K+-induced swelling of the dogfish shark (Squalus acanthias) rectal gland cells is associated with changes of the cytoskeleton

Abstract

Dogfish shark (Squalus acanthias) rectal gland cells swell massively when incubated in elasmobranch media in which Na+ was equivalently replaced by K+; this swelling was abolished when the impermeant gluconate replaced Cl-, while the cell depolarization was comparable in both media. The K+-effect was associated with (a) an increase of the steady-state 42K (and 86Rb) efflux (particularly of the rate constant of the fast cellular efflux component) and a rearrangement of the respective cellular pools of K+; (b) an alteration of cell morphology and the pattern of the F-actin staining along the basolateral cell membrane as revealed with fluorescent analogs of phallacidin. These changes were independent of cell volume, being identical in KCl and K-gluconate media. The observations were specific for K+ (and Rb+): replacement of media Na+ by Li+ (which is not actively extruded by the cells), or the presence of ouabain, produced only minor swelling without affecting cell morphology and F-acting distribution. The results are consistent with the following view: as opposed to Na+ or Li+ media, the K+-induced changes of the cortical F-actin component of the cytoskeleton permit the observed massive cell swelling due to the osmotic contribution of intracellular impermeant anion(s).