Molecular and cellular designs of insect taste receptor system

Frontiers in Cellular Neuroscience

Volumn 4, Issue , 2010, Pages 1-43

  Isono, Kunio ^a   Morita, Hiromi ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CANAVANINE; CAPSAICIN; G PROTEIN COUPLED RECEPTOR; PHEROMONE; PHEROMONE RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1;

ARTICLE; BITTER TASTE; CELL STRUCTURE; CELLULAR DISTRIBUTION; DROSOPHILA; MOLECULAR EVOLUTION; NERVE CELL DIFFERENTIATION; NERVE PROJECTION; NONHUMAN; OLFACTORY DISCRIMINATION; OLFACTORY RECEPTOR; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SENSORY NERVE CELL; SOMATOSENSORY STIMULATION; SWEETNESS; TASTE ACUITY; TASTE BUD; TASTE DISCRIMINATION;

EID: 77953436599     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2010.00020     Document Type: Article

References (108)

1. Adler, E., Hoon, M. A., Mueller, K. L., Chandrashekar, J., Ryba, N. J., and Zuker, C. S. (2000). A novel family of mammalian taste receptors. Cell 100, 693-702.
2. Al-Anzi, B., Tracey, W. D. Jr, and Benzer, S. (2006). Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANKTM1. Curr. Biol. 16, 1034-1040.
3. Amrein, H., and Thorne, N. (2005). Gustatory Perception and Behavior in Drosophila melanogaster. Curr. Biol. 15, R673-R684
4. Arora K., Rodrigues, V., Joshi, S., Shanbhag, S., and Siddiqi, O. (1987). A gene affecting the specificity of the chemosensory neurons of Drosophila. Nat. 330, 62-63.
5. Awasaki, T., and Kimura, K. (1997). pox-neuro is required for development of chemosensory bristles in Drosophila. J. Neurobiol. 32, 707-721.
6. Bodmer, R., Barbel, S., Sheperd, S., Jack, J. W., Jan, L. Y., and Jan, Y. N. (1987). Transformation of sensory organs by mutations of the cut locus of D. melanogaster. Cell 51, 293-307.
7. Bray, S., and Amrein, H. (2003). A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39, 1019-1029.
8. Bruyne, M. de, and Warr C. G. (2005). Molecular and cellular organization of insect chemosensory neurons. BioEssays 28, 23-34.
9. Buck, L., and Axel, R. (1991). A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. Cell 65, 175-187.
10. Chyb, S., Dahanukar, A., Wickens, A., and Carlson, J. R. (2003). Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc. Natl. Acad. Sci. 100, 14526-14530.
11. Clyne, P. J., Warr, C. G., and Carlson, J. R. (2000). Candidate taste receptors in Drosophila. Sci. 287, 1830-1834.
12. Colomb, J., Grillenzoni, N., Ramaekers, A., and Stocker, R. F. (2007). Architecture of the primary taste center of Drosophila melanogaster larvae. J. Compara. Neurol. 502, 834-847.
13. Couto, A., Alenius, M., and Dickson, B. J. (2005). Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535-1547.
14. Dahanukar, A., Foster, K., van der Goes van Naters, W. M., Carlson, J. R. (2001). A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat. Neurosci. 4, 1182-1186.
15. 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.
16. Dambly-Chaudière, C., Jamet, E., Burri, M., Bopp, D., Basler, K., Hafen, E., Dumont, N., Spielmann, P., Ghysen, A., and Noll, M. (1992). The paired box gene pox neuro: a determinant of poly-innervated sense organs in Drosophila. Cell 69, 159-172.
17. Dethier, V. G., and Hanson, F. E. (1968). Electrophysiological responses of the chemoreceptors of the blowfly to sodium salts of fatty acids. Proc. Natl. Acad. Sci. 60, 1296-1303.
18. Dethier, V. G. (1976). The hungry fly: A physiological study of the behavior associated with feeding (Cambridge, MA: Harvard University Press).
