Mutants in phospholipid signaling attenuate the behavioral response of adult Drosophila to trehalose

Chemical Senses

Volumn 35, Issue 8, 2010, Pages 663-673

  Kain, Pinky ^a,d   Badsha, Farhath ^a   Hussain, Syed Mubarak ^a,d   Nair, Amit ^b,e   Hasan, Gaiti ^a   Rodrigues, Veronica ^a,c  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b BABRAHAM INSTITUTE   (United Kingdom)

^c TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e Oakland Innovation   (United Kingdom)

Author keywords

dgq; Plc21C; Proboscis; rdgA; Taste transduction; Wing margins

Indexed keywords

DIACYLGLYCEROL KINASE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; INOSITOL TRISPHOSPHATE; PHOSPHOLIPASE C BETA; PHOSPHOLIPID; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TREHALOSE;

ADULT ANIMAL; ANIMAL ANATOMY; ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; FEEDING BEHAVIOR; GENE EXPRESSION; GENE MUTATION; GENETIC ANALYSIS; HETEROZYGOSITY; NONHUMAN; PRIORITY JOURNAL; PROBOSCIS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TASTE BUD;

ANIMALS; BEHAVIOR, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HETEROZYGOTE; MALE; MUTATION; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TASTE; TREHALOSE; TRPC CATION CHANNELS;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 77957252026     PISSN: 0379864X     EISSN: 14643553     Source Type: Journal    
DOI: 10.1093/chemse/bjq055     Document Type: Article

References (66)

