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J Neurophysiol 81: 2472-2484, 1999;
0022-3077/99 $5.00
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The Journal of Neurophysiology Vol. 81 No. 5 May 1999, pp. 2472-2484
Copyright ©1999 by the American Physiological Society

Auxiliary Hyperkinetic beta  Subunit of K+ Channels: Regulation of Firing Properties and K+ Currents in Drosophila Neurons

Wei-Dong Yao and Chun-Fang Wu

Department of Biological Sciences, University of Iowa, Iowa City, Iowa 52242

Yao, Wei-Dong and Chun-Fang Wu. Auxiliary Hyperkinetic beta  Subunit of K+ Channels: Regulation of Firing Properties and K+ Currents in Drosophila Neurons. J. Neurophysiol. 81: 2472-2484, 1999.Auxiliary Hyperkinetic beta  subunit of K+ channels: regulation of firing properties and K+ currents in Drosophila neurons. Molecular analysis and heterologous expression have shown that K+ channel beta  subunits regulate the properties of the pore-forming alpha  subunits, although how they influence neuronal K+ currents and excitability remains to be explored. We studied cultured Drosophila "giant" neurons derived from mutants of the Hyperkinetic (Hk) gene, which codes for a K+ channel beta  subunit. Whole cell patch-clamp recording revealed broadened action potentials and, more strikingly, persistent rhythmic spontaneous activities in a portion of mutant neurons. Voltage-clamp analysis demonstrated extensive alterations in the kinetics and voltage dependence of K+ current activation and inactivation, especially at subthreshold membrane potentials, suggesting a role in regulating the quiescent state of neurons that are capable of tonic firing. Altered sensitivity of Hk currents to classical K+ channel blockers (4-aminopyridine, alpha -dendrotoxin, and TEA) indicated that Hk mutations modify interactions between voltage-activated K+ channels and these pharmacological probes, apparently by changing both the intra- and extracellular regions of the channel pore. Correlation of voltage- and current-clamp data from the same cells indicated that Hk mutations affect not only the persistently active neurons, but also other neuronal categories. Shaker (Sh) mutations, which alter K+ channel alpha  subunits, increased neuronal excitability but did not cause the robust spontaneous activity characteristic of some Hk neurons. Significantly, Hk Sh double mutants were indistinguishable from Sh single mutants, implying that the rhythmic Hk firing pattern is conferred by intact Shalpha subunits in a distinct neuronal subpopulation. Our results suggest that alterations in beta  subunit regulation, rather than elimination or addition of alpha  subunits, may cause striking modifications in the excitability state of neurons, which may be important for complex neuronal function and plasticity.




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