19. Dong, X., Han, S., Zylka, M. J., Simon, M. I., and Anderson, D. J. (2001). A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell 106, 619-632.
20. Dunipace, L., Meister S., McNealy, C., and Amrein, H. (2001). Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 11, 822-835.
21. Edwards, S. L., Charlie, N. K., Milfort, M. C., Brown, B. S., Gravlin, C. N., Knecht, J. E., and Miller, K. G. (2008). A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biol. 6, e198.
22. Ejima, A., Smith, B. P. C., Lucas, C., van der Goes van Naters, W., Miller, C. J., Carlson, J. R., Levine, J. D., and Griffith, L. C. (2007). Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr. Biol. 17, 599-605.
23. Ejima, A., and Griffith, L. C. (2008). Courtship initiation is stimulated by acoustic signals in Drosophila melanogaster. PLoS ONE 3, e3246.
24. Falk, R., and Atidia, J. (1975). Mutation affecting taste perception in Drosophila melanogaster. Nat. 254, 325-326.
25. Faucher, C., Forstreuter, M., Hilker, M., and de Bruyne, M. (2006). Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context. J. Experimental Biol. 209, 2739-2748.
26. Ferveur J. F., and Jallon, J. M. (1996). Genetic control of male cuticular hydrocarbons in Drosophila melanogaster. Genet. Res. 67, 211-218.
27. Fischler, W., Kong, P., Marella, S., and Scott, K. (2007). The detection of carbonation by the Drosophila gustatory system. Nat. 448, 1054-1057.
28. Fishilevich, E., and Vosshall, L. B. (2005a). Genetic and Functional Subdivision of the Drosophila Antennal Lobe. Curr. Biol. 15, 1548-1553.
29. Fishilevich, E., Domingos, A. I., Asahina, K., Naef, F., Vosshall, L. B., and Louis, M. (2005b). Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr. Biol. 15, 2086-2096.
30. Fujishiro, N., Kijima, H., and Morita, H. (1984). Impulse frequency and action potential amplitude in labellar chemosensory neurons of Drosophila melanogaster. J. Insect Physiol. 30, 317-325.
31. García-Bellido, A., and Santamaria, P. (1978). Developmental analysis of the achaete-scute system of Drosophila melanogaster. Genet. 88, 469-486.
32. Gendre, N., Lüer, 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.
33. Glendinning, J. I., Domdom, S., and Long, E. (2001). Selective adaptation to noxious foods by a herbivorous insect. J. Exp. Biol. 204, 3355-3367.
34. Glendinning, J. I., Davis, A., and Ramaswamy, S. (2002). Contribution of different taste cells and signaling pathways to the discrimination of bitter taste stimuli by an insect. J. Neurosci. 22, 7281-7287.
35. Halpern, B. P. (1998). Amiloride and vertebrate gustatory responses to NaCl. Neurosci. Biobehavioral Reviews 23, 5-47.
36. Herness, M. S., and Gilbertson, T. A. (1999). Cellular mechanisms of taste transduction. Annu. Rev. Physiol. 61, 873-900.
37. Hill, C. A., Fox, A. N., Pitts, R. J., Kent, L. B., Tan, P. L., Chrystal, M. A., Cravchik, A., Collins, F. H., Robertson, H. M., and Zwiebel, L. J. (2002). G protein- coupled receptors in Anopheles gambiae. Sci. 298, 176-178.
38. 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.
39. Huang, A. L., Chen, X., Hoon, M. A., Chandrashekar, J., Guo, W., Tränkner, D., Ryba, N. J., and Zuker, C. S. (2006). The cells and logic for mammalian sour taste detection. Nat. 442, 934-938.
40. Hummel, T., Vasconcelos, M. L., Clemens, J. C., Fishilevich, Y., Vosshall, L. B., and Zipursky, S. L. (2003). Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 37, 221-231.
41. Ikeya, T., Galic, M., Belawat, P., Nairz, K., and Hafen, E. (2002). Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr. Biol. 12, 1293-1300.
