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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 groups1,2. 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 receptors2. 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 fluid3. Our data suggest a model in which these neurons integrate antagonistic signals to control the choice between social and solitary feeding behaviour.

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Figure 1: A functional npr-1::gfp fusion gene is expressed in approximately 20 neuron types.
Figure 2: Expression of npr-1::gfp from a heat-shock-inducible promoter in adults, or specifically in the AQR, PQR and URX neurons, suppresses social feeding in npr-1 animals.
Figure 3: Targeted expression of the EGL-2(gf) dominantly active K+ channel in the AQR, PQR and URX body cavity neurons suppresses social feeding.
Figure 4: The cGMP-gated ion channel subunits tax-2 and tax-4 mediate social feeding.


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We thank C. Bargmann, A. Fire, R. Horvitz, C. Li, I. Mori, A. Wei and S. Yu for sharing unpublished data, constructs and strains; T. Stiernagle and the Caenorhabditis Genetics Centre for strains; and G. Brown, N. Hopper, N. Tremain and C. Bargmann for suggestions. Some of this work was done while M.d.B. was in the laboratory of C. Bargmann. We are grateful to B. Amos and S. Reichelt for assistance with confocal microscopy.

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Correspondence to Mario de Bono.

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Coates, J., de Bono, M. Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans. Nature 419, 925–929 (2002).

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