Taste and pheromone perception in the fruit fly Drosophila melanogaster

Pflugers Archiv European Journal of Physiology

Volumn 454, Issue 5, 2007, Pages 735-747

  Ebbs, Michelle L ^a   Amrein, Hubert ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Drosophila; GTP binding protein coupled receptors; Gustatory receptor neurons

Indexed keywords

LIGAND; PHEROMONE;

ANATOMY; DROSOPHILA MELANOGASTER; ELECTROPHYSIOLOGY; GUSTATORY SYSTEM; IMAGING; MODEL; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; RESEARCH; REVIEW; SENSORY SYSTEM; SIGNAL PROCESSING; SOCIAL BEHAVIOR; TASTE; TASTE BUD; WILD TYPE;

EID: 34250887007     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-007-0246-y     Document Type: Review

References (105)

1. Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3-26
2. Dethier VG (1976) The hungry fly. Harvard Univ. Press, Cambridge, MA
3. Greenspan RJ, Ferveur JF (2000) Courtship in Drosophila. Annu Rev Genet 34:205-232
4. Hall JC (1994) The mating of a fly. Science 264:1702-1714
5. Amrein H (2004) Pheromone perception and behavior in Drosophila. Curr Opin Neurobiol 14:435-442
6. Ackerman SL, Siegel RW (1986) Chemically reinforced conditioned courtship in Drosophila: responses of wild-type and the dunce, amnesiac and don giovanni mutants. J Neurogenet 3:111-123
7. Bartelt R, Schaner A, Jackson L (1985) Cis-vacceyl acetate as an aggregation pheromone in Drosophila melanogaster. J Chem Ecol 11:1747-1756
8. Xu P, Atkinson R, Jones DN, Smith DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45:193-200
9. Zawistowski S (1988) A replication demonstrating reduced courtship of Drosophila melanogaster by associative learning. J Comp Psychol 102:174-176
10. Coyne JA, Crittenden AP, Mah K (1994) Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila. Science 265:1461-1464
11. Ferveur JF, Cobb M, Boukella H, Jallon JM (1996) World-wide variation in Drosophila melanogaster sex pheromone: behavioural effects, genetic bases and potential evolutionary consequences. Genetica 97:73-80
12. Ferveur JF, Sureau G (1996) Simultaneous influence on male courtship of stimulatory and inhibitory pheromones produced by live sex-mosaic Drosophila melanogaster. Proc R Soc Lond B Biol Sci 263:967-973
13. Scott D (1986) Sexual mimicry regulates the attractiveness of mated Drosophila melanogaster females. Proc Natl Acad Sci USA 83:8429-8433
14. Keverne EB (1999) The vomeronasal organ. Science 286:716-720
15. Amrein H, Thorne N (2005) Gustatory perception and behavior in Drosophila melanogaster. Curr Biol 15:R673-R684
16. Arora K, Rodrigues V, Joshi S, Shanbhag S, Siddiqi O (1987) A gene affecting the specificity of the chemosensory neurons of Drosophila. Nature 330:62-63
17. Rodrigues V, Siddiqi O (1978) Genetic analysis of chemosensory pathway. Proc Indian Acad Sci 87B:147-160
18. Fujishiro N, Kijima H, Morita H (1984) Impulse frequency and action potential amplitude in labellar chemosensory neurons of Drosophila melanogaster. J Insect Physiol 30:317-325
19. Hiroi M, Meunier N, Marion-Poll F, Tanimura T (2004) Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J Neurobiol 61:333-342
20. Meunier N, Marion-Poll F, Rospars JP, Tanimura T (2003) Peripheral coding of bitter taste in Drosophila. J Neurobiol 56:139-152
21. Nayak S, Singh RN (1983) Sensilla on the tarsal segments and the mouthparts of adult Drosophila melanogaster. Int J Insect Morphol Embryol 12
22. Stocker RF, Schorderet M (1981) Cobalt filling of sensory projections from internal and external mouthparts in Drosophila. Cell Tissue Res 216:513-523
23. Rajashekhar KP, Singh RN (1994) Neuroarchitecture of the tritocerebrum of Drosophila melanogaster. J Comp Neurol 349:633-645
24. Falk R, Bleiser-Avivi N, Atidia J (1976) Labellar taste organs of Drosophila melanogaster. J Morphol 150:327-342
25. O'Neil RG, Heller S (2005) The mechanosensitive nature of TRPV channels. Pflügers Arch 451:193-203
