Effects of substrate and hypoxia on smooth muscle metabolism and contraction

Abstract

Suprabasal heat production, oxygen consumption, and lactate production were measured, together with force, in 30-s isometric contractions of longitudinal smooth muscle from rabbit urinary bladder at 27 degrees C. Either glucose or pyruvate was provided as exogenous substrate. Under aerobic conditions with glucose as substrate, force averaged 95 mN/mm2 and heat production 121 mJ/g. Oxygen consumption (0.18 mumol/g) could account for only two-thirds of the total energy expenditure represented as heat production. The remaining one-third was accounted for by aerobic lactate production (0.36 mumol/g). When pyruvate replaced glucose as substrate, both the force developed and the total heat liberated were unchanged. Oxygen consumption, however, increased by approximately 40% (to 0.25 mumol/g) and was able to fully account for the measured heat production. The frequency of spontaneous contractions under aerobic conditions was always reduced in the presence of pyruvate. Under anaerobic conditions force was essentially unaltered, and heat production was only slightly reduced (101 mJ/g) with glucose present. Lactate production increased threefold over that under aerobic conditions. With pyruvate as substrate both force and heat production declined markedly (to less than 5% of the aerobic values). The results indicate that under aerobic conditions and with glucose as substrate, smooth muscle of rabbit urinary bladder generates about one-third of its suprabasal energy requirements through glycolysis and that glycolysis can be further accelerated under anaerobic conditions to provide sufficient energy to sustain contraction. If pyruvate replaces glucose as substrate, the metabolism shifts to being virtually all oxidative, and contraction can no longer be sustained in the absence of oxygen.