Skeletal muscle mitochondrial protein synthesis and respiration in response to the energetic stress of an ultra-endurance race

Adam R. Konopka, William M. Castor, Christopher A. Wolff, Robert V. Musci, Justin J. Reid, Jaime L. Laurin, Zackary J. Valenti, Karyn L. Hamilton, Benjamin F. Miller

Research output: Contribution to journalArticlepeer-review

Abstract

The 2016 Colorado Trail Race (CTR) was an ultra-endurance mountain bike race in which competitors cycled for up to 24 h/day between altitudes of 1,675 and 4,025 m to complete 800 km and 21,000 m of elevation gain. In one athlete, we had the unique opportunity to characterize skeletal muscle protein synthesis and mitochondrial respiration in response to a normal activity control period (CON) and the CTR. We hypothesized that mitochondrial protein synthesis would be elevated and mitochondrial respiration would be maintained during the extreme stresses of the CTR. Titrated and bolus doses of ADP were provided to determine substrate-specific oxidative phosphorylation (OXPHOS) and electron transport system (ETS) capacities in permeabilized muscle fibers via high-resolution respirometry. Protein synthetic rates were determined by daily oral consumption of deuterium oxide (2H2O). The endurance athlete had OXPHOS (226 pmol s-1 mg tissue-1) and ETS (231 pmol s-1 mg tissue-1) capacities that rank among the highest published to date in humans. Mitochondrial (3.2-fold), cytoplasmic (2.3-fold), and myofibrillar (1.5-fold) protein synthesis rates were greater during CTR compared with CON. With titrated ADP doses, the apparent Km of ADP, OXPHOS, and ETS increased after the CTR. With provision of ADP boluses after the CTR, the addition of fatty acids (-12 and -14%) mitigated the decline in OXPHOS and ETS capacity during carbohydrate-supported respiration (-26 and -31%). In the face of extreme stresses during the CTR, elevated rates of mitochondrial protein synthesis may contribute to rapid adaptations in mitochondrial bioenergetics. NEW & NOTEWORTHY The mechanisms that maintain skeletal muscle function during extreme stresses remain incompletely understood. In the current study, greater rates of mitochondrial protein synthesis during the energetic demands of ultra-endurance exercise may contribute to rapid adaptations in mitochondrial bioenergetics. The endurance athlete herein achieved mitochondrial respiratory capacities among the highest published for humans. Greater mitochondrial protein synthesis during ultra-endurance exercise may contribute to improved mitochondrial respiration and serve as a mechanism to resist cellular energetic stresses.

Original languageEnglish (US)
Pages (from-to)1516-1524
Number of pages9
JournalJournal of Applied Physiology
Volume123
Issue number6
DOIs
StatePublished - Dec 2017

Keywords

  • Deuterium oxide
  • Endurance exercise
  • Mitochondrial bioenergetics
  • Proteostasis
  • Stress resistance

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

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