26. Sukharev S, Corey DP (2004) Mechanosensitive channels: multiplicity of families and gating paradigms. Sci STKE 2004:re4
27. Shanbhag SR, Hekmat-Scafe D, Kim MS, Park SK, Carlson JR, Pikielny C, Smith DP, Steinbrecht RA (2001) Expression mosaic of odorant-binding proteins in Drosophila olfactory organs. Microsc Res Tech 55:297-306
28. Koganezawa M, Shimada I (2002) Novel odorant-binding proteins expressed in the taste tissue of the fly. Chem Senses 27:319-332
29. Galindo K, Smith DP (2001) A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetics 159:1059-1072
30. Ha TS, Smith DP (2006) A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J Neurosci 26:8727-8733
31. Xu A, Park SK, D'Mello S, Kim E, Wang Q, Pikielny CW (2002) Novel genes expressed in subsets of chemosensory sensilla on the front legs of male Drosophila melanogaster. Cell Tissue Res 307:381-392
32. Park SK, Mann KJ, Lin H, Starostina E, Kolski-Andreaco A, Pikielny CW (2006) A Drosophila protein specific to pheromone-sensing gustatory hairs delays males' copulation attempts. Curr Biol 16:1154-1159
33. Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS (2000) A novel family of mammalian taste receptors. Cell 100:693-702
34. Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJ (2000) T2Rs function as bitter taste receptors. Cell 100:703-711
35. Clyne PJ, Warr CG, Carlson JR (2000) Candidate taste receptors in Drosophila. Science 287:1830-1834
36. Dunipace L, Meister S, McNealy C, Amrein H (2001) Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr Biol 11:822-835
37. Hoon MA, Adler E, Lindemeier J, Battey JF, Ryba NJ, Zuker CS (1999) Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell 96:541-551
38. Matsunami H, Montmayeur JP, Buck LB (2000) A family of candidate taste receptors in human and mouse. Nature 404:601-604
39. Max M, Shanker YG, Huang L, Rong M, Liu Z, Campagne F, Weinstein H, Damak S, Margolskee RF (2001) Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet 28:58-63
40. Montmayeur JP, Liberles SD, Matsunami H, Buck LB (2001) A candidate taste receptor gene near a sweet taste locus. Nat Neurosci 4:492-498
41. Sainz E, Korley JN, Battey JF, Sullivan SL (2001) Identification of a novel member of the T1R family of putative taste receptors. J Neurochem 77:896-903
42. Scott K, Brady R Jr, Cravchik A, Morozov P, Rzhetsky A, Zuker C, Axel R (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104:661-673
43. Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci USA 100(Suppl 2):14537-14542
44. Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20
45. Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117:965-979
46. Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713-723
47. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, Zuker CS, Ryba NJ (2003) Coding of sweet, bitter and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293-301
48. Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS (2003) The receptors for mammalian sweet and umami taste. Cell 115:255-266
49. Ueno K, Ohta M, Morita H, Mikuni Y, Nakajima S, Yamamoto K, Isono K (2001) Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a. Curr Biol 11:1451-1455
50. Chyb S, Dahanukar A, Wickens A, Carlson JR (2003) Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc Natl Acad Sci USA 100(Suppl 2):14526-14530
51. Dahanukar A, Foster K, van der Goes van Naters WM, Carlson JR (2001) A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat Neurosci 4:1182-1186
52. Bray S, Amrein H (2003) A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39:1019-1029
53. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development (Cambridge, England) 118:401-415
54. Thorne N, Chromey C, Bray S, Amrein H (2004) Taste perception and coding in Drosophila. Curr Biol 14:1065-1079
