Functional heterogeneity in the early distal tubule of the Amphiuma kidney: evidence for two modes of Cl- and K+ transport across the basolateral cell membrane

Abstract

Measurements of cell volume and basolateral cell membrane potential difference (Vbl) were made simultaneously and on the same cell to study chloride and potassium transport across the basolateral cell membrane of individual cells from the Amphiuma early distal tubule or diluting segment. Two distinct types of responses of Vbl are evident when either chloride is lowered or potassium is raised in the basolateral solution. In one cell type (high basolateral conductance, HBC), these maneuvers cause large depolarizations in Vbl, suggesting that the basolateral cell membrane has significant partial conductances to both chloride and to potassium. In contrast, Vbl of another group (low basolateral conductance, LBC) is much less sensitive to the same maneuvers, indicating that the partial conductance of the basolateral cell membrane is quite low. Consistent with the difference in partial conductance is the ratio of resistances, which is immeasurably high in HBC cells and averages 1.2 +/- 0.4 in LBC cells. Increasing basolateral potassium to 98 mM causes both types to swell, with HBC cells swelling approximately two times faster than LBC cells. In both cell types, potassium-induced cell swelling is inhibited by removing chloride from the perfusion solutions. In animals kept in a low-potassium environment, the number of HBC cells is approximately equal to the number of LBC cells. The proportion of LBC cells increases following potassium adaptation. This data suggests that there are at least two types of cells present in Amphiuma early distal tubule, one cell type in which both chloride and potassium move across the basolateral cell membrane primarily via a conductive pathway and another in which the movements are mostly electroneutral, probably involving a K-Cl cotransport system, and that this heterogeneity may change in response to the metabolic state of the animal.