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Involvement of a Gr2a-Expressing Drosophila Pharyngeal Gustatory Receptor Neuron in Regulation of Aversion to High-Salt Foods

  • Kim, Haein (Department of Biological Sciences, Sungkyunkwan University) ;
  • Jeong, Yong Taek (Department of Oral Biology, BK21 PLUS Project, Yonsei University College of Dentistry) ;
  • Choi, Min Sung (Department of Biological Sciences, Sungkyunkwan University) ;
  • Choi, Jaekyun (Department of Biological Sciences, Sungkyunkwan University) ;
  • Moon, Seok Jun (Department of Oral Biology, BK21 PLUS Project, Yonsei University College of Dentistry) ;
  • Kwon, Jae Young (Department of Biological Sciences, Sungkyunkwan University)
  • Received : 2017.02.23
  • Accepted : 2017.04.18
  • Published : 2017.05.31

Abstract

Regulation of feeding is essential for animal survival. The pharyngeal sense organs can act as a second checkpoint of food quality, due to their position between external taste organs such as the labellum which initially assess food quality, and the digestive tract. Growing evidence provides support that the pharyngeal sensory neurons regulate feeding, but much is still unknown. We found that a pair of gustatory receptor neurons in the LSO, a Drosophila adult pharyngeal organ which expresses four gustatory receptors, is involved in feeding inhibition in response to high concentrations of sodium ions. RNAi experiments and mutant analysis showed that the gustatory receptor Gr2a is necessary for this process. This feeding preference determined by whether a food source is perceived as appetizing or not is influenced by nutritional conditions, such that when the animal is hungry, the need for energy dominates over how appealing the food source is. Our results provide experimental evidence that factors involved in feeding function in a context-dependent manner.

