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The Journal of Neuroscience, June 6, 2007, 27(23):6150-6162; doi:10.1523/JNEUROSCI.1466-07.2007

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Cellular/Molecular
UNC-31 (CAPS) Is Required for Dense-Core Vesicle But Not Synaptic Vesicle Exocytosis in Caenorhabditis elegans

Sean Speese,^1 * Matt Petrie,^2 * Kim Schuske,¹ Michael Ailion,¹ Kyoungsook Ann,² Kouichi Iwasaki,³ Erik M. Jorgensen,¹ and Thomas F. J. Martin²

¹Department of Biology, University of Utah, Salt Lake City, Utah 84112, ²Department of Biochemistry, University of Wisconsin–Madison, Madison, Wisconsin 53706, and ³Department of Molecular Pharmacology and Biological Chemistry, Northwestern University Medical School, Chicago, Illinois 60611

Correspondence should be addressed to Thomas F. J. Martin, Department of Biochemistry, University of Wisconsin–Madison, Madison, WI 53706. Email: tfmartin{at}wisc.edu

Previous studies indicated that CAPS (calcium-dependent activator protein for secretion) functions as an essential component for the Ca²⁺-dependent exocytosis of dense-core vesicles in neuroendocrine cells. However, recent mouse knock-out studies suggested an alternative role in the vesicular uptake or storage of catecholamines. To genetically assess the functional role of CAPS, we characterized the sole Caenorhabditis elegans CAPS ortholog UNC-31 (uncoordinated family member) and determined its role in dense-core vesicle-mediated peptide secretion and in synaptic vesicle recycling. Novel assays for dense-core vesicle exocytosis were developed by expressing a prepro-atrial natriuretic factor–green fluorescent protein fusion protein in C. elegans. unc-31 mutants exhibited reduced peptide release in vivo and lacked evoked peptide release in cultured neurons. In contrast, cultured neurons from unc-31 mutants exhibited normal stimulated synaptic vesicle recycling measured by FM4-64 [N-(3-triethylammoniumpropyl)-4-(6-(4-diethylamino)phenyl)hexatrienyl)pyridinium dibromide] dye uptake. Conversely, UNC-13, which exhibits sequence homology to CAPS/UNC-31, was found to be essential for synaptic vesicle but not dense-core vesicle exocytosis. These findings indicate that CAPS/UNC-31 function is not restricted to catecholaminergic vesicles but is generally required for and specific to dense-core vesicle exocytosis. Our results suggest that CAPS/UNC-31 and UNC-13 serve parallel and dedicated roles in dense-core vesicle and synaptic vesicle exocytosis, respectively, in the C. elegans nervous system.

Key words: CAPS; UNC-13; dense-core vesicle; exocytosis; synaptic vesicle; C. elegans

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Received Nov. 20, 2006; revised April 25, 2007; accepted April 28, 2007.

Correspondence should be addressed to Thomas F. J. Martin, Department of Biochemistry, University of Wisconsin–Madison, Madison, WI 53706. Email: tfmartin{at}wisc.edu

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