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The Journal of Neuroscience, April 29, 2009, 29(17):5654-5665; doi:10.1523/JNEUROSCI.5978-08.2009

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Cellular/Molecular
The N-Terminal Domain of Slack Determines the Formation and Trafficking of Slick/Slack Heteromeric Sodium-Activated Potassium Channels

Haijun Chen,^1,2 Jack Kronengold,² Yangyang Yan,³ Valeswara-Rao Gazula,² Maile R. Brown,² Liqun Ma,¹ Gonzalo Ferreira,⁴ Youshan Yang,³ Arin Bhattacharjee,⁵ Fred J. Sigworth,³ Larry Salkoff,⁶ and Leonard K. Kaczmarek^2,3

¹Department of Biological Sciences, State University of New York at Albany, Albany, New York 12222, Departments of ²Pharmacology and ³Molecular and Cellular Physiology, Yale University School of Medicine, New Haven, Connecticut 06510, ⁴Department of Biophysics, School of Medicine, University of the Republic, Montevideo 11800, Uruguay, ⁵Department of Pharmacology and Toxicology, State University of New York at Buffalo, Buffalo, New York 14214, and ⁶Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110

Correspondence should be addressed to Leonard K. Kaczmarek, Department of Pharmacology, Yale University School of Medicine, New Haven, CT 06510. Email: leonard.kaczmarek{at}yale.edu

Potassium channels activated by intracellular Na⁺ ions (K_Na) play several distinct roles in regulating the firing patterns of neurons, and, at the single channel level, their properties are quite diverse. Two known genes, Slick and Slack, encode K_Na channels. We have now found that Slick and Slack subunits coassemble to form heteromeric channels that differ from the homomers in their unitary conductance, kinetic behavior, subcellular localization, and response to activation of protein kinase C. Heteromer formation requires the N-terminal domain of Slack-B, one of the alternative splice variants of the Slack channel. This cytoplasmic N-terminal domain of Slack-B also facilitates the localization of heteromeric K_Na channels to the plasma membrane. Immunocytochemical studies indicate that Slick and Slack-B subunits are coexpressed in many central neurons. Our findings provide a molecular explanation for some of the diversity in reported properties of neuronal K_Na channels.

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Received Dec. 16, 2008; revised April 2, 2009; accepted April 2, 2009.

Correspondence should be addressed to Leonard K. Kaczmarek, Department of Pharmacology, Yale University School of Medicine, New Haven, CT 06510. Email: leonard.kaczmarek{at}yale.edu

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