42. Inomata, N., Goto, H., Itoh, M., and Isono, K. (2004). A single-amino-acid change of the gustatory receptor gene, Gr5a, has a major effect on trehalose Sensitivity in a natural population of Drosophila melanogaster. Genet. 167, 1749-1758.
43. Isono, K., and Kikuchi, T. (1974). Autosomal recessive mutation in sugar response of Drosophila. Nat. 248, 243-244.
44. Isono, K., Morita, H., Kohatsu, S., Ueno, K., Matsubayashi, H., and Yamamoto, M. T. (2005). Trehalose sensitvity of the gustatory neurons expressing wild-type, mutant and ectopic Gr5a in Drosophila. Chem. Senses 30, i275-276.
45. Jallon, J. M. (1984). A few chemical words exchanged by Drosophila during courtship and mating. Behav.Genet. 14, 441-478.
46. 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. 104, 14110-14115.
47. 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.
48. Jones, W. D., Cayirlioglu, P., Kadow, I. G., and Vosshall, L. B. (2007). Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nat. 445, 86-90.
49. Kankel, D. R., Ferrus, A., Garen, S. H., Harte, P. J., and Lewis, P. E. (1980). The genetics and biology of Drosophila, 2d, M. Ashburner and T. R. F. Wright, ed. (London and New York: Academic Press), pp. 295-368.
50. Kent, L.B. and Robertson, H. M. (2009). Evolution of the sugar receptors in insects. BMC Evolutionary Biol. 9:41.
51. Komiyama, T., Carlson, J. R., and Luo, L. (2004). Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions. Nat. Neurosci. 7, 819-825.
52. Kwon, J. Y., Dahanukar, A., Weiss, L. A., and Carlson, J. R. (2007). The molecular basis of CO2 reception in Drosophila. Proc. Natl. Acad. Sci. 104, 3574-3578.
53. Lacaille, F., Hiroi, M., Twele, R., Inoshita, T., Umemoto, D., Manière, G., Marion-Poll, F., Ozaki, M., Francke, W., Cobb, M., Everaerts, C., Tanimura, T., and Ferveur, J. F. (2007). An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS One 2, e661.
54. Lee, Y., Lee, Y., Lee, J., Bang, S., Hyun, S., Kang, J., Hong, S. T., Bae, E., Kaang, B. K., and Kim, J. (2005). Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster. Nat. Genet. 37, 305-310.
55. Lee, Y., Moon, S. J., and Montell, C. (2009). Multiple gustatory receptors required for the caffeine response in Drosophila. Proc. Natl. Acad. Sci. 106, 4495-4500.
56. Liu, L., Leonard, A. S., Motto, D. G., Feller, M. A., Price, M. P., Johnson, W. A., and Welsh, M. J. (2003). Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron 39, 133-146.
57. McBride, C. S., and Arguello, J. R. (2007). Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics 177, 1395-1416.
58. Meunier, N., Marion-Poll, F., Rospars, J. P., and Tanimura, T. (2003). Peripheral coding of bitter taste in Drosophila. J. Neurobiol. 56, 139-152.
59. Meunier, N., Marion-Poll, F., and Lucas, P. (2009). Water taste transduction pathway is calcium dependent in Drosophila. Chem. Senses. 34, 441-449.
60. Minke, B., and Parnas, M. (2006). Insights on TRP channels from in vivo studies in Drosophila. Annu. Rev. Physiol. 68, 649-684.
61. Minnnich, D. E. (1921). An experimental study of the tarsal chemoreceptors of two nymphalid butterflies. J. Exp. Zool. 33, 173-203.
62. Mitchell, B. K., Itagaki, H., and Rivet, M. P. (1999). Peripheral and central structures involved in insect gustation. Microsc. Res. Tech. 47, 401-415.
63. Mitri, C., Soustelle, L., Framery, B., Bockaert, J., Parmentier, M. L., and Grau, Y. (2009). Plant insecticide L-canavanine repels Drosophila via the insect orphan GPCR DmX. PLoS Biol. 7, e1000147.
64. Miyamoto, T., and Amrein, H. (2008). Suppression of male courtship by a Drosophila pheromone receptor. Nat. Neurosci. 11, 874-876.
