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MBC in Press, published online ahead of print December 19, 2007
Mol. Biol. Cell 10.1091/mbc.E07-07-0719

A more recent version of this article appeared on March 1, 2008
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Submitted on July 28, 2007
Revised on November 26, 2007
Accepted on December 10, 2007

Polyunsaturated Fatty Acids Influence Synaptojanin Localization to Regulate Synaptic Vesicle Recycling

Esther Marza,* Toni Long,{dagger} Adolfo Saiardi,*{ddagger} Marija Sumakovic,{sect} Stefan Eimer,{sect} David H. Hall,{dagger} and Giovanni M. Lesa*||

*MRC Laboratory for Molecular Cell Biology, {ddagger}Cell Biology Unit, and ||Department of Physiology, University College London, London, WC1E 6BT, United Kingdom; {dagger}Center for C. elegans Anatomy, Department of Neuroscience, Albert Einstein College of Medicine, NY 10461; {sect}European Neuroscience Institute, Center for Molecular Physiology of the Brain, 37077 Goettingen, Germany

Monitoring Editor: Howard Riezman

The lipid polyunsaturated fatty acids are highly enriched in synaptic membranes, including synaptic vesicles, but their precise function there is unknown. C. elegans fat-3 mutants lack long-chain polyunsaturated fatty acids (LC-PUFAs); they release abnormally low levels of serotonin and acetylcholine and are depleted of synaptic vesicles, but the mechanistic basis of these defects is unclear. Here we demonstrate that synaptic vesicle endocytosis is impaired in the mutants: the synaptic vesicle protein synaptobrevin is not efficiently retrieved after synaptic vesicles fuse with the presynaptic membrane, and the presynaptic terminals contain abnormally large endosomal-like compartments and synaptic vesicles. Moreover, the mutants have abnormally low levels of the phosphoinositide phosphatase synaptojanin at release sites and accumulate the main synaptojanin substrate phosphatidylinositol 4,5-bisphosphate at these sites. Both synaptobrevin and synaptojanin mislocalization can be rescued by providing exogenous arachidonic acid, an LC-PUFA, suggesting that the endocytosis defect is caused by LC-PUFA depletion. By showing that the genes fat-3 and synaptojanin act in the same endocytic pathway at synapses, our findings suggest that LC-PUFAs are required for efficient synaptic vesicle recycling, probably by modulating synaptojanin localization at synapses.

Address correspondence to: Giovanni M. Lesa (Giovanni.Lesa{at}ucl.ac.uk)




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