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Originally published In Press as doi:10.1074/jbc.M108186200 on October 16, 2001

J. Biol. Chem., Vol. 276, Issue 51, 47877-47885, December 21, 2001
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Phosphorylation of Cysteine String Protein by Protein Kinase A
IMPLICATIONS FOR THE MODULATION OF EXOCYTOSIS*

Gareth J. O. Evans, Mark C. WilkinsonDagger , Margaret E. Graham, Kathryn M. Turner§, Luke H. Chamberlain, Robert D. Burgoyne, and Alan Morgan||

From the Physiological Laboratory and Dagger  School of Biological Sciences, University of Liverpool, Crown Street, Liverpool L69 3BX, United Kingdom

Cyclic AMP-dependent protein kinase (PKA) enhances regulated exocytosis in neurons and most other secretory cells. To explore the molecular basis of this effect, known exocytotic proteins were screened for PKA substrates. Both cysteine string protein (CSP) and soluble NSF attachment protein-alpha (alpha -SNAP) were phosphorylated by PKA in vitro, but immunoprecipitation of cellular alpha -SNAP failed to detect 32P incorporation. In contrast, endogenous CSP was phosphorylated in synaptosomes, PC12 cells, and chromaffin cells. In-gel kinase assays confirmed PKA to be a cellular CSP kinase, with phosphorylation occurring on Ser10. PKA phosphorylation of CSP reduced its binding to syntaxin by 10-fold but had little effect on its interaction with HSC70 or G-protein subunits. Furthermore, an in vivo role for Ser10 phosphorylation at a late stage of exocytosis is suggested by analysis of chromaffin cells transfected with wild type or non-phosphorylatable mutant CSP. We propose that PKA phosphorylation of CSP could modulate the exocytotic machinery, by selectively altering its availability for protein-protein interactions.

* This work was supported by Wellcome Trust Prize studentships (to K. M. T. and L. H. C.) and grants from the Nuffield Foundation (to M. C. W.), the Wellcome Trust (to R. D. B.), and the Medical Research Council (to A. M.).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.

§ Present address: School of Biological Sciences, University of Manchester, Oxford Rd., Manchester M13 9PT, UK.

Present address: Division of Biochemistry and Molecular Biology, University of Glasgow, Glasgow G12 8QQ, UK.

|| To whom correspondence should be addressed. Tel.: 44 0 151 794 5333; Fax: 44 0 151 794 5337; E-mail: amorgan@liverpool.ac.uk.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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