Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans.
Wild isolates of Caenorhabditis elegans can feed either alone or in groups. This natural variation in behaviour is associated with a single residue difference in NPR-1, a predicted G-protein-coupled neuropeptide receptor related to Neuropeptide Y receptors. Here we show that the NPR-1 isoform associated with solitary feeding acts in neurons exposed to the body fluid to inhibit social feeding. Furthermore, suppressing the activity of these neurons, called AQR, PQR and URX, using an activated K(+) channel, inhibits social feeding. NPR-1 activity in AQR, PQR and URX neurons seems to suppress social feeding by antagonizing signalling through a cyclic GMP-gated ion channel encoded by tax-2 and tax-4. We show that mutations in tax-2 or tax-4 disrupt social feeding, and that tax-4 is required in several neurons for social feeding, including one or more of AQR, PQR and URX. The AQR, PQR and URX neurons are unusual in C. elegans because they are directly exposed to the pseudocoelomic body fluid. Our data suggest a model in which these neurons integrate antagonistic signals to control the choice between social and solitary feeding behaviour.
Coates
Juliet C
JC
MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, UK.
de Bono
Mario
M
D000818:Animals; D030801:Animals, Genetically Modified; D001685:Biological Factors / Q000494:pharmacology*; D001826:Body Fluids / Q000737:chemistry*; D017173:Caenorhabditis elegans / Q000187:drug effects* / Q000235:genetics / Q000502:physiology; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D006152:Cyclic GMP / Q000494:pharmacology; D005247:Feeding Behavior / Q000187:drug effects*; D017353:Gene Deletion; D015640:Ion Channel Gating / Q000187:drug effects; D007473:Ion Channels / Q000235:genetics / Q000378:metabolism; D009434:Neural Pathways / Q000187:drug effects*; D009474:Neurons / Q000187:drug effects* / Q000502:physiology; D015221:Potassium Channels / Q000378:metabolism; D011401:Promoter Regions, Genetic / Q000235:genetics; D017476:Receptors, Neuropeptide Y / Q000235:genetics / Q000378:metabolism; D015398:Signal Transduction / Q000187:drug effects; D012919:Social Behavior
D001685:Biological Factors; D029742:Caenorhabditis elegans Proteins; D007473:Ion Channels; C468272:NPR-1 protein, C elegans; D015221:Potassium Channels; D017476:Receptors, Neuropeptide Y; C102183:tax-2 protein, C elegans; C102184:tax-4 protein, C elegans; D006152:Cyclic GMP