Keywords

References

  1. Choi, J., van Giesen, L., Choi, M.S., Kang, K., Sprecher, S.G., and Kwon, J.Y. (2016). A pair of pharyngeal gustatory receptor neurons regulates caffeine-dependent ingestion in Drosophila Larvae. Front Cell Neurosci. 10, 181.
  2. Clyne, P.J., Warr, C.G., and Carlson, J.R. (2000). Candidate taste receptors in Drosophila. Science 287, 1830-1834. https://doi.org/10.1126/science.287.5459.1830
  3. Dahanukar, A., Lei, Y.T., Kwon, J.Y., and Carlson, J.R. (2007). Two Gr genes underlie sugar reception in Drosophila. Neuron 56, 503-516. https://doi.org/10.1016/j.neuron.2007.10.024
  4. Du, E.J., Ahn, T.J., Choi, M.S., Kwon, I., Kim, H.W., Kwon, J.Y., and Kang, K. (2015). The mosquito repellent citronellal directly potentiates drosophila TRPA1, facilitating feeding suppression. Mol. Cells 38, 911-917. https://doi.org/10.14348/molcells.2015.0215
  5. Freeman, E.G., and Dahanukar, A. (2015). Molecular neurobiology of Drosophila taste. Curr. Opin. Neurobiol. 34, 140-148. https://doi.org/10.1016/j.conb.2015.06.001
  6. Fujii, S., Yavuz, A., Slone, J., Jagge, C., Song, X., and Amrein, H. (2015). Drosophila sugar receptors in sweet taste perception, olfaction, and internal nutrient sensing. Curr. Biol. 25, 621-627. https://doi.org/10.1016/j.cub.2014.12.058
  7. Gendre, N., Luer, K., Friche, S., Grillenzoni, N., Ramaekers, A., Technau, G.M., and Stocker, R.F. (2004). Integration of complex larval chemosensory organs into the adult nervous system of Drosophila. Development 131, 83-92. https://doi.org/10.1242/dev.00879
  8. Gong, W.J., and Golic, K.G. (2003). Ends-out, or replacement, gene targeting in Drosophila. Proc. Natl. Acad. Sci. USA 100, 2556-2561. https://doi.org/10.1073/pnas.0535280100
  9. Jiao, Y., Moon, S.J., and Montell, C. (2007). A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proc. Natl. Acad. Sci. USA 104, 14110-14115. https://doi.org/10.1073/pnas.0702421104
  10. Jiao, Y., Moon, S.J., Wang, X., Ren, Q., and Montell, C. (2008). Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr. Biol. 18, 1797-1801. https://doi.org/10.1016/j.cub.2008.10.009
  11. Kim, H., Choi, M.S., Kang, K., and Kwon, J.Y. (2016). Behavioral analysis of bitter taste perception in Drosophila larvae. Chem Senses 41, 85-94. https://doi.org/10.1093/chemse/bjv061
  12. Kwon, J.Y., Dahanukar, A., Weiss, L.A., and Carlson, J.R. (2011). Molecular and cellular organization of the taste system in the Drosophila larva. J. Neurosci. 31, 15300-15309. https://doi.org/10.1523/JNEUROSCI.3363-11.2011
  13. LeDue, E.E., Chen, Y.C., Jung, A.Y., Dahanukar, A., and Gordon, M.D. (2015). Pharyngeal sense organs drive robust sugar consumption in Drosophila. Nat. Commun. 6, 6667. https://doi.org/10.1038/ncomms7667
  14. Lee, Y., Moon, S.J., and Montell, C. (2009). Multiple gustatory receptors required for the caffeine response in Drosophila. Proc. Natl. Acad. Sci. USA 106, 4495-4500. https://doi.org/10.1073/pnas.0811744106
  15. Lee, Y., Moon, S.J., Wang, Y., and Montell, C. (2015). A Drosophila gustatory receptor required for strychnine sensation. Chem. Senses 40, 525-533. https://doi.org/10.1093/chemse/bjv038
  16. Mishra, D., Miyamoto, T., Rezenom, Y.H., Broussard, A., Yavuz, A., Slone, J., Russell, D.H., and Amrein, H. (2013). The molecular basis of sugar sensing in Drosophila larvae. Curr. Biol. 23, 1466-1471. https://doi.org/10.1016/j.cub.2013.06.028
  17. Miyamoto, T., Slone, J., Song, X., and Amrein, H. (2012). A fructose receptor functions as a nutrient sensor in the Drosophila brain. Cell 151, 1113-1125. https://doi.org/10.1016/j.cell.2012.10.024
  18. Moon, S.J., Lee, Y., Jiao, Y., and Montell, C. (2009). A Drosophila gustatory receptor essential for aversive taste and inhibiting male-tomale courtship. Curr. Biol. 19, 1623-1627. https://doi.org/10.1016/j.cub.2009.07.061
  19. Park, J.H., and Kwon, J.Y. (2011). Heterogeneous expression of Drosophila gustatory receptors in enteroendocrine cells. PLoS ONE 6, e29022. https://doi.org/10.1371/journal.pone.0029022
  20. Robertson, H.M., Warr, C.G., and Carlson, J.R. (2003). Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 100 Suppl 2, 14537-14542. https://doi.org/10.1073/pnas.2335847100
  21. Scott, K., Brady, R., Jr., Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C., and Axel, R. (2001). A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661-673. https://doi.org/10.1016/S0092-8674(01)00263-X
  22. Shim, J., Lee, Y., Jeong, Y.T., Kim, Y., Lee, M.G., Montell, C., and Moon, S.J. (2015). The full repertoire of Drosophila gustatory receptors for detecting an aversive compound. Nat. Commun. 6, 8867. https://doi.org/10.1038/ncomms9867
  23. Stafford, J.W., Lynd, K.M., Jung, A.Y., and Gordon, M.D. (2012). Integration of taste and calorie sensing in Drosophila. J. Neurosci. 32, 14767-14774. https://doi.org/10.1523/JNEUROSCI.1887-12.2012
  24. Stocker, R.F. (1994). The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275, 3-26. https://doi.org/10.1007/BF00305372
  25. Stocker, R.F. (2004). Taste perception: Drosophila - a model of good taste. Curr. Biol. 14, R560-561. https://doi.org/10.1016/j.cub.2004.07.011
  26. Sweeney, S.T., Broadie, K., Keane, J., Niemann, H., and O'Kane, C.J. (1995). Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14, 341-351. https://doi.org/10.1016/0896-6273(95)90290-2
  27. Tissot, M., and Stocker, R.F. (2000). Metamorphosis in Drosophila and other insects: the fate of neurons throughout the stages. Prog Neurobiol. 62, 89-111. https://doi.org/10.1016/S0301-0082(99)00069-6
  28. Vosshall, L.B., and Stocker, R.F. (2007). Molecular architecture of smell and taste in Drosophila. Annu. Rev. Neurosci. 30, 505-533. https://doi.org/10.1146/annurev.neuro.30.051606.094306
  29. Weiss, L.A., Dahanukar, A., Kwon, J.Y., Banerjee, D., and Carlson, J.R. (2011). The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258-272. https://doi.org/10.1016/j.neuron.2011.01.001
  30. Zhang, Y.V., Ni, J., and Montell, C. (2013). The molecular basis for attractive salt-taste coding in Drosophila. Science 340, 1334-1338. https://doi.org/10.1126/science.1234133

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