The neuronal and molecular basis of quinine-dependent bitter taste signaling in Drosophila larvae

Frontiers in Behavioral Neuroscience

Volumn 8, Issue JAN, 2014, Pages

  Apostolopoulou, Anthi A ^a   Mazija, Lorena ^a   Wüst, Alexander ^a   Thum, Andreas S ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Bitter; Drosophila larvae; Feeding; Gustation; Gustatory receptors; Learning and memory; Single cell

Indexed keywords

QUININE;

ANIMAL EXPERIMENT; ARTICLE; BITTER TASTE; CONTROLLED STUDY; DECISION MAKING; DROSOPHILA; FEEDING BEHAVIOR; GENE EXPRESSION; GR33A GENE; GR66A GENE; GR97A GENE; INFORMATION PROCESSING; LARVA; NONHUMAN; OLFACTORY MEMORY; RECEPTOR GENE; SENSORY NERVE CELL; SENSORY RECEPTOR; SIGNAL TRANSDUCTION; STATE DEPENDENT LEARNING; SURVIVAL FACTOR;

EID: 84893182541     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00006     Document Type: Article

References (64)

1. 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. doi: 10.1016/j.cub.2006.04.002
2. Ayestaran, A., Giurfa, M., and De Brito Sanchez, M. G. (2010). Toxic but drank: gustatory aversive compounds induce post-ingestional malaise in harnessed honeybees. PLoS ONE5:e15000. doi: 10.1371/journal.pone.0015000
3. Bader, R., Colomb, J., Pankratz, B., Schrock, A., Stocker, R. F., and Pankratz, M. J. (2007). Genetic dissection of neural circuit anatomy underlying feeding behavior in Drosophila: distinct classes of hugin-expressing neurons. J. Comp. Neurol. 502, 848-856. doi: 10.1002/cne.21342
4. Benton, R., Vannice, K. S., Gomez-Diaz, C., and Vosshall, L. B. (2009). Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136, 149-162. doi: 10.1016/j.cell.2008.12.001
5. Brand, A. H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
6. Burke, C. J., and Waddell, S. (2011). Remembering nutrient quality of sugar in Drosophila. Curr. Biol. 21, 746-750. doi: 10.1016/j.cub.2011.03.032
7. Cameron, P., Hiroi, M., Ngai, J., and Scott, K. (2010). The molecular basis for water taste in Drosophila. Nature 465, 91-95. doi: 10.1038/nature09011
8. Chyb, S., Dahanukar, A., Wickens, A., and Carlson, J. R. (2003). Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc. Natl. Acad. Sci. U.S.A. 100(Suppl. 2), 14526-14530. doi: 10.1073/pnas.2135339100
9. Cobb, M., Scott, K., and Pankratz, M. (2009). Gustation in Drosophila melanogaster. SEB Exp. Biol. Ser. 63, 1-38. doi: 10.1007/400_2008_9
10. Colomb, J., Grillenzoni, N., Ramaekers, A., and Stocker, R. F. (2007). Architecture of the primary taste center of Drosophila melanogaster larvae. J. Comp. Neurol. 502, 834-847. doi: 10.1002/cne.21312
11. 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. doi: 10.1016/j.neuron.2007.10.024
12. Dus, M., Ai, M., and Suh, G. S. (2013). Taste-independent nutrient selection is mediated by a brain-specific Na+/solute co-transporter in Drosophila. Nat. Neurosci. 16, 526-528. doi: 10.1038/nn.3372
13. Ebbs, M. L., and Amrein, H. (2007). Taste and pheromone perception in the fruit flyDrosophila melanogaster. Pflugers Arch. 454, 735-747. doi: 10.1007/s00424-007-0246-y
14. El-Keredy, A., Schleyer, M., Konig, C., Ekim, A., and Gerber, B. (2012). Behavioural analyses of quinine processing in choice, feeding and learning of larval Drosophila. PLoS ONE7:e40525. doi: 10.1371/journal.pone.0040525
15. Fishilevich, E., Domingos, A. I., Asahina, K., Naef, F., Vosshall, L. B., and Louis, M. (2005). Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr. Biol. 15, 2086-2096. doi: 10.1016/j.cub.2005.11.016
16. Gendre, N., Luer, K., Friche, S., Grillenzoni, N., Ramaekers, A., Technau, G. M., et al. (2004). Integration of complex larval chemosensory organs into the adult nervous system of Drosophila. Development 131, 83-92. doi: 10.1242/dev.00879
17. Gerber, B., and Stocker, R. F. (2007). The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chem. Senses 32, 65-89. doi: 10.1093/chemse/bjl030
18. Glendinning, J. I., Davis, A., and Rai, M. (2006). Temporal coding mediates discrimination of "bitter" taste stimuli by an insect. J. Neurosci. 26, 8900-8908. doi: 10.1523/JNEUROSCI.2351-06.2006
19. 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.
20. Gruber, F., Knapek, S., Fujita, M., Matsuo, K., Bracker, L., Shinzato, N., et al. (2013). Suppression of conditioned odor approach by feeding is independent of taste and nutritional value in Drosophila. Curr. Biol. 23, 507-514. doi: 10.1016/j.cub.2013.02.010
