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The Journal of Neuroscience, February 14, 2007, 27(7):1651-1658; doi:10.1523/JNEUROSCI.4006-06.2007

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Cellular/Molecular
K⁺ Channel Facilitation of Exocytosis by Dynamic Interaction with Syntaxin

Dafna Singer-Lahat,¹ Anton Sheinin,¹ Dodo Chikvashvili,¹ Sharon Tsuk,¹ Dafna Greitzer,¹ Reut Friedrich,² Lori Feinshreiber,¹ Uri Ashery,² Morris Benveniste,^1,4 Edwin S. Levitan,³ and Ilana Lotan¹

¹Department of Physiology and Pharmacology, Sackler Faculty of Medicine, and ²Department of Neurobiochemistry, Life Sciences Institute, Tel-Aviv University, 69978 Ramat-Aviv, Israel, ³Department of Pharmacology, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, and ⁴Neuroscience Institute, Morehouse School of Medicine, Atlanta, Georgia 30310

Correspondence should be addressed to Dr. Ilana Lotan, Department of Physiology and Pharmacology, Sackler Faculty of Medicine, Tel-Aviv University, 69978 Ramat-Aviv, Israel. Email: ilotan{at}post.tau.ac.il

Kv channels inhibit release indirectly by hyperpolarizing membrane potential, but the significance of Kv channel interaction with the secretory apparatus is not known. The Kv2.1 channel is commonly expressed in the soma and dendrites of neurons, where it could influence the release of neuropeptides and neurotrophins, and in neuroendocrine cells, where it could influence hormone release. Here we show that Kv2.1 channels increase dense-core vesicle (DCV)-mediated release after elevation of cytoplasmic Ca²⁺. This facilitation occurs even after disruption of pore function and cannot be explained by changes in membrane potential and cytoplasmic Ca²⁺. However, triggering release increases channel binding to syntaxin, a secretory apparatus protein. Disrupting this interaction with competing peptides or by deleting the syntaxin association domain of the channel at the C terminus blocks facilitation of release. Thus, direct association of Kv2.1 with syntaxin promotes exocytosis. The dual functioning of the Kv channel to influence release, through its pore to hyperpolarize the membrane potential and through its C-terminal association with syntaxin to directly facilitate release, reinforces the requirements for repetitive firing for exocytosis of DCVs in neuroendocrine cells and in dendrites.

Key words: exocytosis; Kv2.1 channel; syntaxin 1A; dense-core vesicles (DCVs); PC12 cells; neuropeptides; SNAREs

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Received Sept. 14, 2006; revised Jan. 7, 2007; accepted Jan. 9, 2007.

Correspondence should be addressed to Dr. Ilana Lotan, Department of Physiology and Pharmacology, Sackler Faculty of Medicine, Tel-Aviv University, 69978 Ramat-Aviv, Israel. Email: ilotan{at}post.tau.ac.il

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