Potassium‐stimulated respiration and intracellular calcium release in frog skeletal muscle

Abstract

In 1931 Fenn showed that the respiration of frog twitch muscles increases when [K+]0 is raised. The present paper is a further study of potassium-stimulated respiration. Stimulation depends on membrane potential, since respiration is also stimulated by elevated [Rb+]0 or [Cs+]0 in direct relation to their ability to depolarize. When [K+]o is elevated to 25 mM there is an increase in respiration which is sustained for hr. If [K+]o is 30 mM or above, there is a transitory burst of stimulated respiration, followed by a decline back to the basal level. If [K+]0 is raised in steps from 20-30 mM, there may never be a burst of increased 02 consumption. Often a rise in [K+]o from 20-24 mM decreases respiration. The response to elevated [K+]0 can be blocked by divalent cations or by local anesthetics; the blocking agents do not interfere with the depolarization of the membrane. The blocking agents act rapidly; they probably take effect soon after they contact the cell membrane. Either extracellular Ca2+ or Sr2+ is important for the stimulation of respiration. The burst produced by 50 mM [K+]o is transformed into a sustained rise in respiration when [Ca2+]0 or [Sr2+ 0 are also raised. If a muscle is stimulated with 25 mM [K+]o in the absence of extracellular Ca, respiration is elevated as usual, but now the rise is transitory unless Ca2+ or Sr2+ are added back to the extracellular solution. Depolarization seems to stimulate respiration by causing the release of Ca2+ into the sarcoplasm. Since respiration is increased by a depolarization below the threshold for producing a contracture, respiration is more sensitive than contraction as an indicator of sarcoplasmic Ca concentration. A model for the relation between sarcoplasmic Ca and membrane potential is proposed. The model accounts for the time course of the stimulation of respiration and also for much of the available data on K contracture. In the model, Ca2+ is released into the sarcoplasm from a store in the cell. With depolarization, the release of Ca2+ from the store is increased, but the rate at which extracellular Ca2+ can replenish the store is decreased. The ability of the longitudinal reticulum to pump Ca2+ from the sarcoplasm does not vary with membrane potential.