Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Ionotropic Receptor 76b Is Required for Gustatory Aversion to Excessive Na+ in Drosophila

  • Lee, Min Jung (Samsung Medical Center, Department of Anatomy and Cell Biology, School of Medicine, Sungkyunkwan University) ;
  • Sung, Ha Yeon (Department of Biological Sciences, Sungkyunkwan University) ;
  • Jo, HyunJi (Samsung Medical Center, Department of Anatomy and Cell Biology, School of Medicine, Sungkyunkwan University) ;
  • Kim, Hyung-Wook (College of Life Sciences, Sejong University) ;
  • Choi, Min Sung (Department of Biological Sciences, Sungkyunkwan University) ;
  • Kwon, Jae Young (Department of Biological Sciences, Sungkyunkwan University) ;
  • Kang, KyeongJin (Samsung Medical Center, Department of Anatomy and Cell Biology, School of Medicine, Sungkyunkwan University)
  • Received : 2017.08.03
  • Accepted : 2017.08.23
  • Published : 2017.10.31
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Abstract

Avoiding ingestion of excessively salty food is essential for cation homeostasis that underlies various physiological processes in organisms. The molecular and cellular basis of the aversive salt taste, however, remains elusive. Through a behavioral reverse genetic screening, we discover that feeding suppression by $Na^+$-rich food requires Ionotropic Receptor 76b (Ir76b) in Drosophila labellar gustatory receptor neurons (GRNs). Concentrated sodium solutions with various anions caused feeding suppression dependent on Ir76b. Feeding aversion to caffeine and high concentrations of divalent cations and sorbitol was unimpaired in Ir76b-deficient animals, indicating sensory specificity of Ir76b-dependent $Na^+$ detection and the irrelevance of hyperosmolarity-driven mechanosensation to Ir76b-mediated feeding aversion. Ir76b-dependent $Na^+$-sensing GRNs in both L- and s-bristles are required for repulsion as opposed to the previous report where the L-bristle GRNs direct only low-$Na^+$ attraction. Our work extends the physiological implications of Ir76b from low-$Na^+$ attraction to high-$Na^+$ aversion, prompting further investigation of the physiological mechanisms that modulate two competing components of $Na^+$-evoked gustation coded in heterogeneous Ir76b-positive GRNs.

