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Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans

Abstract

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.

References

  1. Hodgkin, J. & Doniach, T. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146, 149–164 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  2. de Bono, M. & Bargmann, C. I. Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94, 679–689 (1998)

    CAS  Article  Google Scholar 

  3. White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. R Soc. Lond. B 314, 1–340 (1986)

    ADS  CAS  Article  Google Scholar 

  4. Wang, Q. & Wadsworth, W. G. The C domain of NETRIN UNC-6 silences calcium/calmodulin-dependent protein kinase- and diacylglycerol-dependent axon branching in Caenorhabditis elegans. J. Neurosci. 22, 2274–2282 (2002)

    CAS  Article  Google Scholar 

  5. Sengupta, P., Chou, J. H. & Bargmann, C. I. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84, 899–909 (1996)

    CAS  Article  Google Scholar 

  6. Dwyer, N. D., Troemel, E. R., Sengupta, P. & Bargmann, C. I. Odorant receptor localization to olfactory cilia is mediated by ODR-4, a novel membrane-associated protein. Cell 93, 455–466 (1998)

    CAS  Article  Google Scholar 

  7. Stringham, E. G., Dixon, D. K., Jones, D. & Candido, E. P. Temporal and spatial expression patterns of the small heat shock (hsp16) genes in transgenic Caenorhabditis elegans. Mol. Biol. Cell 3, 221–233 (1992)

    CAS  Article  Google Scholar 

  8. Yu, S., Avery, L., Baude, E. & Garbers, D. L. Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc. Natl Acad. Sci. USA 94, 3384–3387 (1997)

    ADS  CAS  Article  Google Scholar 

  9. Weinshenker, D., Wei, A., Salkoff, L. & Thomas, J. H. Block of an ether-a-go-go-like K+ channel by imipramine rescues egl-2 excitation defects in Caenorhabditis elegans. J. Neurosci. 19, 9831–9840 (1999)

    CAS  Article  Google Scholar 

  10. Mori, I. Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. Annu. Rev. Genet. 33, 399–422 (1999)

    CAS  Article  Google Scholar 

  11. Finn, J. T., Grunwald, M. E. & Yau, K. W. Cyclic nucleotide-gated ion channels: an extended family with diverse functions. Annu. Rev. Physiol. 58, 395–426 (1996)

    CAS  Article  Google Scholar 

  12. Coburn, C. M. & Bargmann, C. I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17, 695–706 (1996)

    CAS  Article  Google Scholar 

  13. Komatsu, H. et al. Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells. Brain Res. 821, 160–168 (1999)

    CAS  Article  Google Scholar 

  14. Komatsu, H., Mori, I., Rhee, J. S., Akaike, N. & Ohshima, Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17, 707–718 (1996)

    CAS  Article  Google Scholar 

  15. Osborne, K. A. et al. Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277, 834–836 (1997)

    CAS  Article  Google Scholar 

  16. Ben-Shahar, Y., Robichon, A., Sokolowski, M. B. & Robinson, G. E. Influence of gene action across different time scales on behavior. Science 296, 741–744 (2002)

    ADS  CAS  Article  Google Scholar 

  17. Marsh, D. J., Baraban, S. C., Hollopeter, G. & Palmiter, R. D. Role of the Y5 neuropeptide Y receptor in limbic seizures. Proc. Natl Acad. Sci. USA 96, 13518–13523 (1999)

    ADS  CAS  Article  Google Scholar 

  18. Cowley, M. A. et al. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411, 480–484 (2001)

    ADS  CAS  Article  Google Scholar 

  19. Lee, D. L. & Atkinson, H. J. Physiology of Nematodes (Macmillan, London, 1976)

    Book  Google Scholar 

  20. Li, C., Nelson, L., Kyuhyung, K., Nathoo, A. & Hart, A. C. Neuropeptide gene families in the nematode Caenorhabditis elegans. Ann. NY Acad. Sci. 897, 239–252 (1999)

    ADS  CAS  Article  Google Scholar 

  21. Schwartz, M. W., Woods, S. C., Porte, D. Jr, Seeley, R. J. & Baskin, D. G. Central nervous system control of food intake. Nature 404, 661–671 (2000)

    CAS  Article  Google Scholar 

  22. Robinson, G. E., Fahrbach, S. E. & Winston, M. L. Insect societies and the molecular biology of social behavior. Bioessays 19, 1099–1108 (1997)

    CAS  Article  Google Scholar 

  23. Giraldeau, L.-A. & Caraco, T. Social Foraging Theory (Princeton Univ. Press, Princeton, New Jersey, 2000)

    Google Scholar 

  24. Sulston, J. & Hodgkin, J. The Nematode Caenorhabditis elegans (ed. Wood, W. B.) 587–606 (Cold Spring Harbor Laboratory, Cold Spring Harbor, 1988)

    Google Scholar 

  25. Clark, S. G., Lu, X. & Horvitz, H. R. The Caenorhabditis elegans locus lin-15, a negative regulator of a tyrosine kinase signaling pathway, encodes two different proteins. Genetics 137, 987–997 (1994)

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Mello, C. C., Kramer, J. M., Stinchcomb, D. & Ambros, V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959–3970 (1991)

    CAS  Article  Google Scholar 

  27. Walhout, A. J. et al. GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol. 328, 575–592 (2000)

    CAS  Article  Google Scholar 

  28. Li, C., Kim, K. & Nelson, L. S. FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Res. 848, 26–34 (1999)

    CAS  Article  Google Scholar 

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Acknowledgements

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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Coates, J., de Bono, M. Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans. Nature 419, 925–929 (2002). https://doi.org/10.1038/nature01170

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