. Despite this, there has been little study into exactly how mitochondria adapt to changing demands of the host tissue. In order to further explore the effects exercise has on the mitochondria within skeletal muscle, ten participants performed three different training volumes over 12 weeks. Training phases included a combination of normal-, high- and reduced-volume training regimens, with muscle biopsies taken following each phase. A combination of RNA-seq, quantitative proteomics, and lipidomics was performed on tissue biopsies and mitochondrial isolates, allowing for a holistic visualisation of the effects that exercise has on the mitochondria and associated pathways. Surprisingly, the significant changes in tissue respiratory capacity with increasing exercise volume could be attributed to an increase in mitochondrial content, rather than an increase in the efficiency of mitochondrial respiration within mitochondria. To accommodate extensive biogenesis of new mitochondria, we found that mitochondria initially prioritise tricarboxylic acid cycle linked fatty acid oxidation, with biogenesis of oxidative phosphorylation (OXPHOS) complexes peaking at high volumes of exercise. Related transcripts as well as proteins involved in the biogenesis of OXPHOS complexes preceded this phase, peaking following normal volume training, suggesting the delay is related to biogenesis and assembly of the complexes. Although we observed an increase in abundance of cardiolipins with exercise volume, a lipid solely found within the membranes of mitochondria, we found that at high volumes the dominant tetra-linoleoyl cardiolipin was supplanted by other species. Cessation of high-volume exercise rapidly reversed most, but not all of these changes. Our findings therefore provide important insights into how tissues accommodate the acute proliferation of mitochondria while maintaining the need for uninterrupted energy supply.