55. Wang Z, Singhvi A, Kong P, Scott K (2004) Taste representations in the Drosophila brain. Cell 117:981-991
56. Moon SJ, Kottgen M, Jiao Y, Xu H, Montell C (2006) A taste receptor required for the caffeine response in vivo. Curr Biol 16:1812-1817
57. Tanimura T, Isono K, Takamura T, Shimada I (1982) Genetic dimorphism in the taste sensitivity to trehalose in Drosophila melanogaster. J Comp Physiol 147:433-437
58. Deak II (1976) Demonstration of sensory neurones in the ectopic cuticle of spineless-aristapedia, a homoeotic mutant of Drosophila. Nature 260:252-254
59. Stocker RF, Edwards JS, Palka J, Schubiger G (1976) Projection of sensory neurons from a homeotic mutant appendage, Antennapedia, in Drosophila melanogaster. Dev Biol 52:210-220
60. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS (2001) Mammalian sweet taste receptors. Cell 106:381-390
61. Meunier N, Ferveur JF, Marion-Poll F (2000) Sex-specific non-pheromonal taste receptors in Drosophila. Curr Biol 10:1583-1586
62. Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, Baker BS (2005) Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436:395-400
63. Stockinger P, Kvitsiani D, Rotkopf S, Tirian L, Dickson BJ (2005) Neural circuitry that governs Drosophila male courtship behavior. Cell 121:795-807
64. Demir E, Dickson BJ (2005) Fruitless splicing specifies male courtship behavior in Drosophila. Cell 121:785-794
65. Ferveur JF, Savarit F, O_Kane CJ, Sureau G, Greenspan RJ, Jallon JM (1997) Genetic feminization of pheromones and its behavioral consequences in Drosophila males. Science 276:1555-1558
66. Sakai T, Kitamoto T (2006) Differential roles of two major brain structures, mushroom bodies and central complex, for Drosophila male courtship behavior. J Neurobiol 66:821-834
67. Broughton SJ, Kitamoto T, Greenspan RJ (2004) Excitatory and inhibitory switches for courtship in the brain of Drosophila melanogaster. Curr Biol 14:538-547
68. Hall JC (1977) Portions of the central nervous system controlling reproductive behavior in Drosophila melanogaster. Behav Genet 7:291-312
69. Hall JC (1979) Control of male reproductive behavior by the central nervous system of Drosophila: dissection of a courtship pathway by genetic mosaics. Genetics 92:437-457
70. Hotta Y, Benzer S (1976) Courtship in Drosophila mosaics: sex-specific foci for sequential action patterns. Proc Natl Acad Sci USA 73:4154-4158
71. Saito H, Kubota M, Roberts RW, Chi Q, Matsunami H (2004) RTP family members induce functional expression of mammalian odorant receptors. Cell 119:679-691
72. Wetzel CH, Behrendt HJ, Gisselmann G, Stortkuhl KF, Hovemann B, Hatt H (2001) From the cover: functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system. Proc Natl Acad Sci USA 98:9377-9380
73. Tanimura T, Shimada I (1981) Multiple receptor proteins for sweet taste in Drosophila discriminated by papain treatment. J Comp Physiol 141:265-269
74. Koseki T, Koganezawa M, Furuyama A, Isono K, Shimada I (2004) A specific receptor site for glycerol, a new sweet tastant for Drosophila: structure-taste relationship of glycerol in the labellar sugar receptor cell. Chem Senses 29:703-711
75. Ferveur JF (2005) Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35:279-295
76. Coyne JA, Oyama R (1995) Localization of pheromonal sexual dimorphism in Drosophila melanogaster and its effect on sexual isolation. Proc Natl Acad Sci USA 92:9505-9509
77. Savarit F, Sureau G, Cobb M, Ferveur JF (1999) Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation in Drosophila. Proc Natl Acad Sci USA 96:9015-9020
78. Wong SK (2003) G protein selectivity is regulated by multiple intracellular regions of GPCRs. NeuroSignals 12:1-12
79. Neves SR, Ram PT, Iyengar R (2002) G protein pathways. Science 296:1636-1639
80. Nobles M, Benians A, Tinker A (2005) Heterotrimeric G proteins precouple with G protein-coupled receptors in living cells. Proc Natl Acad Sci USA 102:18706-18711
