The full repertoire of Drosophila gustatory receptors for detecting an aversive compound

Nature Communications

Volumn 6, Issue , 2015, Pages

  Shim, Jaewon ^a,b   Lee, Youngseok ^c   Jeong, Yong Taek ^a   Kim, Yonjung ^d   Lee, Min Goo ^d   Montell, Craig ^e   Moon, Seok Jun ^a  

^a Yonsei University College of Dentistry   (South Korea)

^b Korea Food Research Institute   (South Korea)

^c Kookmin University   (South Korea)

^d Yonsei University College of Medicine   (South Korea)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANAVANINE; CELL SURFACE RECEPTOR; DROSOPHILA PROTEIN; GR66A PROTEIN, DROSOPHILA; GR8A PROTEIN, DROSOPHILA; GR98A PROTEIN, DROSOPHILA; GUSTATORY RECEPTOR, DROSOPHILA; INSECTICIDE;

AVOIDANCE REACTION; CATION; FLY; GENE EXPRESSION; SENSORY SYSTEM; SURVIVAL; TOXIC MATERIAL;

ACTION POTENTIAL; ARTICLE; CATION TRANSPORT; CONTROLLED STUDY; DROSOPHILA; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TASTE AVERSION; TASTE BUD; ANIMAL; AVOIDANCE BEHAVIOR; CHEMORECEPTOR CELL; DROSOPHILA MELANOGASTER; GENETICS; METABOLISM; PATCH CLAMP TECHNIQUE;

ANIMALIA; HEXAPODA;

ANIMALS; AVOIDANCE LEARNING; CANAVANINE; CHEMORECEPTOR CELLS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; INSECTICIDES; PATCH-CLAMP TECHNIQUES; RECEPTORS, CELL SURFACE; TASTE BUDS;

EID: 84947292961     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9867     Document Type: Article

References (46)

