Apical K+ channels in frog skin (Rana temporaria): Cation adsorption and voltage influence gating kinetics

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Abstract
Open-close kinetics of fluctuating K+ channels in the apical frog skin membrane were studied with noise analysis of the K+ current (I K). The mucosa to serosa directedI K was obtained with serosal NaCl-and mucosal KCl-Ringer under voltage clamp conditions. Mucosal protons (pH>4), several polyvalent metal ions, and choline shifted the plateaus (S 0) of the Lorentzian component in theI K noise spectrum to higher, but the corner frequency (f c) to lower values.S 0 was lowered at pH4) and choline did not affectI K. A slight reduction ofI K was seen with Mg2+, Mn2+, Co2+, Ni2+, Zn2+, Cu2+ and La3+. At pH>4, the H+-induced shifts inS o anf c were almost abolished in solutions of high mucosal Ca2+ concentrations. Clamping the transepithelial potential difference to more positive values (with respect to the serosa) shifted the Lorentzian parametersS 0 andf c in the same way as the cations did. As with protons, mucosal Ca2+ interferred with the effect of voltage. The interference of cationic (probably fixed charge screening) and voltage effects suggests a common, more general mechanism of action, namely alterations in K+-channel fluctuation kinetics by changes in local electrical fields. On this basis, the rates for the open-close reaction of K+ channels and their mean lifetime were calculated. We found that e.g. increasing [Ca2+]0 from 1–10 mM caused no change of the mean open time, but increased the mean time “closed” of the K+ channel by a factor of about 1.5. Other mucosal cations, as well as depolarizing clamp potentials are thought to have the same effect.