Drosophila Fatty Acid Taste Signals through the PLC Pathway in Sugar-Sensing Neurons

PLoS Genetics

Volumn 9, Issue 9, 2013, Pages

  Masek, Pavel ^a   Keene, Alex C ^a  

^a UNIVERSITY OF NEVADA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; PHOSPHOLIPASE C; SUGAR;

ARTICLE; CHEMOSENSITIZATION; CONTROLLED STUDY; DROSOPHILA; GENE; GENE EXPRESSION; GENE MUTATION; GENETIC CONSERVATION; GUSTATORY SYSTEM; NONHUMAN; NORPA GENE; OLFACTORY NERVE; SIGNAL TRANSDUCTION; SWEETNESS; TASTE; TASTE BUD;

ANIMALS; CARBOHYDRATES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FATTY ACIDS; NEURONS; PHOSPHOLIPASE C BETA; SIGNAL TRANSDUCTION; TASTE BUDS; TASTE PERCEPTION;

EID: 84884693719     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003710     Document Type: Article

References (79)

1. Scott K, (2005) Taste recognition: food for thought. Neuron 48: 455-464.
2. Yarmolinsky Da, Zuker CS, Ryba NJP, (2009) Common sense about taste: from mammals to insects. Cell 139: 234-244.
3. Montell C, (2009) A taste of the Drosophila gustatory receptors. Current opinion in neurobiology 19: 345-353.
4. Fujita M, Tanimura T, (2011) Drosophila Evaluates and Learns the Nutritional Value of Sugars. Current Biology 21: 751-755.
5. Burke CJ, Waddell S, (2011) Report Remembering Nutrient Quality of Sugar in Drosophila. Current Biology 21: 746-750.
6. Dus M, Min S, Keene AC, Young G, Suh GSB, (2011) Taste-independent detection of the caloric content of sugar in Drosophila. Direct pp. 2-7.
7. Stafford JW, Lynd KM, Jung AY, Gordon MD, (2012) Integration of taste and calorie sensing in Drosophila. J Neurosci 32: 14767-14774.
8. Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, et al. (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49: 285-295.
9. Amrein H, Thorne N, (2005) Gustatory Perception and Behavior in Drosophila melanogaster. Current 15: 673-684.
10. Wang Z, Singhvi A, Kong P, Scott K, (2004) Taste representations in the Drosophila brain. Cell 117: 981-991.
11. Thorne N, Chromey C, Bray S, Amrein H, Building C, et al. (2004) Taste Perception and Coding in Drosophila. Current 14: 1065-1079.
12. Tepper BJ, Nurse RJ, (1997) Fat perception is related to PROP taster status. Physiol Behav 61: 949-954.
13. Ramirez I, (1994) Chemosensory similarities among oils: does viscosity play a role? Chem Senses 19: 155-168.
14. Kinney NE, Antill RW, (1996) Role of olfaction in the formation of preference for high-fat foods in mice. Physiol Behav 59: 475-478.
15. Greenberg D, Smith GP, (1996) The controls of fat intake. Psychosom Med 58: 559-569.
16. Takeda M, Sawano S, Imaizumi M, Fushiki T, (2001) Preference for corn oil in olfactory-blocked mice in the conditioned place preference test and the two-bottle choice test. Life Sci 69: 847-854.
17. Fukuwatari T, Shibata K, Iguchi K, Saeki T, Iwata A, et al. (2003) Role of gustation in the recognition of oleate and triolein in anosmic rats. Physiol Behav 78: 579-583.
18. Hiraoka T, Fukuwatari T, Imaizumi M, Fushiki T, (2003) Effects of oral stimulation with fats on the cephalic phase of pancreatic enzyme secretion in esophagostomized rats. Physiol Behav 79: 713-717.
19. Kawai T, Fushiki T, (2003) Importance of lipolysis in oral cavity for orosensory detection of fat. Am J Physiol Regul Integr Comp Physiol 285: R447-454.
20. Laugerette F, Passilly-Degrace P, Patris B, Niot I, Febbraio M, et al. (2005) CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J Clin Invest 115: 3177-3184.
21. Chale-Rush A, Burgess JR, Mattes RD, (2007) Multiple routes of chemosensitivity to free fatty acids in humans. Am J Physiol Gastrointest Liver Physiol 292: G1206-1212.
22. Cartoni C, Yasumatsu K, Ohkuri T, Shigemura N, Yoshida R, et al. (2010) Taste preference for fatty acids is mediated by GPR40 and GPR120. J Neurosci 30: 8376-8382.
23. Smith JC (2010) Orosensory Factors in Fat Detection. In: Montmayeur JP, le Coutre J, editors. Fat Detection: Taste, Texture, and Post Ingestive Effects. Boca Raton (FL).
