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The Journal of Neuroscience, December 1, 1998, 18(23):9638-9649

A Product of the Drosophila stoned Locus Regulates Neurotransmitter Release

Daniel T. Stimson¹, Patricia S. Estes¹, Michiko Smith², Leonard E. Kelly², and Mani Ramaswami¹

¹ Arizona Research Laboratories Division of Neurobiology and Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona 85721, and ² Department of Genetics, University of Melbourne, Parkville, Australia

The Drosophila stoned locus encodes two novel gene products termed stonedA and stonedB, which possess sequence motifs shared by proteins involved in intracellular vesicle traffic. A specific requirement for stoned in the synaptic vesicle cycle has been suggested by synthetic genetic interactions between stoned and shibire, a gene essential for synaptic vesicle recycling (). A synaptic role of stoned gene products also is suggested by altered synaptic transients in electroretinograms recorded from stoned mutant eyes (). We show here that the stonedA protein is highly enriched at Drosophila nerve terminals. Mutant alleles that affect stonedA disrupt the normal regulation of synaptic vesicle exocytosis at neuromuscular synapses of Drosophila. Spontaneous neurotransmitter release is enhanced dramatically, and evoked release is reduced substantially in such stoned mutants. Ultrastructural studies reveal no evidence of major disorganization at stoned mutant nerve terminals. Thus, our data indicate a direct role for stonedA in regulating synaptic vesicle exocytosis. However, genetic and morphological observations suggest additional, subtle effects of stoned mutations on synaptic vesicle recycling. Remarkably, almost all phenotypes of stoned mutants are similar to those previously described for mutants of synaptotagmin, a protein postulated to regulate both exocytosis and the recycling of synaptic vesicles. We propose a model in which stonedA functions together with synaptotagmin to regulate synaptic vesicle cycling.

Key words: neurogenetics; stoned; Drosophila; presynaptic function; neurotransmitter release; synaptic vesicle fusion; synaptic vesicle recycling

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Copyright © 1998 Society for Neuroscience  0270-6474/98/18239638-12$05.00/0

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