Increasing temperature speeds intracellular Po2kinetics during contractions in singleXenopusskeletal muscle fibers

Abstract

Precise determination of the effect of muscle temperature (Tm) on mitochondrial oxygen consumption kinetics has proven difficult in humans, in part due to the complexities in controlling for Tm-related variations in blood flow, fiber recruitment, muscle metabolism, and contractile properties. To address this issue, intracellular Po2(PiO2) was measured continuously by phosphorescence quenching following the onset of contractions in single Xenopus myofibers ( n = 24) while controlling extracellular temperature. Fibers were subjected to two identical contraction bouts, in random order, at 15°C (cold, C) and 20°C (normal, N; n = 12), or at N and 25°C (hot, H; n = 12). Contractile properties were determined for every contraction. The time delay of the PiO2response was significantly greater in C (59 ± 35 s) compared with N (35 ± 26 s, P = 0.01) and H (27 ± 14 s, P = 0.01). The time constant for the decline in PiO2was significantly greater in C (89 ± 34 s) compared with N (52 ± 15 s; P < 0.01) and H (37 ± 10 s; P < 0.01). There was a linear relationship between the rate constant for PiO2kinetics and Tm( r = 0.322, P = 0.03). Estimated ATP turnover was significantly greater in H than in C ( P < 0.01), but this increased energy requirement alone with increased Tmcould not account for the differences observed in PiO2kinetics among conditions. These results demonstrate that PiO2kinetics in single contracting myofibers are dependent on Tm, likely caused by temperature-induced differences in metabolic demand and by temperature-dependent processes underlying mitochondrial activation at the start of muscle contractions.