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J. Biol. Chem., Vol. 279, Issue 9, 7884-7892, February 27, 2004

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MinK, MiRP1, and MiRP2 Diversify Kv3.1 and Kv3.2 Potassium Channel Gating^*

Anthony Lewis, Zoe A. McCrossan, and Geoffrey W. Abbott¶

From the Division of Cardiology, Department of Medicine, and the Department of Pharmacology, Weill Medical College of Cornell University, New York, New York 10021

High frequency firing in mammalian neurons requires ultra-rapid delayed rectifier potassium currents generated by homomeric or heteromeric assemblies of Kv3.1 and Kv3.2 potassium channel subunits. Kv3.1 subunits can also form slower activating channels by coassembling with MinK-related peptide 2 (MiRP2), a single transmembrane domain potassium channel ancillary subunit. Here, using channel subunits cloned from rat and expressed in Chinese hamster ovary cells, we show that modulation by MinK, MiRP1, and MiRP2 is a general mechanism for slowing of Kv3.1 and Kv3.2 channel activation and deactivation and acceleration of inactivation, creating a functionally diverse range of channel complexes. MiRP1 also negatively shifts the voltage dependence of Kv3.1 and Kv3.2 channel activation. Furthermore, MinK, MiRP1, and MiRP2 each form channels with Kv3.1-Kv3.2 heteromers that are kinetically distinct from one another and from MiRP/homomeric Kv3 channels. The findings illustrate a mechanism for dynamic expansion of the functional repertoire of Kv3.1 and Kv3.2 potassium currents and suggest roles for these subunits outside the scope of sustained rapid neuronal firing.

Received for publication, September 23, 2003 , and in revised form, December 16, 2003.

^* This work was supported by the Greenberg Atrial Fibrillation Fund and a Scientist Development Grant (0235069N) from the American Heart Association (National) (to G. W. A.). 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.

^¶ To whom correspondence should be addressed: Starr 463, Division of Cardiology, Weill Medical College of Cornell University, 520 East 70th St., New York, NY 10021. Tel.: 212-746-6275; Fax: 212-746-7984; E-mail: gwa2001{at}med.cornell.edu.

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