65. Montell, C. (2009). A taste of the Drosophila gustatory receptors. Curr. Opin. Neurobiol. 19, 345-353.
66. Moon, S. J., Köttgen, M., Jiao, Y., Xu, H., and Montel, C. (2006). A taste receptor required for the caffeine response in vivo. Curr. Biol. 16, 1812-1817.
67. Moon, S. J., Lee, Y., Jiao, Y., and Montell, C. (2009). A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr. Biol. 19, 1623-1627.
68. Morita, H. (1972). Primary processes of insect chemoreception. Adv. Biophys. 3, 161-198.
69. Nakagawa, T., Sakurai, T., Nishioka, T., and Touhara, K. (2005). Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Sci. 307, 1638-1642.
70. Nakamura, M., Baldwin, D., Hannaford, S., Palka, J., and Montell, C. (2002). Defective proboscis extension response (DPR), a member of the Ig superfamily required for the gustatory response to salt. J. Neurosci. 22, 3463-3472.
71. Nayak, S. Y., and Singh, R. N. (1983). Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster meigen (Diptera: Drosophilidae). Int. J. Insect Morphol. Embryol. 12, 273-291.
72. Nelson, G., Hoon, M. A., Chandrashekar, J., Zhang, Y., Ryba, N. J. P., and Zuker, C. S. (2001). Mammalian sweet taste receptors. Cell 106, 381-390.
73. Nelson, G., Chandrashekar, J., Hoon, M. A., Feng, L., Zhao, G., Ryba, N. J. P., and Zuker, C. S. (2002). An amino-acid taste receptor. Nat. 416, 199-202.
74. Neuhaus, E. M., Gisselmann, G., Zhang, W., Dooley, R., Störtkuhl, K., and Hatt, H. (2005). Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat. Neurosci. 8, 15-17.
75. Pitts, R. J., Fox, A. N., and Zwiebel, L. J. (2004). A highly conserved candidate chemoreceptor expressed in both olfactory and gustatory tissues in the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci. 101, 5058-5063.
76. Pollack, G., and Balakrishnan, R. (1997). Taste sensilla of flies: Function, central neuronal projections, and development. Microsc. Res. Tech. 39, 532-546.
77. Python, F., and Stocker, R. F. (2002). Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J. Compara. Neurol. 445, 374-387.
78. Rajashekhar, K. P., and Singh, R. N. (1994). Neuroarchitecture of the tritocerebrum of Drosophila melanogaster. J. Comp. Neurol. 349, 633-645.
79. Ramsey, I. S., Delling, M., and Clapham, D. E. (2006). An introduction to TRP channels. Annu. Rev. Physiol. 68, 619-647.
80. 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. 100, 14537-14542.
81. Robertson, H. M., and Wanner, K. W. (2006). The chemoreceptor superfamily in the honey bee, Apis mellifera: Expansion of the odorant, but not gustatory, receptor family. Genome Research 16, 1395-1403.
82. Rodrigues, V., and Siddiqi, O. (1981). A gustatory mutant of Drosophila defective in pyranose receptors. Mol. Gen. Genet. 181, 406-408.
83. Rosenzweig, M., Kang, K., and Garrity, P. A. (2008). Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster. Proc. Natl. Acad. Sci. 105, 14668-14673.
84. Sakurai, T., Nakagawa, T., Mitsuno, H., Mori, H., Endo, Y., Tanoue, S., Yasukochi, Y., Touhara, K., and Nishioka, T. (2004). Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc. Natl. Acad. Sci. 101, 16653-16658.
85. Sato, T., Hirono, J., Hamana, H., Ishikawa, T., Shimizu, A., Takashima, I., Kajiwara, R., and Iijima, T. (2008). Architecture of odor information processing in the olfactory system. Anat. Sci. Int. 83, 195-206.
