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Originally published In Press as doi:10.1074/jbc.M204702200 on December 5, 2002

J. Biol. Chem., Vol. 278, Issue 8, 6075-6084, February 21, 2003
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Phosphatidylinositol 4-OH Kinase Is a Downstream Target of Neuronal Calcium Sensor-1 in Enhancing Exocytosis in Neuroendocrine Cells*

Manisha RajebhosaleDagger , Sam GreenwoodDagger , Jolanta Vidugiriene§, Andreas Jeromin, and Sabine HilfikerDagger ||

From the Dagger  University of Manchester, School of Biological Sciences, Oxford Road, Manchester M13 9PT, United Kingdom,  Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario M5G 1X5, Canada, and § Research and Development, Promega Corporation, Madison, Wisconsin 53711

Neuronal calcium sensor-1 (NCS-1), the mammalian orthologue of frequenin, belongs to a family of EF-hand-containing Ca2+ sensors. NCS-1/frequenin has been shown to enhance synaptic transmission in PC12 cells and Drosophila and Xenopus, respectively. However, the precise molecular mechanism for the enhancement of exocytosis is largely unknown. In PC12 cells, NCS-1 potentiated exocytosis evoked by ATP, an agonist to phospholipase C-linked receptors, but had no effect on depolarization-evoked release. NCS-1 also enhanced exocytosis triggered by ionomycin, a Ca2+ ionophore that bypasses K+ and Ca2+ channels. Overexpression of NCS-1 caused a shift in the dose-response curve of inhibition of ATP-evoked secretion using phenylarsine oxide, an inhibitor of phosphatidylinositol 4-OH kinase (PI4K). Plasma membrane phosphatidylinositol 4,5-bisphosphate pools were increased upon NCS-1 transfection as visualized using a phospholipase C-delta pleckstrin homology domain-green fluorescent protein construct. NCS-1-transfected cell extracts displayed increased phosphatidylinositol-4-phosphate biosynthesis, indicating an increase in PI4K activity. Mutations in NCS-1 equivalent to those that abolish the interaction of recoverin, another EF-hand-containing Ca2+ sensor, with its downstream target rhodopsin kinase, lost their ability to enhance exocytosis. Taken together, the present data indicate that NCS-1 modulates the activity of PI4K, leading to increased levels of phosphoinositides and concomitant enhancement of exocytosis.

* This work was supported by MRC Grant G9722026 and a BBSRC David Phillips Fellowship (to S. H.).The costs of publication of this article were defrayed in part by the payment of page charges. The 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. Tel.: 44-161-275-5513; Fax: 44-161-275-5082; E-mail: sabine.hilfiker@man.ac.uk.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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