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© The Rockefeller University Press, 0022-1295/1998//625/ $5.00
Journal of General Physiology, Volume 111, Number 5, 1998

Article

Fast Inactivation in Shaker K+ Channels

Properties of Ionic and Gating Currents



Michel J. Roux*, Riccardo Olcese*, Ligia Toro*,{ddagger}, Francisco Bezanilla*,§, and Enrico Stefani*,§,||

From the * Department of Anesthesiology, {ddagger} Department of Molecular and Medical Pharmacology, and § Department of Physiology, University of California, Los Angeles, Los Angeles, California 90095-1778; and || Conicet, Buenos Aires, Argentina 1033

Fast inactivating Shaker H4 potassium channels and nonconducting pore mutant Shaker H4 W434F channels have been used to correlate the installation and recovery of the fast inactivation of ionic current with changes in the kinetics of gating current known as "charge immobilization" (Armstrong, C.M., and F. Bezanilla. 1977. J. Gen. Physiol. 70:567–590.). Shaker H4 W434F gating currents are very similar to those of the conducting clone recorded in potassium-free solutions. This mutant channel allows the recording of the total gating charge return, even when returning from potentials that would largely inactivate conducting channels. As the depolarizing potential increased, the OFF gating currents decay phase at –90 mV return potential changed from a single fast component to at least two components, the slower requiring ~200 ms for a full charge return. The charge immobilization onset and the ionic current decay have an identical time course. The recoveries of gating current (Shaker H4 W434F) and ionic current (Shaker H4) in 2 mM external potassium have at least two components. Both recoveries are similar at –120 and –90 mV. In contrast, at higher potentials (–70 and –50 mV), the gating charge recovers significantly more slowly than the ionic current. A model with a single inactivated state cannot account for all our data, which strongly support the existence of "parallel" inactivated states. In this model, a fraction of the charge can be recovered upon repolarization while the channel pore is occupied by the NH2-terminus region.

Key Words: gating currents • K+ channels • fast inactivation • charge immobilization

Address correspondence to Dr. Enrico Stefani, UCLA, Dept. of Anesthesiology, BH-612 CHS, Box 951778, Los Angeles, CA 90095-1778. Fax: 310-825-6649; E-mail: estefani{at}ucla.edu

Abbreviations: C, closed state; HP, holding potential; I, inactivated state; MES, methanesulfonic acid; NMDG, N-methyl- D-glucamine; O, open state; SHP, subtracting holding potential


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