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

English version České info

Taste is the primary sensory system for detecting food quality and palatability. Drosophila detects five distinct taste modalities that include sweet, bitter, salt, water, and the taste of carbonation. Of these, sweet-sensing neurons appear to have utility for the detection of nutritionally rich food while bitter-sensing neurons signal toxicity and confer repulsion. Growing evidence in mammals suggests that taste for fatty acids (FAs) signals the presence of dietary lipids and promotes feeding. While flies appear to be attracted to fatty acids, the neural basis for fatty acid detection and attraction are unclear. Here, we demonstrate that a range of FAs are detected by the fly gustatory system and elicit a robust feeding response. Flies lacking olfactory organs respond robustly to FAs, confirming that FA attraction is mediated through the gustatory system. Furthermore, flies detect FAs independent of pH, suggesting the molecular basis for FA taste is not due to acidity. We show that low and medium concentrations of FAs serve as an appetitive signal and they are detected exclusively through the same subset of neurons that sense appetitive sweet substances, including most sugars. In mammals, taste perception of sweet and bitter substances is dependent on phospholipase C (PLC) signaling in specialized taste buds. We find that flies mutant for norpA, a Drosophila ortholog of PLC, fail to respond to FAs. Intriguingly, norpA mutants respond normally to other tastants, including sucrose and yeast. The defect of norpA mutants can be rescued by selectively restoring norpA expression in sweet-sensing neurons, corroborating that FAs signal through sweet-sensing neurons, and suggesting PLC signaling in the gustatory system is specifically involved in FA taste. Taken together, these findings reveal that PLC function in Drosophila sweet-sensing neurons is a conserved molecular signaling pathway that confers attraction to fatty acids.

Vyšlo v časopise: Fatty Acid Taste Signals through the PLC Pathway in Sugar-Sensing Neurons. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003710
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003710

Souhrn

Zdroje

1. ScottK (2005) Taste recognition: food for thought. Neuron 48 : 455–464.

2. YarmolinskyDa, ZukerCS, RybaNJP (2009) Common sense about taste: from mammals to insects. Cell 139 : 234–244.

3. MontellC (2009) A taste of the Drosophila gustatory receptors. Current opinion in neurobiology 19 : 345–353.

4. FujitaM, TanimuraT (2011) Drosophila Evaluates and Learns the Nutritional Value of Sugars. Current Biology 21 : 751–755.

5. BurkeCJ, WaddellS (2011) Report Remembering Nutrient Quality of Sugar in Drosophila. Current Biology 21 : 746–750.

6. DusM, MinS, KeeneAC, YoungG, SuhGSB (2011) Taste-independent detection of the caloric content of sugar in Drosophila. Direct 2–7.

7. StaffordJW, LyndKM, JungAY, GordonMD (2012) Integration of taste and calorie sensing in Drosophila. J Neurosci 32 : 14767–14774.

8. MarellaS, FischlerW, KongP, AsgarianS, RueckertE, et al. (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49 : 285–295.

9. AmreinH, ThorneN (2005) Gustatory Perception and Behavior in Drosophila melanogaster. Current 15 : 673–684.

10. WangZ, SinghviA, KongP, ScottK (2004) Taste representations in the Drosophila brain. Cell 117 : 981–991.

11. ThorneN, ChromeyC, BrayS, AmreinH, BuildingC, et al. (2004) Taste Perception and Coding in Drosophila. Current 14 : 1065–1079.

12. TepperBJ, NurseRJ (1997) Fat perception is related to PROP taster status. Physiol Behav 61 : 949–954.

13. RamirezI (1994) Chemosensory similarities among oils: does viscosity play a role? Chem Senses 19 : 155–168.

14. KinneyNE, AntillRW (1996) Role of olfaction in the formation of preference for high-fat foods in mice. Physiol Behav 59 : 475–478.

15. GreenbergD, SmithGP (1996) The controls of fat intake. Psychosom Med 58 : 559–569.

16. TakedaM, SawanoS, ImaizumiM, FushikiT (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. FukuwatariT, ShibataK, IguchiK, SaekiT, IwataA, et al. (2003) Role of gustation in the recognition of oleate and triolein in anosmic rats. Physiol Behav 78 : 579–583.

