Does Lower Oxidative Capacity Influence the Relative Contributions of ATP-Producing Pathways During Muscular Work in Aging?

Abstract

Although the capacity of skeletal muscle to produce ATP via oxidative phosphorylation may decrease in some muscles in older age, the influence of a lower capacity on relative use of oxidative and non-oxidative ATP production pathways in vivo during contractions is unclear. To test the hypothesis that lower oxidative capacity would yield greater non-oxidative ATP production, 19 young (10F) and 17 older (9F) adults performed knee extensor muscle contractions in a 3-tesla magnetic resonance system. Phosphorus metabolites were used to calculate oxidative capacity (rate constant of phosphocreatine recovery; k PCr, s-1) and estimate the maximal rate of oxidative ATP production (Vmax, mM·s-1) following a 24-s dynamic contraction protocol. Next, ATP production (mM·s-1) by the creatine kinase reaction (ATPCK), glycolysis (ATPGLY), and oxidative phosphorylation (ATPOX) was determined during 4 min of dynamic muscle contractions. Proton spectroscopy of deoxymyoglobin was also acquired in a subset (n = 12) and used to calculate the cytosolic partial pressure of oxygen (PO2). Young muscle had a greater k PCr (0.023±0.005s-1, mean±SD) than older muscle (0.020±0.003s-1, p = 0.033). ATPCK, ATPGLY, and ATPOX were not different by group (p ≥ 0.129), but ATPOX as %Vmax was lower in younger than older muscle (55±14%, 71±10%, respectively, p < 0.001). Intracellular oxygen availability (PO2) was not different by group (young: 2.4±0.7 Torr, n = 7; older: 3.2±1.6 Torr, n = 5, p = 0.371). These new findings suggest a bioenergetic rigidity in older muscle, such that it adapts to the energetic demand by using oxidative ATP production at a greater percentage of capacity rather than switching to an increased use of non-oxidative ATP production.