1. Liman, E. R., Zhang, Y. V. & Montell, C. Peripheral coding of taste. Neuron 81, 984-1000 (2014).
2. Kim, S. H. et al. Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons. Proc. Natl Acad. Sci. USA 107, 8440-8445 (2010).
3. Kwon, Y. et al. Drosophila TRPA1 channel is required to avoid the naturally occurring insect repellent citronellal. Curr. Biol. 20, 1672-1678 (2010).
4. Zhang, Y. V., Raghuwanshi, R. P., Shen, W. L. & Montell, C. Food-experience induced taste desensitization modulated by the Drosophila TRPL channel. Nat. Neurosci. 16, 1468-1476 (2013).
5. Clyne, P. J., Warr, C. G. & Carlson, J. R. Candidate taste receptors in Drosophila. Science 287, 1830-1834 (2000).
6. Dunipace, L., Meister, S., McNealy, C. & Amrein, H. Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 11, 822-835 (2001).
7. Robertson, H. M., Warr, C. G. & Carlson, J. R. Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 100(Suppl 2): 14537-14542 (2003).
8. Scott, K. et al. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661-673 (2001).
9. Clyne, P. J. et al. The odor specificities of a subset of olfactory receptor neurons are governed by Acj6, a POU-domain transcription factor. Neuron 22, 339-347 (1999).
10. Gao, Q. & Chess, A. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60, 31-39 (1999).
11. Meunier, N., Marion-Poll, F., Rospars, J. P. & Tanimura, T. Peripheral coding of bitter taste in Drosophila. J. Neurobiol. 56, 139-152 (2003).
12. Montell, C. A taste of the Drosophila gustatory receptors. Curr. Opin. Neurobiol. 19, 345-353 (2009).
13. Scott, K. The sweet and the bitter of mammalian taste. Curr. Opin. Neurobiol. 14, 423-437 (2004).
14. Vosshall, L. B., Amrein, H., Morozov, P. S., Rzhetsky, A. & Axel, R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725-736 (1999).
15. Sato, K. et al. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452, 1002-1006 (2008).
16. Wicher, D. et al. Drosophila odorant receptors are both ligand-gated and cyclicnucleotide-activated cation channels. Nature 452, 1007-1011 (2008).
17. Turner, R. M. et al. Mutational analysis of cysteine residues of the insect odorant co-receptor (Orco) from Drosophila melanogaster reveals differential effects on agonist- and odorant-tuning receptor-dependent activation. J. Biol. Chem. 289, 31837-31845 (2014).
18. Sato, K., Tanaka, K. & Touhara, K. Sugar-regulated cation channel formed by an insect gustatory receptor. Proc. Natl Acad. Sci. USA 108, 11680-11685 (2011).
19. Lee, Y., Kim, S. H. & Montell, C. Avoiding DEET through insect gustatory receptors. Neuron 67, 555-561 (2010).
20. Moon, S. J., Köttgen, M., Jiao, Y., Xu, H. & Montell, C. A taste receptor required for the caffeine response in vivo. Curr. Biol. 16, 1812-1817 (2006).
21. Moon, S. J., Lee, Y., Jiao, Y. & Montell, C. A. Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr. Biol. 19, 1623-1627 (2009).
22. Lee, Y. et al. Gustatory receptors required for avoiding the insecticide L-canavanine. J. Neurosci. 32, 1429-1435 (2012).
23. Lee, Y., Moon, S. J. & Montell, C. Multiple gustatory receptors required for the caffeine response in Drosophila. Proc. Natl Acad. Sci. USA 106, 4495-4500 (2009).
24. Lee, Y., Moon, S., Wang, Y. & Montell, C. A Drosophila gustatory receptor required for strychnine sensation. Chem. Senses 40, 525-533 (2015).
25. Dahlman, D. L. & Rosenthal, G. A. Non-protein aminoacid-insect interactions-I. Growth effects and symptomology of L-canavanine consumption by tobacco hornworm, Manduca sexta (L.). Comp. Biochem. Physiol. A Comp. Physiol. 51, 33-36 (1975).
26. Rosenthal, G. A. L-Canavanine: a higher plant insecticidal allelochemical. Amino Acids 21, 319-330 (2001).
27. Rosenthal, G. A. & Dahlman, D. L. L-Canavanine and protein synthesis in the tobacco hornworm Manduca sexta. Proc. Natl Acad. Sci. USA 83, 14-18 (1986).
28. Croset, V. et al. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet. 6, e1001064 (2010).
29. Koh, T. W. et al. The Drosophila IR20a clade of ionotropic receptors are candidate taste and pheromone receptors. Neuron 83, 850-865 (2014).
30. Weiss, L. A., Dahanukar, A., Kwon, J. Y., Banerjee, D. & Carlson, J. R. The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258-272 (2011).
31. Wang, Z., Singhvi, A., Kong, P. & Scott, K. Taste representations in the Drosophila brain. Cell 117, 981-991 (2004).
32. Thorne, N., Chromey, C., Bray, S. & Amrein, H. Taste perception and coding in Drosophila. Curr. Biol. 14, 1065-1079 (2004).
33. Zhang, Y. V., Ni, J. & Montell, C. The molecular basis for attractive salt-taste coding in Drosophila. Science 340, 1334-1338 (2013).
34. Freeman, E. G., Wisotsky, Z. & Dahanukar, A. Detection of sweet tastants by a conserved group of insect gustatory receptors. Proc. Natl Acad. Sci. USA 111, 1598-1603 (2014).
35. Marella, S. et al. Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49, 285-295 (2006).
36. Mueller, K. L. et al. The receptors and coding logic for bitter taste. Nature 434, 225-229 (2005).
37. Zhao, G. Q. et al. The receptors for mammalian sweet and umami taste. Cell 115, 255-266 (2003).
38. Wisotsky, Z., Medina, A., Freeman, E. & Dahanukar, A. Evolutionary differences in food preference rely on Gr64e, a receptor for glycerol. Nat. Neurosci. 14, 1534-1541 (2011).
39. Jones, W. D., Cayirlioglu, P., Grunwald Kadow, I. & Vosshall, L. B. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445, 86-90 (2007).
40. Jiao, Y., Moon, S. J. & Montell, C. 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 (2007).
41. Jiao, Y., Moon, S. J., Wang, X., Ren, Q. & Montell, C. Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr. Biol. 18, 1797-1801 (2008).
42. Slone, J., Daniels, J. & Amrein, H. Sugar receptors in Drosophila. Curr. Biol. 17, 1809-1816 (2007).
43. Benton, R., Sachse, S., Michnick, S. W. & Vosshall, L. B. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4, e20 (2006).
44. Dahanukar, A., Lei, Y. T., Kwon, J. Y. & Carlson, J. R. Two Gr genes underlie sugar reception in Drosophila. Neuron 56, 503-516 (2007).
45. Gong, W. J. & Golic, K. G. Ends-out, or replacement, gene targeting in Drosophila. Proc. Natl Acad. Sci. USA 100, 2556-2561 (2003).
46. Hodgson, E. S., Lettvin, J. Y. & Roeder, K. D. Physiology of a primary chemoreceptor unit. Science 122, 417-418 (1955).