24. Harada E, Haba D, Aigaki T, Matsuo T, (2008) Behavioral analyses of mutants for two odorant-binding protein genes, Obp57d and Obp57e, in Drosophila melanogaster. Genes Genet Syst 83: 257-264.
25. Thorne N, Amrein H, (2008) Atypical Expression of Drosophila Gustatory Receptor Genes in Sensory. Receptor 568: 548-568.
26. Marella S, Mann K, Scott K, (2012) Dopaminergic modulation of sucrose acceptance behavior in Drosophila. Neuron 73: 941-950.
27. Shiraiwa T, Carlson JR, (2007) Proboscis extension response (PER) assay in Drosophila. J Vis Exp pp. 193.
28. Keene AC, Masek P, (2012) Optogenetic induction of aversive taste memory. Neuroscience 222: 173-180.
29. Awasaki T, Kimura K, (1997) pox-neuro is required for development of chemosensory bristles in Drosophila. J Neurobiol 32: 707-721.
30. Masek P, Scott K, (2010) Limited taste discrimination in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 107: 14833-14838.
31. Clyne PJ, Warr CG, Carlson JR, (2000) Candidate taste receptors in Drosophila. Science 287: 1830-1834.
32. Robertson HM, Warr CG, Carlson JR, (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci U S A 100 Suppl 2: 14537-14542.
33. Gerber B, Stocker RF, Tanimura T, Thum AS (2008) Smelling, Tasting, Learning: Drosophila as a Study Case. 1-47.
34. Shiraiwa T, (2008) Multimodal chemosensory integration through the maxillary palp in Drosophila. PloS one 3: e2191.
35. Charro MJ, Alcorta E, (1994) Quantifying relative importance of maxillary palp information on the olfactory behavior of Drosophila melanogaster. J Comp Physiol A 175: 761-766.
36. Ai M, Min S, Grosjean Y, Leblanc C, Bell R, et al. (2010) Acid sensing by the Drosophila olfactory system. Nature 468: 691-695.
37. Slone J, Daniels J, Amrein H, (2007) Sugar receptors in Drosophila. Curr Biol 17: 1809-1816.
38. Jiao Y, Moon SJ, Wang X, Ren Q, Montell C, (2008) Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr Biol 18: 1797-1801.
39. Baines RA, Uhler JP, Thompson A, Sweeney ST, Bate M, (2001) Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci 21: 1523-1531.
40. Thum AS, Knapek S, Rister J, Dierichs-schmitt EVA, Heisenberg M, et al. (2006) Differential Potencies of Effector Genes in Adult Drosophila. Time 203: 194-203.
41. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL, (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765-1768.
42. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, et al. (2003) Coding of Sweet, Bitter, and Umami Tastes: Different Receptor Cells Sharing Similar Signaling Pathways. Receptor 112: 293-301.
43. 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.
44. Yoshida Y, Saitoh K, Aihara Y, Okada S, Misaka T, et al. (2007) Transient receptor potential channel M5 and phospholipaseC-beta2 colocalizing in zebrafish taste receptor cells. Neuroreport 18: 1517-1520.
45. Hardie RC, Martin F, Chyb S, Raghu P, (2003) Rescue of light responses in the Drosophila "null" phospholipase C mutant, norpAP24, by the diacylglycerol kinase mutant, rdgA, and by metabolic inhibition. J Biol Chem 278: 18851-18858.
46. Chyb S, Raghu P, Hardie RC, (1999) Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL. Nature 397: 255-259.
47. Motter AL, Ahern GP, (2012) TRPA1 is a polyunsaturated fatty acid sensor in mammals. PLoS One 7: e38439.
48. Kim SH, Lee Y, Akitake B, Woodward OM, Guggino WB, et al. (2010) Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons. Proc Natl Acad Sci U S A 107: 8440-8445.
49. Kang K, Panzano VC, Chang EC, Ni L, Dainis AM, et al. (2012) Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481: 76-80.
50. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, et al. (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454: 217-220.
51. Wisotsky Z, Medina A, Freeman E, Dahanukar A, (2011) Evolutionary differences in food preference rely on Gr64e, a receptor for glycerol. Nature neuroscience 14: 1534-1541.
52. Fougeron A-s, Farine J-p, Flaven-pouchon J, Everaerts C (2011) Fatty-Acid Preference Changes during Development in Drosophila melanogaster. October 6.
53. Bosch OJ, Geier M, Boeckh J, (2000) Contribution of fatty acids to olfactory host finding of female Aedes aegypti. Chem Senses 25: 323-330.
