Xenopus oocyte K+ current. III. Phorbol esters and pH regulate current at gap junctions.

Xenopus follicles consist of a single large oocyte surrounded by a monolayer of follicle cells attached to the oocyte by gap junctions. Adenosine 3',5'-cyclic monophosphate (cAMP) activates an outward K+ current which is completely abolished if follicle cells are removed or if phorbol esters (which have been reported to reduce gap junctional conductance) are added. In this study we show that phorbol esters do not reduce cAMP levels in follicles and that acid pH, another known stimulus for reducing gap junctional conductance, mimics the action of phorbol esters to inhibit the cAMP-stimulated K+ current. We also examined electrical coupling between oocytes of pairs of follicles placed in physical contact (across 2 oocyte-follicle cell and 1 follicle cell-follicle cell gap junction). Phorbol esters and acid pH (5.5-6.5) decreased electrical coupling without eliciting a shunt current, since slope conductance of current-voltage curves recorded during voltage clamp was simultaneously decreased. Increasing cAMP, which has been reported to enhance gap junctional conductance in mammalian cells, increased slope conductance without decreasing electrical coupling between pairs of follicles. The data suggest that cAMP increases and phorbol esters and acid pH decrease K+ currents at least in part by effects on gap junctions. The effects of phorbol esters and acid pH to reduce electrical coupling between oocytes cannot be due to blockade of K+ channels, since such an action would increase electrical coupling (as verified by computer simulations). These findings are consistent with the idea that cAMP-activated K+ currents originate in follicle cells and are communicated to the oocyte via gap junctions.