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References

  1. Benton, R., Vannice, K.S., Gomez-Diaz, C., and Vosshall, L.B. (2009). Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136, 149-162. https://doi.org/10.1016/j.cell.2008.12.001
  2. Brand, J. G., Teeter, J. H., Kumazawa, T., Huque, T., and Bayley, D. L. (1991). Transduction mechanisms for the taste of amino acids. Physiol. Behav. 49, 899-904. https://doi.org/10.1016/0031-9384(91)90201-X
  3. Calleja, M., Moreno, E., Pelaz, S., and Morata, G. (1996). Visualization of gene expression in living adult Drosophila. Science 274, 252-255. https://doi.org/10.1126/science.274.5285.252
  4. Chandrashekar, J., Kuhn, C., Oka, Y., Yarmolinsky, D.A., Hummler, E., Ryba, N.J.P., and Zuker, C.S. (2010). The cells and peripheral representation of sodium taste in mice. Nature 464, 297-301. https://doi.org/10.1038/nature08783
  5. Chatzigeorgiou, M., Bang, S., Hwang, S.W., and Schafer, W.R. (2013). tmc-1 encodes a sodium-sensitive channel required for salt chemosensation in C. elegans. Nature 494, 95-99. https://doi.org/10.1038/nature11845
  6. Chung, K.M., Lee, S.B., Heur, R., Cho, Y.K., Lee, C.H., Jung, H.Y., Chung, S.H., Lee, S.P., and Kim, K.N. (2005). Glutamate-induced cobalt uptake elicited by kainate receptors in rat taste bud cells. Chem. Senses 30, 137-143. https://doi.org/10.1093/chemse/bji009
  7. Croset, V., Schleyer, M., Arguello, J.R., Gerber, B., and Benton, R. (2016). A molecular and neuronal basis for amino acid sensing in the Drosophila larva. Sci. Rep. 6, 34871. https://doi.org/10.1038/srep34871
  8. Deshpande, S.A., Carvalho, G.B., Amador, A., Phillips, A.M., Hoxha, S., Lizotte, K.J., and Ja, W.W. (2014). Quantifying Drosophila food intake: comparative analysis of current methodology. Nat. Meth. 11, 535-540. https://doi.org/10.1038/nmeth.2899
  9. 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
  10. Du, E.J., Ahn, T.J., Kwon, I., Lee, J.H., Park, J.-H., Park, S.H., Kang, T.M., Cho, H., Kim, T.J., Kim, H.-W., et al. (2016a). TrpA1 regulates defecation of food-borne pathogens under the control of the duox pathway. PLoS Genet. 12, e1005773. https://doi.org/10.1371/journal.pgen.1005773
  11. Du, E.J., Ahn, T.J., Wen, X., Seo, D.-W., Na, D.L., Kwon, J.Y., Choi, M., Kim, H.-W., Cho, H., and Kang, K. (2016b). Nucleophile sensitivity of Drosophila TRPA1 underlies light-induced feeding deterrence. Elife 5, e18425.
  12. Frisoli, T.M., Schmieder, R.E., Grodzicki, T., and Messerli, F.H. (2012). Salt and hypertension: is salt dietary reduction worth the effort? Am. J. Med. 125, 433-439. https://doi.org/10.1016/j.amjmed.2011.10.023
  13. Ganguly, A., Pang, L., Duong, V.-K., Lee, A., Schoniger, H., Varady, E., and Dahanukar, A. (2017). A Molecular and cellular contextdependent role for Ir76b in detection of amino acid taste. Cell Rep. 18, 737-750. https://doi.org/10.1016/j.celrep.2016.12.071
  14. Gramates, L.S., Marygold, S.J., Santos, G. dos, Urbano, J.-M., Antonazzo, G., Matthews, B.B., Rey, A.J., Tabone, C.J., Crosby, M.A., Emmert, D.B., et al. (2017). FlyBase at 25: looking to the future. Nucleic Acids Res. 45, D663-D671. https://doi.org/10.1093/nar/gkw1016
  15. Hahn, Y., Kim, D.S., Pastan, I.H., and Lee, B. (2009). Anoctamin and transmembrane channel-like proteins are evolutionarily related. Int. J. Mol. Med. 24, 51-55.
  16. He, F.J., and MacGregor, G.A. (2008). A comprehensive review on salt and health and current experience of worldwide salt reduction programmes. J. Hum. Hypertens 23, 363-384.
  17. Hiroi, M., Meunier, N., Marion-Poll, F., and Tanimura, T. (2004). Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J. Neurobiol. 61, 333-342. https://doi.org/10.1002/neu.20063
  18. Hodgson, E.S., Lettvin, J.Y., and Roedert, K.D. (1955). Physiology of a primary chemoreceptor unit. Science 122, 121-122. https://doi.org/10.1126/science.122.3159.121
  19. Ja, W.W., Carvalho, G.B., Mak, E.M., de la Rosa, N.N., Fang, A.Y., Liong, J.C., Brummel, T., and Benzer, S. (2007). Prandiology of Drosophila and the CAFE assay. Proc. Natl. Acad. Sci. USA 104, 8253-8256. https://doi.org/10.1073/pnas.0702726104
  20. Kang, K., Pulver, S.R., Panzano, V.C., Chang, E.C., Griffith, L.C., Theobald, D.L., and Garrity, P.A. (2010). Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature 464, 597-600. https://doi.org/10.1038/nature08848
