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First published online January 31, 2006
Journal of Experimental Biology 209, 731-747 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02032
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A potassium channel (Kv4) cloned from the heart of the tunicate Ciona intestinalis and its modulation by a KChIP subunit

Vicenta Salvador-Recatalà1,2, Warren J. Gallin3, Jennifer Abbruzzese4, Peter C. Ruben4 and Andrew N. Spencer2,3,*

1 Department of Physiology, University of Alberta, Edmonton, AB, T6G 2H7, Canada
2 Bamfield Marine Sciences Centre, Bamfield, BC, V0R 1B0, Canada
3 Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9, Canada
4 Department of Biology, Utah State University, Utah, 84322 USA

* Author for correspondence (e-mail: andy.spencer{at}shaw.ca)

Accepted 10 December 2005

Voltage-gated ion channels of the Kv4 subfamily produce A-type currents whose properties are tuned by accessory subunits termed KChIPs, which are a family of Ca2+ sensor proteins. By modifying expression levels and the intrinsic biophysical properties of Kv4 channels, KChIPs modulate the excitability properties of neurons and myocytes. We studied how a Kv4 channel from a tunicate, the first branching clade of the chordates, is modulated by endogenous KChIP subunits. BLAST searches in the genome of Ciona intestinalis identified a single Kv4 gene and a single KChIP gene, implying that the diversification of both genes occurred during early vertebrate evolution, since the corresponding mammalian gene families are formed by several paralogues. In this study we describe the cloning and characterization of a tunicate Kv4 channel, CionaKv4, and a tunicate KChIP subunit, CionaKChIP. We demonstrate that CionaKChIP strongly modulates CionaKv4 by producing larger currents that inactivate more slowly than in the absence of the KChIP subunit. Furthermore, CionaKChIP shifted the midpoints of activation and inactivation and slowed deactivation and recovery from inactivation of CionaKv4. Modulation by CionaKChIP requires the presence of the intact N terminus of CionaKv4 because, except for a minor effect on inactivation, CionaKChIP did not modulate CionaKv4 channels that lacked amino acids 2-32. In summary, our results suggest that modulation of Kv4 channels by KChIP subunits is an ancient mechanism for modulating electrical excitability.

Key words: Kv4, KChIP, potassium channel, Ciona intestinalis, tunicate, heart


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