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J. Biol. Chem., Vol. 279, Issue 48, 50524-50536, November 26, 2004

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Presynaptic Trafficking of Synaptotagmin I Is Regulated by Protein Palmitoylation^*

Rujun Kang, Richard Swayze¶, Marie France Lise, Kimberly Gerrow¶, Asher Mullard, William G. Honer, and Alaa El-Husseini, Canadian Institutes of Health Research New Investigator and Michael Smith Foundation for Health Research Scholar||

From the Department of Psychiatry, Centre for Complex Disorders, and the Brain Research Centre, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada

Protein palmitoylation plays a critical role in sorting and targeting of several proteins to pre- and postsynaptic sites. In this study, we have analyzed the role of palmitoylation in trafficking of synaptotagmin I and its modulation by synaptic activity. We found that palmitoylation of N-terminal cysteines contributed to sorting of synaptotagmin I to an intracellular vesicular compartment at the presynaptic terminal. Presynaptic targeting is a unique feature of N-terminal sequences of synaptotagmin I because the palmitoylated N terminus of synaptotagmin VII failed to localize to presynaptic sites. We also found that palmitate was stably associated with both synaptotagmin I and SNAP-25 and that rapid neuronal depolarization did not affect palmitate turnover on these proteins. However, long-term treatment with drugs that either block synaptic activity or disrupt SNARE complex assembly modulated palmitoylation and accumulation of synaptotagmin I at presynaptic sites. We conclude that palmitoylation is involved in trafficking of specific elements involved in transmitter release and that distinct mechanisms regulate addition and removal of palmitate on select neuronal proteins.

Received for publication, May 5, 2004 , and in revised form, August 31, 2004.

^* This work was supported in part by a grant from the Michael Smith Foundation for Health Research (to A. E.-H.) and by Canadian Institutes of Health Research Grants 20R90479 (to A. E.-H.), MOP-14037 (to W. G. H.), and NET-54013. 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. 1–5.

Both authors equally contributed to this work.

Supported by a Canadian Institutes of Health Research studentship.

^¶ Supported by a Michael Smith Foundation for Health Research student fellowship.

^|| To whom correspondence should be addressed: Dept. of Psychiatry, University of British Columbia, 2255 Wesbrook Mall, Vancouver, BC V6T 1Z3, Canada. Tel.: 604-822-7526; Fax: 604-822-7981; E-mail: alaa{at}interchange.ubc.ca.

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