21. Heimbeck, G., Bugnon, V., Gendre, N., Keller, A., and Stocker, R. F. (2001). A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 98, 15336-15341. doi: 10.1073/pnas.011314898
22. Hendel, T., Michels, B., Neuser, K., Schipanski, A., Kaun, K., Sokolowski, M. B., et al. (2005). The carrot, not the stick: appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191, 265-279. doi: 10.1007/s00359-004-0574-8
23. Hwang, R. Y., Zhong, L., Xu, Y., Johnson, T., Zhang, F., Deisseroth, K., et al. (2007). Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr. Biol. 17, 2105-2116. doi: 10.1016/j.cub.2007.11.029
24. Inoshita, T., and Tanimura, T. (2006). Cellular identification of water gustatory receptor neurons and their central projection pattern in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 103, 1094-1099. doi: 10.1073/pnas.0502376103
25. Keene, A. C., Mazzoni, E. O., Zhen, J., Younger, M. A., Yamaguchi, S., Blau, J., et al. (2011). Distinct visual pathways mediate Drosophila larval light avoidance and circadian clock entrainment. J. Neurosci. 31, 6527-6534. doi: 10.1523/JNEUROSCI.6165-10.2011
26. Kreher, S. A., Kwon, J. Y., and Carlson, J. R. (2005). The molecular basis of odor coding in the Drosophila larva. Neuron 46, 445-456. doi: 10.1016/j.neuron.2005.04.007
27. Kurada, P., and White, K. (1998). Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95, 319-329. doi: 10.1016/S0092-8674(00)81764-X
28. Kwon, J. Y., Dahanukar, A., Weiss, L. A., and Carlson, J. R. (2011). Molecular and cellular organization of the taste system in the Drosophila larva. J. Neurosci. 31, 15300-15309. doi: 10.1523/JNEUROSCI.3363-11.2011
29. Larsson, M. C., Domingos, A. I., Jones, W. D., Chiappe, M. E., Amrein, H., and Vosshall, L. B. (2004). Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703-714. doi: 10.1016/j.neuron.2004.08.019
30. Lee, Y., Moon, S. J., and Montell, C. (2009). Multiple gustatory receptors required for the caffeine response in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 106, 4495-4500. doi: 10.1073/pnas.0811744106
31. Liu, L., Leonard, A. S., Motto, D. G., Feller, M. A., Price, M. P., Johnson, W. A., et al. (2003). Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron 39, 133-146. doi: 10.1016/S0896-6273(03)00394-5
32. Louis, M., Huber, T., Benton, R., Sakmar, T. P., and Vosshall, L. B. (2008). Bilateral olfactory sensory input enhances chemotaxis behavior. Nat. Neurosci. 11, 187-199. doi: 10.1038/nn2031
33. Marella, S., Fischler, W., Kong, P., Asgarian, S., Rueckert, E., and Scott, K. (2006). Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49, 285-295. doi: 10.1016/j.neuron.2005.11.037
34. Masek, P., and Scott, K. (2010). Limited taste discrimination in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 107, 14833-14838. doi: 10.1073/pnas.1009318107
35. Masuda-Nakagawa, L. M., Gendre, N., O'Kane, C. J., and Stocker, R. F. (2009). Localized olfactory representation in mushroom bodies of Drosophila larvae. Proc. Natl. Acad. Sci. U.S.A. 106, 10314-10319. doi: 10.1073/pnas.0900178106
36. Mishra, D., Miyamoto, T., Rezenom, Y. H., Broussard, A., Yavuz, A., Slone, J., et al. (2013). The molecular basis of sugar sensing in Drosophila larvae. Curr. Biol. 23, 15. doi: 10.1016/j.cub.2013.06.028
37. Miyakawa, Y. (1982). Behavioral evidence for the existence of sugar, salt and amino acid taste receptor cells and some of their properties in Drosophila larvae. J. Insect Physiol. 28, 405-410. doi: 10.1016/0022-1910(82)90066-X
38. Miyamoto, T., Slone, J., Song, X., and Amrein, H. (2012). A fructose receptor functions as a nutrient sensor in the Drosophila brain. Cell 151, 1113-1125. doi: 10.1016/j.cell.2012.10.024
39. Moon, S. J., Kottgen, M., Jiao, Y., Xu, H., and Montell, C. (2006). A taste receptor required for the caffeine response in vivo. Curr. Biol. 16, 1812-1817. doi: 10.1016/j.cub.2006.07.024
40. 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. doi: 10.1016/j.cub.2009.07.061
41. Oppliger, F. Y., Guerin, P. M., and Vlimant, M. (2000). Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae. J. Insect Physiol. 46, 135-144. doi: 10.1016/S0022-1910(99)00109-2