  21. Kang, K., Panzano, V.C., Chang, E.C., Ni, L., Dainis, A.M., Jenkins, A.M., Regna, K., Muskavitch, M.A.T. and Garrity, P.A. (2012). Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481, 76-80. https://doi.org/10.1038/nature10715
  22. Kleinewietfeld, M., Manzel, A., Titze, J., Kvakan, H., Yosef, N., Linker, R.A., Muller, D.N., and Hafler, D.A. (2013). Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 496, 518-522. https://doi.org/10.1038/nature11868
  23. Knecht, Z.A., Silbering, A.F., Ni, L., Klein, M., Budelli, G., Bell, R., Abuin, L., Ferrer, A.J., Samuel, A.D., Benton, R., et al. (2016). Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. Elife 5, 44-60.
  24. Knecht, Z.A., Silbering, A.F., Cruz, J., Yang, L., Croset, V., Benton, R. and Garrity, P.A. (2017). Ionotropic Receptor-dependent moist and dry cells control hygrosensation in Drosophila. Elife 6,.
  25. Ko, K.I., Root, C.M., Lindsay, S.A., Zaninovich, O.A., Shepherd, A.K., Wasserman, S.A., Kim, S.M., Wang, J.W., Pachter, L., Lavista-Llanos, S., et al. (2015). Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits. Elife 4, e50801.
  26. Koushika, S.P., Lisbin, M.J., and White, K. (1996). ELAV, a Drosophila neuron-specific protein, mediates the generation of an alternatively spliced neural protein isoform. Curr. Biol. 6, 1634-1641. https://doi.org/10.1016/S0960-9822(02)70787-2
  27. Mun, H.-C., Franks, A.H., Culverston, E.L., Krapcho, K., Nemeth, E.F., and Conigrave, A.D. (2004). The venus fly trap domain of the extracellular $Ca^{2+}$-sensing receptor is required for l-amino acid sensing. J. Biol. Chem. 279, 51739-51744. https://doi.org/10.1074/jbc.M406164200
  28. Ni, L., Klein, M., Svec, K.V, Budelli, G., Chang, E.C., Ferrer, A.J., Benton, R., Samuel, A.D., and Garrity, P. A. (2016). The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila. Elife 5, e13254.
  29. Niewalda, T., Singhal, N., Fiala, A., Saumweber, T., Wegener, S., and Gerber, B. (2008). Salt processing in larval Drosophila: choice, feeding, and learning shift from appetitive to aversive in a concentration-dependent way. Chem. Senses 33, 685-692. https://doi.org/10.1093/chemse/bjn037
  30. Oka, Y., Butnaru, M., von Buchholtz, L., Ryba, N.J.P., and Zuker, C.S. (2013). High salt recruits aversive taste pathways. Nature 1-5.
  31. Plested, A.J.R., Vijayan, R., Biggin, P.C., and Mayer, M.L. (2008). Molecular basis of kainate receptor modulation by sodium. Neuron 58, 720-735. https://doi.org/10.1016/j.neuron.2008.04.001
  32. Rosenzweig, M., Kang, K., and Garrity, P.A.P.A. (2008). Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 105, 14668-73. https://doi.org/10.1073/pnas.0805041105
  33. Silbering, A.F., Rytz, R., Grosjean, Y., Abuin, L., Ramdya, P., Jefferis, G.S.X.E., and Benton, R. (2011). Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J. Neurosci. 31, 13357-75. https://doi.org/10.1523/JNEUROSCI.2360-11.2011
  34. Tsugane, S., Sasazuki, S., Kobayashi, M., and Sasaki, S. (2004). Salt and salted food intake and subsequent risk of gastric cancer among middle-aged Japanese men and women. Br. J. Cancer 90, 128-134. https://doi.org/10.1038/sj.bjc.6601511
  35. Wang, X., Li, G., Liu, J., Liu, J., Xu, X.Z.S., Wang, X., Li, G., Liu, J., Liu, J., and Xu, X.Z.S. (2016). TMC-1 mediates alkaline sensation in C . elegans through nociceptive neurons. Neuron 91, 146-154. https://doi.org/10.1016/j.neuron.2016.05.023
  36. 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
  37. Wong, X.M., Younger, S., Peters, C.J., Jan, Y.N., Jan, L.Y., and Shim, W. (2013). Subdued, a TMEM16 family $Ca^{2+}$ -activated $Ca^{-}$ channel in Drosophila melanogaster with an unexpected role in host defense. Elife 2, e00862.
  38. Yarmolinsky, D.A, Zuker, C.S., and Ryba, N.J.P. (2009). Common sense about taste: from mammals to insects. Cell 139, 234-244. https://doi.org/10.1016/j.cell.2009.10.001
  39. Zelle, K.M., Lu, B., Pyfrom, S.C., and Ben-Shahar, Y. (2013). The genetic architecture of degenerin/epithelial sodium channels in Drosophila. G3 (Bethesda). 3, 441-450.
  40. 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
  41. Zitron, A.E., and Hawley, R.S. (1989). The genetic analysis of distributive segregation in Drosophila melanogaster. Genetics 122, 801-821.

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