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J. Biol. Chem., Vol. 278, Issue 23, 21178-21187, June 6, 2003

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Expression and Modulation of an Invertebrate Presynaptic Calcium Channel ₁ Subunit Homolog^*

J. David Spafford   ¶, Lina Chen , Zhong-Ping Feng  ||, August B. Smit  and Gerald W. Zamponi  **

From the Department of Physiology and Biophysics, Cellular and Molecular Neurobiology Research Group, University of Calgary, Calgary, T2N 4N1, Canada and Department of Molecular and Cellular Neurobiology, Research Institute Neurosciences, Vrije Universiteit, 1081 HV Amsterdam, The Netherlands

Here we report the first assessment of the expression and modulation of an invertebrate ₁ subunit homolog of mammalian presynaptic Ca_v2 calcium channels (N-type and P/Q-type) in mammalian cells. Our data show that molluscan channel (LCa_v2a) isolated from Lymnaea stagnalis is effectively membrane-targeted and electrophysiologically recordable in tsA-201 cells only when the first 44 amino acids of LCa_v2a are substituted for the corresponding region of rat Ca_v2.1. When coexpressed with rat accessory subunits, the biophysical properties of LCa_v2a-5'rbA resemble those of mammalian N-type calcium channels with respect to activation and inactivation, lack of pronounced calcium dependent inactivation, preferential permeation of barium ions, and cadmium block. Consistent with reports of native Lymnaea calcium currents, the LCa_v2a-5'rbA channel is insensitive to micromolar concentrations of -conotoxin GVIA and is not affected by nifedipine, thus confirming that it is not of the L-type. Interestingly, the LCa_v2a-5'rbA channel is almost completely and irreversibly inhibited by guanosine 5'-3-O-(thio)triphosphate but not regulated by syntaxin1, suggesting that invertebrate presynaptic calcium channels are differently modulated from their vertebrate counterparts.

Received for publication, March 3, 2003 , and in revised form, April 1, 2003.

This work is dedicated to the late Nikita Grigoriev.

^* This work was supported by an operating grant from the Canadian Institutes of Health Research (to G. W. Z.). 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.

^¶ This author holds a postdoctoral fellowship award from the Human Frontier Science Program.

^|| This author previously held postdoctoral research fellowships from the Canadian Institutes of Health Research and the Heart and Stroke Foundation of Canada.

^** This author holds a Senior Scholar Award from the Alberta Heritage Foundation for Medical Research and is a Canadian Institutes of Health Research Investigator. To whom correspondence should be addressed: Dept. of Physiology and Biophysics, University of Calgary, 3330 Hospital Dr. NW, Calgary, T2N 4N1, Canada. Tel.: 403-220-8687; Fax: 403-210-8106; E-mail: Zamponi{at}ucalgary.ca.

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