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J. Biol. Chem., Vol. 280, Issue 7, 6047-6054, February 18, 2005

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Interaction of Neuronal Calcium Sensor-1 and ADP-ribosylation Factor 1 Allows Bidirectional Control of Phosphatidylinositol 4-Kinase and trans-Golgi Network-Plasma Membrane Traffic^*

Lee P. Haynes, Geraint M. H. Thomas, and Robert D. Burgoyne¶

From the Physiological Laboratory, School of Biomedical Sciences, University of Liverpool, Crown St., Liverpool L69 3BX and the Department of Physiology, University College London, London WC1E 6JJ, United Kingdom

We have identified a novel Ca²⁺-dependent interaction between neuronal calcium sensor-1 (NCS-1) and the GTPase ARF1. Both of these proteins are localized to the Golgi complex, and both regulate phosphatidylinositol 4-kinase III (PI(4)K). Spatial and temporal control of phosphatidylinositol 4-phosphate levels through activation of PI(4)K is important for the recruitment of trafficking complexes to the trans-Golgi network (TGN) and vesicular traffic from this organelle. The NCS-1-ARF1 interaction and its specificity have been demonstrated through in vitro binding assays, in vitro enzyme assay, and through functional cellular assays. We show that NCS-1 can exert bidirectional effects to activate PI(4)K on its own or inhibit the activation by ARF1. NCS-1 was shown to modulate the effects of expression of ARF mutants that disrupt Golgi morphology and to recruit GDP-loaded ARF to the Golgi complex in a Ca²⁺-dependent manner. We demonstrate antagonist effects of NCS-1 and ARF on constitutive and regulated exocytosis. The NCS-1-ARF1 interaction provides evidence for functional cross-talk between Ca²⁺-dependent and ARF-dependent pathways in TGN to plasma membrane traffic.

Received for publication, November 19, 2004 , and in revised form, November 30, 2004.

^* This work was supported by a grant from the Wellcome Trust (to R. D. B.). 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.

^¶ To whom correspondence should be addressed. Tel.: 44-151-794-5305; Fax: 44-151-794-5337; E-mail: burgoyne{at}liv.ac.uk.

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