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The Journal of Neuroscience, March 15, 2001, 21(6):1964-1974

Direct Interaction of a Brain Voltage-Gated K⁺ Channel with Syntaxin 1A: Functional Impact on Channel Gating

Oded Fili¹, Itzhak Michaelevski¹, Yaniv Bledi², Dodo Chikvashvili¹, Dafna Singer-Lahat¹, Hassia Boshwitz², Michal Linial², and Ilana Lotan¹

¹ Department of Physiology and Pharmacology, Sackler School of Medicine, Tel-Aviv University, 69978 Ramat-Aviv, Israel, and ² Department of Biological Chemistry, Life Sciences Institute, The Hebrew University of Jerusalem, 91904 Jerusalem, Israel

Presynaptic voltage-gated K⁺ (Kv) channels play a physiological role in the regulation of transmitter release by virtue of their ability to shape presynaptic action potentials. However, the possibility of a direct interaction of these channels with the exocytotic apparatus has never been examined. We report the existence of a physical interaction in brain synaptosomes between Kv1.1 and Kv subunits with syntaxin 1A, occurring, at least partially, within the context of a macromolecular complex containing syntaxin, synaptotagmin, and SNAP-25. The interaction was altered after stimulation of neurotransmitter release. The interaction with syntaxin was further characterized in Xenopus oocytes by both overexpression and antisense knock-down of syntaxin. Direct physical interaction of syntaxin with the channel protein resulted in an increase in the extent of fast inactivation of the Kv1.1/Kv1.1 channel. Syntaxin also affected the channel amplitude in a biphasic manner, depending on its concentration. At low syntaxin concentrations there was a significant increase in amplitudes, with no detectable change in cell-surface channel expression. At higher concentrations, however, the amplitudes decreased, probably because of a concomitant decrease in cell-surface channel expression, consistent with the role of syntaxin in regulation of vesicle trafficking. The observed physical and functional interactions between syntaxin 1A and a Kv channel may play a role in synaptic efficacy and neuronal excitability.

Key words: Kv channel; potassium channel; SNARE complex; syntaxin 1A; gating; K⁺ channel; Kv1.1 subunits; Kv subunits; Xenopus oocytes; rat brain synaptosomes

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Copyright © 2001 Society for Neuroscience  0270-6474/01/2161964-11$05.00/0

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