Differential effects of temperature on three components of passive permeability to potassium in rodent red cells.

The effect of temperature on ouabain-insensitive fluxes of K+ was characterized in red cells from a non-hibernator (guinea-pig) and a hibernator (thirteen-lined ground squirrel). The residual K+ influx which remains in the presence of ouabain and bumetanide, and which is linearly dependent on [K+]o was the same in the erythrocytes of the two species at low temperature (5 degrees C). At 5 degrees C co-transport of K+ was abolished in guinea-pig red cells but was still present in ground squirrel red cells. In guinea-pig cells, ouabain-and-bumetanide-insensitive K+ flux was increased by Ca2+ at low temperatures. This flux was inhibited by quinine and selective for K+ over Na+, indicating activation of the Ca2+-sensitive K+ pathway (Gárdos channel). Ouabain-and-bumetanide-insensitive K+ permeability in red cells from the ground squirrel was insensitive to Ca2+ added to the medium at low temperature. When ground squirrel red cells were depleted of ATP or treated with A23187, Ca2+ induced a flux which was inhibitable by quinine. Hence, ground squirrel red cells possess Gárdos channels. The temperature sensitivity of the K+ channels was assessed using A23187-mediated K+ influx as a measure of Gárdos channel activation. The influence of temperature on the Ca2+-stimulated K+ fluxes under these conditions was indistinguishable between the two species. It is concluded that K+ loss through the Ca2+-sensitive K+ channel is minimal in hibernators' erythrocytes because of more efficient regulation of cytoplasmic Ca2+ during cold storage.