81. Lee YH, Naider F, Becker JM (2006) Interacting residues in an activated state of a G protein-coupled receptor. J Biol Chem 281:2263-2272
82. Kang H, Lee WK, Choi YH, Vukoti KM, Bang WG, Yu YG (2005) Molecular analysis of the interaction between the intracellular loops of the human serotonin receptor type 6 (5-HT6) and the alpha subunit of GS protein. Biochem Biophys Res Commun 329:684-692
83. Elefsinioti AL, Bagos PG, Spyropoulos IC, Hamodrakas SJ (2004) A database for G proteins and their interaction with GPCRs. BMC Bioinformatics 5:208
84. Striem BJ, Pace U, Zehavi U, Naim M, Lancet D (1989) Sweet tastants stimulate adenylate cyclase coupled to GTP-binding protein in rat tongue membranes. Biochem J 260:121-126
85. Naim M, Ronen T, Striem BJ, Levinson M, Zehavi U (1991) Adenylate cyclase responses to sucrose stimulation in membranes of pig circumvallate taste papillae. Comp Biochem Physiol B 100:455-458
86. Trubey KR, Culpepper S, Maruyama Y, Kinnamon SC, Chaudhari N (2006) Tastants evoke cAMP signal in taste buds that is independent of calcium signaling. Am J Physiol Cell Physiol 291:C237-C244
87. Wong GT, Gannon KS, Margolskee RF (1996) Transduction of bitter and sweet taste by gustducin. Nature 381:796-800
88. Huang L, Shanker YG, Dubauskaite J, Zheng JZ, Yan W, Rosenzweig S, Spielman AI, Max M, Margolskee RF (1999) Gγ13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium. Nat Neurosci 2:1055-1062
89. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Gabor GL, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J et al (2000) The genome sequence of Drosophila melanogaster. Science 287:2185-2195
90. Ishimoto H, Takahashi K, Ueda R, Tanimura T (2005) G-protein gamma subunit 1 is required for sugar reception in Drosophila. EMBO J 24:3259-3265
91. Ueno K, Kohatsu S, Clay C, Forte M, Isono K, Kidokoro Y (2006) Gsalpha is involved in sugar perception in Drosophila melanogaster. J Neurosci 26:6143-6152
92. Talluri S, Bhatt A, Smith DP (1995) Identification of a Drosophila G protein α subunit (dGqα-3) expressed in chemosensory cells and central neurons. Proc Natl Acad Sci USA 92:11475-11479
93. Asano-Miyoshi M, Abe K, Emori Y (2000) Co-expression of calcium signaling components in vertebrate taste bud cells. Neurosci Lett 283:61-64
94. Miyoshi MA, Abe K, Emori Y (2001) IP(3) receptor type 3 and PLCâ2 are co-expressed with taste receptors T1R and T2R in rat taste bud cells. Chem Senses 26:259-265
95. Perez CA, Huang L, Rong M, Kozak JA, Preuss AK, Zhang H, Max M, Margolskee RF (2002) A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5:1169-1176
96. Rossler P, Kroner C, Freitag J, Noe J, Breer H (1998) Identification of a phospholipase C beta subtype in rat taste cells. Eur J Cell Biol 77:253-261
97. Riesgo-Escovar J, Raha D, Carlson JR (1995) Requirement for a phospholipase C in odor response: overlap between olfaction and vision in Drosophila. Proc Natl Acad Sci USA 92:2864-2868
98. Usui-Aoki K, Matsumoto K, Koganezawa M, Kohatsu S, Isono K, Matsubayashi H, Yamamoto MT, Ueda R, Takahashi K, Saigo K, Mikoshiba K, Yamamoto D (2005) Targeted expression of Ip3 sponge and Ip3 dsRNA impaires sugar taste sensation in Drosophila. J Neurogenet 19:123-141
99. Voets T, Talavera K, Owsianik G, Nilius B (2005) Sensing with TRP channels. Nat Chem Biol 1:85-92
100. Al-Anzi B, Tracey WD Jr, Benzer S (2006) Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANKTM1. Curr Biol 16:1034-1040
101. Getting P (1971) The sensory control of motor output in fly proboscis extension. Z Vgl Physiol 74:103-120
102. Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535-1547
103. Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548-1553
104. Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, Scott K (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49:285-295
105. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824