Single-channel Properties of IKs Potassium Channels

Overview

Journal J Gen Physiol

Specialty Physiology

Date 1998 Dec 2

PMID 9834139

Citations 70

Authors

Y Yang

F J Sigworth

Affiliations

Soon will be listed here.

Abstract

Expressed in Xenopus oocytes, KvLQT1 channel subunits yield a small, rapidly activating, voltage- dependent potassium conductance. When coexpressed with the minK gene product, a slowly activating and much larger potassium current results. Using fluctuation analysis and single-channel recordings, we have studied the currents formed by human KvLQT1 subunits alone and in conjunction with human or rat minK subunits. With low external K+, the single-channel conductances of these three channel types are estimated to be 0.7, 4.5, and 6.5 pS, respectively, based on noise analysis at 20 kHz bandwidth of currents at +50 mV. Power spectra computed over the range 0.1 Hz-20 kHz show a weak frequency dependence, consistent with current interruptions occurring on a broad range of time scales. The broad spectrum causes the apparent single-channel current value to depend on the bandwidth of the recording, and is mirrored in very "flickery" single-channel events of the channels from coexpressed KvLQT1 and human minK subunits. The increase in macroscopic current due to the presence of the minK subunit is accounted for by the increased apparent single-channel conductance it confers on the expressed channels. The rat minK subunit also confers the property that the outward single-channel current is increased by external potassium ions.

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References

Sigworth F . Interpreting power spectra from nonstationary membrane current fluctuations. Biophys J. 1981; 35(2):289-300. PMC: 1327523. DOI: 10.1016/S0006-3495(81)84790-X. View

Sigworth F . The variance of sodium current fluctuations at the node of Ranvier. J Physiol. 1980; 307:97-129. PMC: 1283036. DOI: 10.1113/jphysiol.1980.sp013426. View

Boyle M, Maclusky N, Naftolin F, Kaczmarek L . Hormonal regulation of K+-channel messenger RNA in rat myometrium during oestrus cycle and in pregnancy. Nature. 1987; 330(6146):373-5. DOI: 10.1038/330373a0. View

Murai T, Kakizuka A, Takumi T, Ohkubo H, Nakanishi S . Molecular cloning and sequence analysis of human genomic DNA encoding a novel membrane protein which exhibits a slowly activating potassium channel activity. Biochem Biophys Res Commun. 1989; 161(1):176-81. DOI: 10.1016/0006-291x(89)91577-5. View

Swanson R, Marshall J, Smith J, Williams J, Boyle M, Folander K . Cloning and expression of cDNA and genomic clones encoding three delayed rectifier potassium channels in rat brain. Neuron. 1990; 4(6):929-39. DOI: 10.1016/0896-6273(90)90146-7. View

Hausdorff S, Goldstein S, Rushin E, Miller C . Functional characterization of a minimal K+ channel expressed from a synthetic gene. Biochemistry. 1991; 30(13):3341-6. DOI: 10.1021/bi00227a025. View

Walsh K, Arena J, Kwok W, Freeman L, Kass R . Delayed-rectifier potassium channel activity in isolated membrane patches of guinea pig ventricular myocytes. Am J Physiol. 1991; 260(4 Pt 2):H1390-3. DOI: 10.1152/ajpheart.1991.260.4.H1390. View

Goldstein S, Miller C . Site-specific mutations in a minimal voltage-dependent K+ channel alter ion selectivity and open-channel block. Neuron. 1991; 7(3):403-8. DOI: 10.1016/0896-6273(91)90292-8. View

Keating M, Dunn C, Atkinson D, Timothy K, Vincent G, Leppert M . Consistent linkage of the long-QT syndrome to the Harvey ras-1 locus on chromosome 11. Am J Hum Genet. 1991; 49(6):1335-9. PMC: 1686462. View

10.

Sakagami M, Fukazawa K, Matsunaga T, Fujita H, Mori N, Takumi T . Cellular localization of rat Isk protein in the stria vascularis by immunohistochemical observation. Hear Res. 1991; 56(1-2):168-72. DOI: 10.1016/0378-5955(91)90166-7. View

11.

Heinemann S, Conti F . Nonstationary noise analysis and application to patch clamp recordings. Methods Enzymol. 1992; 207:131-48. DOI: 10.1016/0076-6879(92)07009-d. View

12.

Freeman L, Kass R . Expression of a minimal K+ channel protein in mammalian cells and immunolocalization in guinea pig heart. Circ Res. 1993; 73(5):968-73. DOI: 10.1161/01.res.73.5.968. View

13.

Attali B, Guillemare E, Lesage F, Honore E, Romey G, Lazdunski M . The protein IsK is a dual activator of K+ and Cl- channels. Nature. 1993; 365(6449):850-2. DOI: 10.1038/365850a0. View

14.

Varnum M, Busch A, Bond C, Maylie J, Adelman J . The min K channel underlies the cardiac potassium current IKs and mediates species-specific responses to protein kinase C. Proc Natl Acad Sci U S A. 1993; 90(24):11528-32. PMC: 48017. DOI: 10.1073/pnas.90.24.11528. View

15.

BLUMENTHAL E, Kaczmarek L . The minK potassium channel exists in functional and nonfunctional forms when expressed in the plasma membrane of Xenopus oocytes. J Neurosci. 1994; 14(5 Pt 2):3097-105. PMC: 6577436. View

16.

Lesage F, Attali B, Lakey J, Honore E, Romey G, Faurobert E . Are Xenopus oocytes unique in displaying functional IsK channel heterologous expression?. Recept Channels. 1993; 1(2):143-52. View

17.

Marcus D, Shen Z . Slowly activating voltage-dependent K+ conductance is apical pathway for K+ secretion in vestibular dark cells. Am J Physiol. 1994; 267(3 Pt 1):C857-64. DOI: 10.1152/ajpcell.1994.267.3.C857. View

18.

Sanguinetti M, Jiang C, Curran M, Keating M . A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell. 1995; 81(2):299-307. DOI: 10.1016/0092-8674(95)90340-2. View

19.

Wang K, Goldstein S . Subunit composition of minK potassium channels. Neuron. 1995; 14(6):1303-9. DOI: 10.1016/0896-6273(95)90277-5. View

20.

Tzounopoulos T, Guy H, Durell S, Adelman J, Maylie J . min K channels form by assembly of at least 14 subunits. Proc Natl Acad Sci U S A. 1995; 92(21):9593-7. PMC: 40848. DOI: 10.1073/pnas.92.21.9593. View