18. HiraokaT, FukuwatariT, ImaizumiM, FushikiT (2003) Effects of oral stimulation with fats on the cephalic phase of pancreatic enzyme secretion in esophagostomized rats. Physiol Behav 79 : 713–717.

19. KawaiT, FushikiT (2003) Importance of lipolysis in oral cavity for orosensory detection of fat. Am J Physiol Regul Integr Comp Physiol 285: R447–454.

20. LaugeretteF, Passilly-DegraceP, PatrisB, NiotI, FebbraioM, 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-RushA, BurgessJR, MattesRD (2007) Multiple routes of chemosensitivity to free fatty acids in humans. Am J Physiol Gastrointest Liver Physiol 292: G1206–1212.

22. CartoniC, YasumatsuK, OhkuriT, ShigemuraN, YoshidaR, 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. HaradaE, HabaD, AigakiT, MatsuoT (2008) Behavioral analyses of mutants for two odorant-binding protein genes, Obp57d and Obp57e, in Drosophila melanogaster. Genes Genet Syst 83 : 257–264.

25. ThorneN, AmreinH (2008) Atypical Expression of Drosophila Gustatory Receptor Genes in Sensory. Receptor 568 : 548–568.

26. MarellaS, MannK, ScottK (2012) Dopaminergic modulation of sucrose acceptance behavior in Drosophila. Neuron 73 : 941–950.

27. ShiraiwaT, CarlsonJR (2007) Proboscis extension response (PER) assay in Drosophila. J Vis Exp 193.

28. KeeneAC, MasekP (2012) Optogenetic induction of aversive taste memory. Neuroscience 222 : 173–180.

29. AwasakiT, KimuraK (1997) pox-neuro is required for development of chemosensory bristles in Drosophila. J Neurobiol 32 : 707–721.

30. MasekP, ScottK (2010) Limited taste discrimination in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 107 : 14833–14838.

31. ClynePJ, WarrCG, CarlsonJR (2000) Candidate taste receptors in Drosophila. Science 287 : 1830–1834.

32. RobertsonHM, WarrCG, CarlsonJR (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. ShiraiwaT (2008) Multimodal chemosensory integration through the maxillary palp in Drosophila. PloS one 3: e2191.

35. CharroMJ, AlcortaE (1994) Quantifying relative importance of maxillary palp information on the olfactory behavior of Drosophila melanogaster. J Comp Physiol A 175 : 761–766.

36. AiM, MinS, GrosjeanY, LeblancC, BellR, et al. (2010) Acid sensing by the Drosophila olfactory system. Nature 468 : 691–695.

37. SloneJ, DanielsJ, AmreinH (2007) Sugar receptors in Drosophila. Curr Biol 17 : 1809–1816.

38. JiaoY, MoonSJ, WangX, RenQ, MontellC (2008) Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr Biol 18 : 1797–1801.

39. BainesRA, UhlerJP, ThompsonA, SweeneyST, BateM (2001) Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci 21 : 1523–1531.

40. ThumAS, KnapekS, RisterJ, Dierichs-schmittEVA, HeisenbergM, et al. (2006) Differential Potencies of Effector Genes in Adult Drosophila. Time 203 : 194–203.

41. McGuireSE, LePT, OsbornAJ, MatsumotoK, DavisRL (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302 : 1765–1768.

42. ZhangY, HoonMA, ChandrashekarJ, MuellerKL, CookB, et al. (2003) Coding of Sweet , Bitter , and Umami Tastes : Different Receptor Cells Sharing Similar Signaling Pathways. Receptor 112 : 293–301.

43. RosslerP, KronerC, FreitagJ, NoeJ, BreerH (1998) Identification of a phospholipase C beta subtype in rat taste cells. Eur J Cell Biol 77 : 253–261.

44. YoshidaY, SaitohK, AiharaY, OkadaS, MisakaT, et al. (2007) Transient receptor potential channel M5 and phospholipaseC-beta2 colocalizing in zebrafish taste receptor cells. Neuroreport 18 : 1517–1520.

