External barium influences the gating charge movement of Shaker potassium channels

External Ba2+ speeds the OFF gating currents (I-g(OFF)) of Shaker K+ channels but only upon repolarization from potentials that are expected to open the channel pore. To study this effect we used a nonconducting and noninactivating mutant of the Shaker K+ channel, ShH4-IR (W434F). External Ba2+ slightly decreases the quantity of ON gating charge (Q(ON)) upon depolarization to potentials near -30 mV but has little effect on the quantity of charge upon stepping to more hyperpolarized or depolarized potentials. More strikingly, Ba2+ significantly increases the decay rate of I-g(OFF) upon repolarization to -90 mV from potentials positive to similar to-55 mV. For Ba2+ to have this effect, the depolarizing command must be maintained for a duration that is dependent on the depolarizing potential (>4 ms at -30 mV and >1 ms at 0 mV). The actions of Ba2+ on the gating current are dose-dependent (EC(50) approximate to 0.2 mM) and are not produced by either Ca2+ or Mg2+ (2 mM). The results suggest that Ba2+ binds to a specific site on the Shaker K+ channel that destabilizes the open conformation and thus facilitates the return of gating charge upon repolarization.