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Originally published In Press as doi:10.1074/jbc.M201132200 on May 28, 2002

J. Biol. Chem., Vol. 277, Issue 33, 30315-30324, August 16, 2002
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Mechanisms Underlying the Neuronal Calcium Sensor-1-evoked Enhancement of Exocytosis in PC12 Cells*

Schuichi KoizumiDagger §, Patrizia Rosa, Gary B. Willars||, R. A. John Challiss||, Elena Taverna, Maura Francolini, Martin D. Bootman**, Peter Lipp**, Kazuhide InoueDagger , John RoderDagger Dagger , and Andreas JerominDagger Dagger §§

From the Dagger  Section of Neuropharmacology, Division of Pharmacology, National Institute of Health Sciences, 1-18-1 Kamiyoga, Setagaya, Tokyo 158-8501, Japan,  Institute of Neuroscience, Cellular and Molecular Pharmacology, Department of Pharmacology, 20129 Milano, Italy, the || Department of Cell Physiology and Pharmacology, University of Leicester, University Road, Leicester LE1 9HN, United Kingdom, the ** Laboratory of Molecular Signalling, The Babraham Institute, Babraham Hall, Cambridge CB2 4AT, United Kingdom, and the Dagger Dagger  Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario M5G 1X5, Canada

Neuronal calcium sensor-1 (NCS-1) or the originally identified homologue frequenin belongs to a superfamily of EF-hand calcium binding proteins. Although NCS-1 is thought to enhance synaptic efficacy or exocytosis mainly by activating ion channel function, the detailed molecular basis for the enhancement is still a matter of debate. Here, mechanisms underlying the NCS-1-evoked enhancement of exocytosis were investigated using PC12 cells overexpressing NCS-1. NCS-1 was found to have a broad distribution in the cells being partially distributed in the cytosol and associated to vesicles and tubular-like structures. Biochemical and immunohistochemical studies indicated that NCS-1 partially colocalized with the light synaptic vesicle marker synaptophysin. When stimulated with UTP or bradykinin, agonists to phospholipase C-linked receptors, NCS-1 enhanced the agonist-mediated elementary and global Ca2+ signaling and increased the levels of downstream signals of phosphatidylinositol 4-kinase. NCS-1 enhanced the UTP-evoked exocytosis but not the depolarization-evoked Ca2+ responses or exocytosis, suggesting that the enhancement by NCS-1 should involve phospholipase C-linked receptor-mediated signals rather than the Ca2+ channels or exocytotic machinery per se. Taken together, NCS-1 enhances phosphoinositide turnover, resulting in enhancement of Ca2+ signaling and exocytosis. This is a novel regulatory mechanism of exocytosis that might involve the activation of phosphatidylinositol 4-kinase.

* This work was supported by the Consighia Nationale Ricerche Target Project on Biotechnology (to P. R.) and the Japanese Health Science Foundation (to K. I.).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.

§ Supported by the Uehara Memorial Foundation and a Grant-in-Aid for Scientific Research in Japan (12780593). To whom correspondence should be addressed: Section of Neuropharmacology, Division of Pharmacology, National Institute of Health Sciences, 1-18-1 Kamiyoga, Setagaya, Tokyo 158-8501 Japan. Tel.: 81-3-3700-1141 (ext. 344); Fax: 81-3-3707-6950; E-mail: skoizumi@nihs.go.jp.

§§ Supported by the Medical Research Council of Canada.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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