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From the Department of Physiology, Botterell Hall, Queen's University, Kingston, Ontario K7L 3N6, Canada
K+ channel gating currents are usually measured in the absence of permeating ions, when a common
feature of channel closing is a rising phase of off-gating current and slow subsequent decay. Current models of gating invoke a concerted rearrangement of subunits just before the open state to explain this very slow charge return from opening potentials. We have measured gating currents from the voltage-gated K+ channel, Kv1.5, highly overexpressed in human embryonic kidney cells. In the presence of permeating K+ or Cs+, we show, by comparison
with data obtained in the absence of permeant ions, that there is a rapid return of charge after depolarizations. Measurement of off-gating currents on repolarization before and after K+ dialysis from cells allowed a comparison
of off-gating current amplitudes and time course in the same cells. Parallel experiments utilizing the low permeability of Cs+ through Kv1.5 revealed similar rapid charge return during measurements of off-gating currents at ECs.
Such effects could not be reproduced in a nonconducting mutant (W472F) of Kv1.5, in which, by definition, ion
permeation was macroscopically absent. This preservation of a fast kinetic structure of off-gating currents on return
from potentials at which channels open suggests an allosteric modulation by permeant cations. This may arise from
a direct action on a slow step late in the activation pathway, or via a retardation in the rate of C-type inactivation.
The activation energy barrier for K+ channel closing is reduced, which may be important during repetitive action
potential spiking where ion channels characteristically undergo continuous cyclical activation and deactivation.
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