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Genetics, Vol. 167, 1677-1687, August 2004, Copyright © 2004
doi:10.1534/genetics.103.024786

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A Network of Stimulatory and Inhibitory G{alpha}-Subunits Regulates Olfaction in Caenorhabditis elegans

Hannes Lans, Suzanne Rademakers and Gert Jansen1

MGC Department of Cell Biology and Genetics, Center for Biomedical Genetics, Erasmus Medical Center, 3000 DR Rotterdam, The Netherlands

1 Corresponding author: MGC Department of Cell Biology and Genetics, Center for Biomedical Genetics, Erasmus Medical Center, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands.
E-mail: g.jansen{at}erasmusmc.nl

The two pairs of sensory neurons of C. elegans, AWA and AWC, that mediate odorant attraction, express six G{alpha}-subunits, suggesting that olfaction is regulated by a complex signaling network. Here, we describe the cellular localization and functions of the six olfactory G{alpha}-subunits: GPA-2, GPA-3, GPA-5, GPA-6, GPA-13, and ODR-3. All except GPA-6 localize to sensory cilia, suggesting a direct role in sensory transduction. GPA-2, GPA-3, GPA-5, and GPA-6 are also present in cell bodies and axons and GPA-5 specifically localizes to synaptic sites. Analysis of animals with single- to sixfold loss-of-function mutations shows that olfaction involves a balance between multiple stimulatory and inhibitory signals. ODR-3 constitutes the main stimulatory signal and is sufficient for the detection of odorants. GPA-3 forms a second stimulatory signal in the AWA and AWC neurons, also sufficient for odorant detection. In AWA, signaling is suppressed by GPA-5. In AWC, GPA-2 and GPA-13 negatively and positively regulate signaling, respectively. Finally, we show that only ODR-3 plays a role in cilia morphogenesis. Defects in this process are, however, independent of olfactory behavior. Our findings reveal the existence of a complex signaling network that controls odorant detection by C. elegans.




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