Luminal and basolateral surface membranes of secretory acinar cells: electrophysiological comparison of cationic sensitivities

Abstract

Cation sensitivities (K+, Na+, and Ca2+) of luminal and basolateral membrane surfaces of secretory acinar cells were compared using a luminally perfused and externally superfused salivary gland from the aquatic snail, Helisoma trivolvis. Tight junctions delimiting the two membrane surfaces were observed near the acinar lumen suggesting that the total membrane area exposed to the superfusion solution exceeded that in contact with the luminal perfusion solution. The resting membrane potential of acinar cells was found to be dependent upon the K+ concentration in both the external superfusion and the luminal perfusion solutions. Unilateral K+ elevation at either membrane surface produced a rapid and sustained depolarization of the acinar cell. For a given K+ concentration, the level of depolarization produced by K+ elevation at the basolateral surface was significantly higher than at the luminal surface. The highest level of membrane depolarization was observed following simultaneous K+ elevation at both membrane surfaces. The ability of acinar cells to generate overshooting action potentials in response to electrical field stimulation was dependent upon both Na+ and Ca2+. Complete blockade invariably occurred following bilateral removal of either cation. The effects of unilateral removal of either Na+ or Ca2+ proved to be somewhat variable. In general, unilateral removal of Na+ was more effective in reducing the regenerative response than Ca2+ while removal of either cation from the basolateral surface was more effective in reducing the regenerative response than its removal from the luminal surface. Electrically evoked action potentials in acinar cells could also be blocked with unilateral application of the Ca2+ antagonist, cadmium (Cd2+), at either membrane surface. However, higher Cd2+ concentrations were required to achieve complete blockade when applied to the luminal than to the basolateral gland surface. This result fails to support a hypothesis of voltage-sensitive Ca2+ channels being spatially restricted to the luminal cell surface in this preparation.