54. Matsuo T, Sugaya S, Yasukawa J, Aigaki T, Fuyama Y, (2007) Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 5: e118.
55. Joseph RM, Devineni AV, King IFG, Heberlein U, (2009) Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 106: 11352-11357.
56. Gilbertson TA, Liu L, Kim I, Burks CA, Hansen DR, (2005) Fatty acid responses in taste cells from obesity-prone and-resistant rats. Physiol Behav 86: 681-690.
57. Pittman DW, Labban CE, Anderson AA, O'Connor HE, (2006) Linoleic and oleic acids alter the licking responses to sweet, salt, sour, and bitter tastants in rats. Chem Senses 31: 835-843.
58. Mattes RD (2010) Fat Taste in Humans: Is It a Primary? In: Montmayeur JP, le Coutre J, editors. Fat Detection: Taste, Texture, and Post Ingestive Effects. Boca Raton (FL).
59. Tucker RM, Mattes RD, (2012) Are free fatty acids effective taste stimuli in humans? Presented at the symposium "The Taste for Fat: New Discoveries on the Role of Fat in Sensory Perception, Metabolism, Sensory Pleasure and Beyond" held at the iNstitute of Food Technologists 2011 Annual Meeting, New Orleans, LA, June 12, 2011. J Food Sci 77: S148-151.
60. Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, et al. (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49: 285-295.
61. Liu L, Leonard AS, Motto DG, Feller MA, Price MP, et al. (2003) Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron 39: 133-146.
62. Fischler W, Kong P, Marella S, Scott K, (2007) The detection of carbonation by the Drosophila gustatory system. Nature 448: 1054-1057.
63. Cameron P, Hiroi M, Ngai J, Scott K, (2010) The molecular basis for water taste in Drosophila. Nature 465: 91-95.
64. Wisotsky Z, Medina A, Freeman E, Dahanukar A, (2011) Evolutionary differences in food preference rely on Gr64e, a receptor for glycerol. Nat Neurosci 14: 1534-1541.
65. Stocker RF, (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275: 3-26.
66. Ikeya T, Galic M, Belawat P, Nairz K, 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.
67. Bloomquist BT, Shortridge RD, Schneuwly S, Perdew M, Montell C, et al. (1988) Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 54: 723-733.
68. Kim S, McKay RR, Miller K, Shortridge RD, (1995) Multiple subtypes of phospholipase C are encoded by the norpA gene of Drosophila melanogaster. J Biol Chem 270: 14376-14382.
69. Yan W, Sunavala G, Rosenzweig S, Dasso M, Brand JG, et al. (2001) Bitter taste transduced by PLC-beta(2)-dependent rise in IP(3) and alpha-gustducin-dependent fall in cyclic nucleotides. Am J Physiol Cell Physiol 280: C742-751.
70. Hardie RC, (2007) TRP channels and lipids: from Drosophila to mammalian physiology. J Physiol 578: 9-24.
71. 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.
72. Perez CA, Huang L, Rong M, Kozak JA, Preuss AK, et al. (2002) A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5: 1169-1176.
73. Sclafani A, Ackroff K, Abumrad NA, (2007) CD36 gene deletion reduces fat preference and intake but not post-oral fat conditioning in mice. Am J Physiol Regul Integr Comp Physiol 293: R1823-1832.
74. Benton R, Vannice KS, Vosshall LB, (2007) An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450: 289-293.
75. Nagoshi E, Sugino K, Kula E, Okazaki E, Tachibana T, et al. (2010) Dissecting differential gene expression within the circadian neuronal circuit of Drosophila. Nat Neurosci 13: 60-68.
76. Dahanukar A, Lei Y-t, Kwon JY, Carlson JR, (2007) Article Two Gr Genes Underlie Sugar Reception in Drosophila. Neuron pp. 503-516.
77. Ni JQ, Markstein M, Binari R, Pfeiffer B, Liu LP, et al. (2008) Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster. Nat Methods 5: 49-51.
78. Chabaud MA, Devaud JM, Pham-Delegue MH, Preat T, Kaiser L, (2006) Olfactory conditioning of proboscis activity in Drosophila melanogaster. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192: 1335-1348.
79. Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, et al. (2007) Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci U S A 104: 8253-8256.