42. Pauls, D., Selcho, M., Gendre, N., Stocker, R. F., and Thum, A. S. (2010). Drosophila larvae establish appetitive olfactory memories via mushroom body neurons of embryonic origin. J. Neurosci. 30, 10655-10666. doi: 10.1523/JNEUROSCI.1281-10.2010
43. 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. Comp. Neurol. 445, 374-387. doi: 10.1002/cne.10188
44. Ramaekers, A., Magnenat, E., Marin, E. C., Gendre, N., Jefferis, G. S., Luo, L., et al. (2005). Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr. Biol. 15, 982-992. doi: 10.1016/j.cub.2005.04.032
45. Rohwedder, A., Pfitzenmaier, J. E., Ramsperger, N., Apostolopoulou, A. A., Widmann, A., and Thum, A. S. (2012). Nutritional value-dependent and nutritional value-independent effects onDrosophila melanogaster larval behavior. Chem. Senses 37, 711-721. doi: 10.1093/chemse/bjs055
46. Schleyer, M., Saumweber, T., Nahrendorf, W., Fischer, B., Von Alpen, D., Pauls, D., et al. (2011). A behavior-based circuit model of how outcome expectations organize learned behavior in larval Drosophila. Learn. Mem. 18, 639-653. doi: 10.1101/lm.2163411
47. Scott, K., Brady, R. Jr., Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C., et al. (2001). A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661-673. doi: 10.1016/S0092-8674(01)00263-X
48. Scragg, A. H., and Allan, E. J. (1987). The potential of plant cell culture for the production of quinine. Acta Leiden. 55, 45-51.
49. Selcho, M., Pauls, D., El Jundi, B., Stocker, R. F., and Thum, A. S. (2012). The role of octopamine and tyramine in Drosophila larval locomotion. J. Comp. Neurol. 520, 3764-3785. doi: 10.1002/cne.23152
50. Selcho, M., Pauls, D., Han, K. A., Stocker, R. F., and Thum, A. S. (2009). The role of dopamine in Drosophila larval classical olfactory conditioning. PLoS ONE 4:e5897. doi: 10.1371/journal.pone.0005897
51. Singh, R. N., and Singh, K. (1984). Fine structure of the sensory organs of Drosophila melanogaster Meigen larva (Diptera: Drosophilidae). Int. J. Insect. Morphol. Embryol. 13, 255-273. doi: 10.1016/0020-7322(84)90001-1
52. Thorne, N., Chromey, C., Bray, S., and Amrein, H. (2004). Taste perception and coding in Drosophila. Curr. Biol. 14, 1065-1079. doi: 10.1016/j.cub.2004.05.019
53. Thum, A. S., Leisibach, B., Gendre, N., Selcho, M., and Stocker, R. F. (2011). Diversity, variability, and suboesophageal connectivity of antennal lobe neurons in D. melanogaster larvae. J. Comp. Neurol. 519, 3415-3432. doi: 10.1002/cne.22713
54. Tissot, M., and Stocker, R. F. (2000). Metamorphosis in drosophila and other insects: the fate of neurons throughout the stages. Prog. Neurobiol. 62, 89-111. doi: 10.1016/S0301-0082(99)00069-6
55. Vosshall, L. B., and Stocker, R. F. (2007). Molecular architecture of smell and taste in Drosophila. Annu. Rev. Neurosci. 30, 505-533. doi: 10.1146/annurev.neuro.30.051606.094306
56. Wang, Z., Singhvi, A., Kong, P., and Scott, K. (2004). Taste representations in the Drosophila brain. Cell 117, 981-991. doi: 10.1016/j.cell.2004.06.011
57. Weiss, L. A., Dahanukar, A., Kwon, J. Y., Banerjee, D., and Carlson, J. R. (2011). The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258-272. doi: 10.1016/j.neuron.2011.01.001
58. Wernsdorfer, W. H. (1987). Quinine in health care in the tropics. Acta Leiden. 55, 197-208.
59. White, K., Tahaoglu, E., and Steller, H. (1996). Cell killing by the Drosophila gene reaper. Science 271, 805-807. doi: 10.1126/science.271.5250.805
60. White, N. J. (1987). The pharmacokinetics of quinine and quinidine in malaria. Acta Leiden. 55, 65-76.
61. Wu, Q., Zhao, Z., and Shen, P. (2005). Regulation of aversion to noxious food by Drosophila neuropeptide Y-and insulin-like systems. Nat. Neurosci. 8, 1350-1355. doi: 10.1038/nn1540
62. Xiang, Y., Yuan, Q., Vogt, N., Looger, L. L., Jan, L. Y., and Jan, Y. N. (2010). Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468, 921-926. doi: 10.1038/nature09576
63. Zhang, Y. V., Ni, J., and Montell, C. (2013). The molecular basis for attractive salt-taste coding in Drosophila. Science 340, 1334-1338. doi: 10.1126/science.1234133
64. Zhong, L., Hwang, R. Y., and Tracey, W. D. (2010). Pickpocket is a DEG/ENaC protein required for mechanical nociception in Drosophila larvae. Curr. Biol. 20, 429-434. doi: 10.1016/j.cub.2009.12.057