Abstract
Shal (Kv4) alpha-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.
Highlights
Gories as follows: noninactivating or slowly inactivating Kϩ currents, and rapidly inactivating transient currents known as “A-type” currents
We show that the fast transient current carried by Shal channels contrasts with Shaker channels from C. elegans, which express currents that are only slowly inactivating
Shal channels are typically described as operating in an hyperpolarized voltage range relative to other voltage-gated Kϩ channels [37, 52]
Summary
Gories as follows: noninactivating or slowly inactivating Kϩ currents, and rapidly inactivating transient currents known as “A-type” currents. The classical A-type currents activate at subthreshold voltages and recover from inactivation quickly compared with other Kv currents. Fast transient Kϩ currents in cardiac muscles contribute both to myocyte excitability [18] and to the fast repolarization phase of the cardiac action potential [2, 8, 19, 20]. We show that the fast transient current carried by Shal channels contrasts with Shaker channels (shk-1) from C. elegans, which express currents that are only slowly inactivating. Both Shal and Shaker channels are expressed in body wall muscle cells and in a variety of neurons. The phenotype of the shl-1 deletion mutation was manifested by an increase in muscle excitability reflected in abnormal aldicarb sensitivity, abnormal thrashing behavior, and mating deficiencies
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