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J. Biol. Chem., Vol. 278, Issue 38, 36445-36454, September 19, 2003

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A Fundamental Role for KChIPs in Determining the Molecular Properties and Trafficking of Kv4.2 Potassium Channels^*,

Riichi Shibata , Hiroaki Misonou , Claire R. Campomanes , Anne E. Anderson , Laura A. Schrader , Lisa C. Doliveira ¶, Karen I. Carroll ¶, J. David Sweatt , Kenneth J. Rhodes ¶ || and James S. Trimmer  **

From the Department of Biochemistry and Cell Biology, State University of New York, Stony Brook, New York 11794, Division of Neuroscience, Baylor College of Medicine, Houston, Texas 77030, and ^¶Neuroscience Discovery Research, Wyeth Research, Princeton, New Jersey 08543

Kv4 potassium channels regulate action potentials in neurons and cardiac myocytes. Co-expression of EF hand-containing Ca²⁺-binding proteins termed KChIPs with pore-forming Kv4 subunits causes changes in the gating and amplitude of Kv4 currents (An, W. F., Bowlby, M. R., Betty, M., Cao, J., Ling, H. P., Mendoza, G., Hinson, J. W., Mattsson, K. I., Strassle, B. W., Trimmer, J. S., and Rhodes, K. J. (2000) Nature 403, 553–556). Here we show that KChIPs profoundly affect the intracellular trafficking and molecular properties of Kv4.2 subunits. Co-expression of KChIPs1–3 causes a dramatic redistribution of Kv4.2, releasing intrinsic endoplasmic reticulum retention and allowing for trafficking to the cell surface. KChIP co-expression also causes fundamental changes in Kv4.2 steady-state expression levels, phosphorylation, detergent solubility, and stability that reconstitute the molecular properties of Kv4.2 in native cells. Interestingly, the KChIP4a isoform, which exhibits unique effects on Kv4 channel gating, does not exert these effects on Kv4.2 and negatively influences the impact of other KChIPs. We provide evidence that these KChIP effects occur through the masking of an N-terminal Kv4.2 hydrophobic domain. These studies point to an essential role for KChIPs in determining both the biophysical and molecular characteristics of Kv4 channels and provide a molecular basis for the dramatic phenotype of KChIP knockout mice.

Received for publication, June 11, 2003 , and in revised form, June 19, 2003.

^* This work was supported by National Institutes of Health Grants NS42225 (to J. S. T.) and NS37444 (to J. D. S.) and by Wyeth Research. 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 Figs. 1–3.

^|| Present address: CNS Drug Discovery, Johnson & Johnson Pharmaceutical Research and Development, L.L.C., Raritan, NJ 08869.

^** To whom correspondence should be addressed: Dept. of Pharmacology, School of Medicine, 1311 Tupper Hall, University of California, One Shields Ave., Davis, CA 95616-8635. Tel.: 530-754-6075; Fax: 530-754-6079; E-mail: jtrimmer{at}ucdavis.edu.

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