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J. Biol. Chem., Vol. 283, Issue 41, 27859-27870, October 10, 2008

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Regulation of Nuclear Ca²⁺ Signaling by Translocation of the Ca²⁺ Messenger Synthesizing Enzyme ADP-ribosyl Cyclase during Neuronal Depolarization^*

Stéphanie Bezin, Gilles Charpentier, Hon Cheung Lee^¶, Gérard Baux, Philippe Fossier, and José-Manuel Cancela¹

From the Laboratoire de Neurobiologie Cellulaire et Moléculaire, CNRS, UPR 9040, 1, Avenue de la Terrasse, 91198 Gif-Sur-Yvette Cedex, France, the Université Bordeaux 1 Laboratoire DMPFCS, IECB, 2, Rue Robert Escarpit, 33607 Pessac, France, and the ^¶Department of Physiology, University of Hong Kong, 4/F Lab Block, Faculty of Medicine Building, 21 Sassoon Road, Hong Kong

In neurons, voltage-gated Ca²⁺ channels and nuclear Ca²⁺ signaling play important roles, such as in the regulation of gene expression. However, the link between electrical activity and biochemical cascade activation involved in the generation of the nuclear Ca²⁺ signaling is poorly understood. Here we show that depolarization of Aplysia neurons induces the translocation of ADP-ribosyl cyclase, a Ca²⁺ messenger synthesizing enzyme, from the cytosol into the nucleus. The translocation is dependent on Ca²⁺ influx mainly through the voltage-dependent L-type Ca²⁺ channels. We report also that specific nucleoplasmic Ca²⁺ signals can be induced by three different calcium messengers, cyclic ADP-ribose, nicotinic acid adenine dinucleotide phosphate (NAADP), both produced by the ADP-ribosyl cyclase, and inositol 1,4,5-trisphosphate (IP₃). Moreover, our pharmacological data show that NAADP acts on its own receptor, which cooperates with the IP₃ and the ryanodine receptors to generate nucleoplasmic Ca²⁺ oscillations. We propose a new model where voltage-dependent L-type Ca²⁺ channel-induced nuclear translocation of the cytosolic cyclase is a crucial step in the fine tuning of nuclear Ca²⁺ signals in neurons.

Received for publication, June 19, 2008

^* The work was supported by grants from the Association Française contre les Myopathies and the Association pour la Recherche sur le Cancer (to J.-M. C.). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1 and S2.

¹ To whom correspondence should be addressed. Tel.: 33-01-69-82-41-69; Fax: 33-01-69-82-41-41; E-mail: jose.cancela{at}nbcm.cnrs-gif.fr.

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