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Originally published as Genetics Published Articles Ahead of Print on November 4, 2005.
Genetics, Vol. 172, 943-961, February 2006, Copyright © 2006
doi:10.1534/genetics.105.049577
Presynaptic UNC-31 (CAPS) Is Required to Activate the G
s Pathway of the Caenorhabditis elegans Synaptic Signaling Network
Nicole K. Charlie, Michael A. Schade, Angela M. Thomure and Kenneth G. Miller1
Program in Molecular, Cell and Developmental Biology, Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma 73104
1 Corresponding author: Oklahoma Medical Research Foundation, 825 NE 13th St., Oklahoma City, OK 73104.
E-mail: millerk{at}omrf.ouhsc.edu
C. elegans mutants lacking the dense-core vesicle priming protein UNC-31 (CAPS) share highly similar phenotypes with mutants lacking a neuronal G
s pathway, including strong paralysis despite exhibiting near normal levels of steady-state acetylcholine release as indicated by drug sensitivity assays. Our genetic analysis shows that UNC-31 and neuronal Gs are different parts of the same pathway and that the UNC-31/Gs pathway is functionally distinct from the presynaptic Gq pathway with which it interacts. UNC-31 acts upstream of Gs because mutations that activate the Gs pathway confer similar levels of strongly hyperactive, coordinated locomotion in both unc-31 null and (+) backgrounds. Using cell-specific promoters, we show that both UNC-31 and the Gs pathway function in cholinergic motor neurons to regulate locomotion rate. Using immunostaining we show that UNC-31 is often concentrated at or near active zones of cholinergic motor neuron synapses. Our data suggest that presynaptic UNC-31 activity, likely acting via dense-core vesicle exocytosis, is required to locally activate the neuronal Gs pathway near synaptic active zones.
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