86. Scott, K., Brady, J. R., 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.
87. Scott, K. (2005). Taste recognition: food for thought. Neuron 48, 455-464.
88. Shanbhag, S. R., and Singh, R. N. (1989). Projections and Functional implications of labellar neurons from individual sensilla of Drosophila melanogaster. In Neurobiology of Sensory Systems, R.N. Singh, and N. J. Strausfeld, ed. (New York and London: Plenum Press), pp. 427-437.
89. Shimada, I., Shiraishi, A., Kijima, H., and Morita, H. (1974). Separation of two receptor sites in a single labellar sugar receptor of the flesh-fly by treatment with p-chloromercuribenzoate. J. Insect Physiol. 20, 605-621.
90. Singh, R. N. (1997). Neurobiology of the gustatory systems of Drosophila and some terrestrial insects. Microscopy Res. Tech. 39, 547-563.
91. Slone, J., Daniels, J., and Amrein, H. (2007). Sugar receptors in Drosophila. Curr. Biol. 17, 1809-1816.
92. Stocker, R. F., and Schorderet, M. (1981). Cobalt filling of sensory projections from internal and external mouthparts in Drosophila. Cell Tissue Res. 216, 513-523.
93. Stocker, R. F. (1994). The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275, 3-26.
94. Suh, G. S. B., Wong, A. M., Hergarden, A. C., Wang, J. W., Simon, A. F., Benzer, S., Axel, R., and Anderson, D. J. (2004). A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nat. 431, 854-859.
95. Tanimura, T., Isono, K., Takamura, T., and Shimada, I. (1982). Genetic dimorphism in the taste sensitivity to trehalose in Drosophila melanogaster. J. Compara.Physiol. 147, 433-437.
96. Thomas, J. H., and Robertson, H. M. (2008). The Caenorhabditis chemoreceptor gene families. BioMed Central Biol. 6, 42.
97. Thorne, N., Chromey, C., Bray, S., and Amrein, H. (2004). Taste perception and coding in Drosophila. Curr. Biol. 14, 1065-1079.
98. Thorne, N., and Amrein, H. (2008). Atypical Expression of Drosophila Gustatory Receptor Genes in Sensory and Central Neurons. J. Compa. Neurol. 506, 548-568.
99. Tompkins, L., Cardosa, M. J., White, F. V., and Sanders, T. G. (1979). Isolation and analysis of chemosensory behavior mutants in Drosophila melanogaster. Proc. Natl. Acad. Sci. 76, 884-887.
100. Tracey, W. D. Jr, Wilson, R. I., Laurent, G., and Benzer, S. (2003). Painless, a Drosophila gene essential for nociception. Cell 113, 261-273.
101. Ueno, K., Ohta, M., Morita, H., Mikuni, Y., Nakajima, S., Yamamoto, K., and Isono, K. (2001). Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a. Curr. Biol. 11, 1451-1455.
102. van der Goes van Naters, W., Carlson, J. R. (2007). Receptors and neurons for fly odors in Drosophila. Curr. Biol. 17, 606-612.
103. Wang, Z., Singhvi, A., Kong, P., and Scott, K. (2004). Taste representations in the Drosophila brain. Cell 117, 981-991.
104. Wanner, K. W., Nichols, A. S., Walden, K. K. O., Brockmann, A., Luetje, C. W., and Robertson, H. M. (2007). A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. Proc. Natl. Acad. Sci. 104, 14383-14388.
105. Wicher, D., Schäfer, R., Bauernfeind, R., Stensmyr, M. C., Heller, R., Heinemann, S. H., and Hansson, B. S. (2008). Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nat. 452, 1007-1011.
106. Wilczek, M. (1967). The distribution and neuroanatomy of the labellar sense organs of the blowfly Phormia regina Meigen. J. Morphol. 122, 175-201.
107. Xu, J., Sornborger, A. T., Lee, J. K., and Shen, P. (2008). Drosophila TRPA channel modulates sugar-stimulated neural excitation, avoidance and social response. Nat. Neurosci. 11, 676-682.
108. Zufall, F., and Leinders-Zufall, T. (2007). Mammalian pheromone sensing. Curr. Opini. Neurobiol. 17, 483-489.