45. HardieRC, MartinF, ChybS, RaghuP (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. ChybS, RaghuP, HardieRC (1999) Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL. Nature 397 : 255–259.

47. MotterAL, AhernGP (2012) TRPA1 is a polyunsaturated fatty acid sensor in mammals. PLoS One 7: e38439.

48. KimSH, LeeY, AkitakeB, WoodwardOM, GugginoWB, et al. (2010) Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons. Proc Natl Acad Sci U S A 107 : 8440–8445.

49. KangK, PanzanoVC, ChangEC, NiL, DainisAM, et al. (2012) Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481 : 76–80.

50. HamadaFN, RosenzweigM, KangK, PulverSR, GhezziA, et al. (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454 : 217–220.

51. WisotskyZ, MedinaA, FreemanE, DahanukarA (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. BoschOJ, GeierM, BoeckhJ (2000) Contribution of fatty acids to olfactory host finding of female Aedes aegypti. Chem Senses 25 : 323–330.

54. MatsuoT, SugayaS, YasukawaJ, AigakiT, FuyamaY (2007) Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 5: e118.

55. JosephRM, DevineniAV, KingIFG, HeberleinU (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. GilbertsonTA, LiuL, KimI, BurksCA, HansenDR (2005) Fatty acid responses in taste cells from obesity-prone and -resistant rats. Physiol Behav 86 : 681–690.

57. PittmanDW, LabbanCE, AndersonAA, O'ConnorHE (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. TuckerRM, MattesRD (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. MarellaS, FischlerW, KongP, AsgarianS, RueckertE, et al. (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49 : 285–295.

61. LiuL, LeonardAS, MottoDG, FellerMA, PriceMP, et al. (2003) Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron 39 : 133–146.

62. FischlerW, KongP, MarellaS, ScottK (2007) The detection of carbonation by the Drosophila gustatory system. Nature 448 : 1054–1057.

63. CameronP, HiroiM, NgaiJ, ScottK (2010) The molecular basis for water taste in Drosophila. Nature 465 : 91–95.

64. WisotskyZ, MedinaA, FreemanE, DahanukarA (2011) Evolutionary differences in food preference rely on Gr64e, a receptor for glycerol. Nat Neurosci 14 : 1534–1541.

65. StockerRF (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275 : 3–26.

66. IkeyaT, GalicM, BelawatP, NairzK, HafenE (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. BloomquistBT, ShortridgeRD, SchneuwlyS, PerdewM, MontellC, et al. (1988) Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 54 : 723–733.

68. KimS, McKayRR, MillerK, ShortridgeRD (1995) Multiple subtypes of phospholipase C are encoded by the norpA gene of Drosophila melanogaster. J Biol Chem 270 : 14376–14382.

69. YanW, SunavalaG, RosenzweigS, DassoM, BrandJG, 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. HardieRC (2007) TRP channels and lipids: from Drosophila to mammalian physiology. J Physiol 578 : 9–24.

71. Al-AnziB, TraceyWDJr, BenzerS (2006) Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANKTM1. Curr Biol 16 : 1034–1040.

72. PerezCA, HuangL, RongM, KozakJA, PreussAK, et al. (2002) A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5 : 1169–1176.

73. SclafaniA, AckroffK, AbumradNA (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. BentonR, VanniceKS, VosshallLB (2007) An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450 : 289–293.

75. NagoshiE, SuginoK, KulaE, OkazakiE, TachibanaT, et al. (2010) Dissecting differential gene expression within the circadian neuronal circuit of Drosophila. Nat Neurosci 13 : 60–68.

76. DahanukarA, LeiY-t, KwonJY, CarlsonJR (2007) Article Two Gr Genes Underlie Sugar Reception in Drosophila. Neuron 503–516.

77. NiJQ, MarksteinM, BinariR, PfeifferB, LiuLP, et al. (2008) Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster. Nat Methods 5 : 49–51.

78. ChabaudMA, DevaudJM, Pham-DelegueMH, PreatT, KaiserL (2006) Olfactory conditioning of proboscis activity in Drosophila melanogaster. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192 : 1335–1348.

79. JaWW, CarvalhoGB, MakEM, de la RosaNN, FangAY, et al. (2007) Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci U S A 104 : 8253–8256.