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J. Biol. Chem., Vol. 281, Issue 41, 30725-30735, October 13, 2006

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Mutant Analysis of the Shal (Kv4) Voltage-gated Fast Transient K⁺ Channel in Caenorhabditis elegans^*

Gloria L. Fawcett, Celia M. Santi, Alice Butler, Thanawath Harris, Manuel Covarrubias, and Lawrence Salkoff^¶1

From the Department of Anatomy and Neurobiology and the ^¶Department of Genetics, Washington University School of Medicine, St. Louis, Missouri 63110 and the Department of Pathology, Anatomy, and Cell Biology, Jefferson Medical College, Thomas Jefferson University, Philadelphia, Pennsylvania 19107

Shal (Kv4) -subunits are the most conserved among the family of voltage-gated potassium channels. Previous work has shown that the Shal potassium channel subfamily underlies the predominant fast transient outward current in Drosophila neurons (Tsunoda, S., and Salkoff, L. (1995) J. Neurosci. 15, 1741–1754) and the fast transient outward current in mouse heart muscle (Guo, W., Jung, W. E., Marionneau, C., Aimond, F., Xu, H., Yamada, K. A., Schwarz, T. L., Demolombe, S., and Nerbonne, J. M. (2005) Circ. Res. 97, 1342–1350). We show that Shal channels also play a role as the predominant transient outward current in Caenorhabditis elegans muscle. Green fluorescent protein promoter experiments also revealed SHL-1 expression in a subset of neurons as well as in C. elegans body wall muscle and in male-specific diagonal muscles. The shl-1 (ok1168) null mutant removed all fast transient outward current from muscle cells. SHL-1 currents strongly resembled Shal currents in other species except that they were active in a more depolarized voltage range. We also determined that the remaining delayed-rectifier current in cultured myocytes was carried by the Shaker ortholog SHK-1. In shl-1 (ok1168) mutants there was a significant compensatory increase in the SHK-1 current. Male shl-1 (ok1168) animals exhibited reduced mating efficiency resulting from an apparent difficulty in locating the hermaphrodite vulva. SHL-1 channels are apparently important in fine-tuning complex behaviors, such as mating, that play a crucial role in the survival and propagation of the species.

Received for publication, June 16, 2006 , and in revised form, July 24, 2006.

^* This work was supported by National Institutes of Health Grants R24 RR017342-01, R01 GM067154-01A1 (to L. S.), R01 NS032337 (to M. C.), and T32 AA007463 (to T. H.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. 1 and 2.

¹ To whom correspondence should be addressed: Dept. of Anatomy and Neurobiology, Washington University School of Medicine, 660 S. Euclid Ave., St. Louis, MO 63110. Tel.: 314-362-3644; Fax: 314-362-3446; E-mail: salkoffl{at}pcg.wustl.edu.

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				P. Rojas, J. Garst-Orozco, B. Baban, J. A. de Santiago-Castillo, M. Covarrubias, and L. Salkoff Cumulative Activation of Voltage-Dependent KVS-1 Potassium Channels J. Neurosci., January 16, 2008; 28(3): 757 - 765. [Abstract] [Full Text] [PDF]

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