1. Agrawal N, Padmanabhan N, Hasan G. 2009. Inositol. 1:4,5-trisphosphate receptor function in Drosophila insulin producing cells. PLoS One. 4:e6652.
2. Al-Anzi B, Tracey WD, Benzer S Jr. 2006. Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANKTM1. Curr Biol. 16:1034-1040.
3. Amakawa T, Ozaki M, Kawata K. 1990. Effects of cyclic GMP on the sugar taste receptor cell of the fly Phormia regina. J Insect Physiol. 36:281-286.
4. Arora K, Rodrigues V, Joshi S, Siddiqi O. 1987. A gene affecting the specificity of chemosensory neurons of Drosopgila. Nature. 330:62-63.
5. Avenet P, Lindemann B. 1987. Patch-clamp study of isolated taste receptor cells of the frog. J Membr Biol. 97:223-240.
6. Banerjee S, Joshi R, Venkiteswaran G, Agrawal N, Srikanth S, Alam F, Hasan G. 2006. Compensation of inositol 1,4,5-trisphosphate receptor function by altering sarco-endoplasmic reticulum calcium ATPase activity in the Drosophila flight circuit. J Neurosci. 26:8278-8288.
7. 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.
8. Bloomquist BT, Shortridge RD, Schneuwly S, Perdew M, Montell C, Steller H, Rubin G, Pak WL. 1988. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell. 54:723-733.
9. Chyb S, Dahanukar A, Wickens A, Carlson JR. 2003. Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc Natl Acad Sci U S A. 2 (Suppl 100):14526-14530.
10. Clyne PJ, Warr CG, Carlson JR. 2000. Candidate taste receptors in Drosophila. Science. 287:1830-1834.
11. 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.
12. Dahanukar A, Lei YT, Kwon JY, Carlson JR. 2007. Two Gr genes underlie sugar reception in Drosophila. Neuron. 56:503-516.
13. Dethier VG. 1976. The hungry fly. Cambridge (MA): Harvard University Press.
14. Devary O, Heichal O, Blumenfeld A, Cassel D, Suss E, Barash S, Rubinstein CT, Minke B, Selinger Z. 1987. Coupling of photoexcited rhodopsin to inositol phospholipid hydrolysis in fly photoreceptors. Proc Natl Acad Sci U S A. 84:6939-6943.
15. 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.
16. Falk R, Bleiser-Avivi N, Atidia J. 1976. Labellar taste organs of Drosophila melanogaster. J Morphol. 150:327-341.
17. Hardie RC, Martin F, Cochrane GW, Juusola M, Georgiev P, Raghu P. 2002. Molecular basis of amplification in Drosophila phototransduction: roles for G protein, phospholipase C, and diacylglycerol kinase. Neuron. 36:689-701.
18. 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.
19. Hardie RC. 2003. Regulation of trp channels via lipid second messengers. Annu Rev Physiol. 65:735-759.
20. Hardie RC, Raghu P. 2001. Visual transduction in Drosophila. Nature. 413:186-193.
21. 2+ channel causes massive degeneration of photoreceptors. J Biol Chem. 277:33884-33889.
22. 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.
23. Huang L, Shanker YG, Dubauskaite J, Zheng JZ, Yan W, Rosenzweig S, Spielman AI, Max M, Margolskee RF. 1999. Ggamma13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium. Nat Neurosci. 2:1055-1062.
24. Inoue H, Yoshioka T, Hotta Y. 1989. Diacylglycerol kinase defect in a Drosophila retinal degeneration mutant rdgA. J Biol Chem. 264: 5996-6000.
25. 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.
26. Jiao Y, Moon SJ, Montell C. 2007. A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proc Natl Acad Sci U S A. 104:14110-14115.
27. Kain P, Chakraborty TS, Sundaram S, Siddiqi O, Rodrigues V, Hasan G. 2008. Reduced odor responses from antennal neurons of G(q)alpha, phospholipase Cbeta, and rdgA mutants in Drosophila support a role for a phospholipid intermediate in insect olfactory transduction. J Neurosci. 28:4745-4755.
28. Koganezawa M, Shimada I. 2002. Inositol 1,4,5-trisphosphate transduction cascade in taste reception of the fleshfly, Boettcherisca peregrina. J Neurobiol. 51:66-83.
29. Lee YJ, Dobbs MB, Verardi ML, Hyde DR. 1990. dgq: a Drosophila gene encoding a visual system-specific G alpha molecule. Neuron. 5: 889-898.
30. Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E. 2002. Human receptors for sweet and umami taste. Proc Natl Acad Sci U S A. 99: 4692-4696.
31. Masai I, Okazaki A, Hosoya T, Hotta Y. 1993. Drosophila retinal degeneration A gene encodes an eye-specific diacylglycerol kinase with cysteine-rich zinc-finger motifs and ankyrin repeats. Proc Natl Acad Sci U S A. 90:11157-11161.
32. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. 2003. Spatiotemporal rescue of memory dysfunction in Drosophila. Science. 302: 1765-1768.
33. McLaughlin SK, McKinnon PJ, Margolskee RF. 1992. Gustducin is a tastecell-specific G protein closely related to the transducins. Nature. 357: 563-569.
34. Miyoshi MA, Abe K, Emori Y. 2001. IP(3) receptor type 3 and PLCbeta2 are co-expressed with taste receptors T1R and T2R in rat taste bud cells. Chem Senses. 26:259-265.
35. Montell C, Jones K, Hafen E, Rubin G. 1985. Rescue of the Drosophila phototransduction mutation trp by germline transformation. Science. 230:1040-1043.
36. Montell C, Rubin GM. 1989. Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron. 2:1313-1323.
37. Murata Y, Mashiko M, Ozaki M, Amakawa T, Nakamura T. 2004. Intrinsic nitric oxide regulates the taste response of the sugar receptor cell in the blowfly, Phormia regina. Chem Senses. 29:75-81.
38. 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.
39. Nayak SV, Singh RN. 1983. Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster. Int J Insect Morphol Embryol. 12: 273-291.
40. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS. 2001. Mammalian sweet taste receptors. Cell. 106:381-390.
41. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS. 2002. An amino-acid taste receptor. Nature. 416:199-202.
42. Neves SR, Ram PT, Iyengar R. 2002. G protein pathways. Science. 296: 1636-1639.
43. Niemeyer BA, Suzuki E, Scott K, Jalink K, Zuker CS. 1996. The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell. 85:651-659.
44. Raghu P, Colley NJ, Webel R, James T, Hasan G, Danin M, Selinger Z, Hardie RC. 2000. Normal phototransduction in Drosophila photoreceptors lacking an InsP(3) receptor gene. Mol Cell Neurosci. 15: 429-445.
45. Reuss H, Mojet MH, Chyb S, Hardie RC. 1997. In vivo analysis of the drosophila light-sensitive channels, TRP and TRPL. Neuron. 19: 1249-1259.
46. 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. 2 (Suppl 100):14537-14542.
47. Rodrigues V, Siddiqi O. 1978. Genetic analysis of chemosensory pathway. Proc Ind Acad Sci. B87:147-160.
48. Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K. 2008. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature. 452:1002-1006.
49. Scott K, Becker A, Sun Y, Hardy R, Zuker C. 1995. Gq alpha protein function in vivo: genetic dissection of its role in photoreceptor cell physiology. Neuron. 15:919-927.
50. Scott K, Sun Y, Beckingham K, Zuker CS. 1997. Calmodulin regulation of Drosophila light-activated channels and receptor function mediates termination of the light response in vivo. Cell. 91:375-383.
51. 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.
52. Shortridge RD, Yoon J, Lending CR, Bloomquist BT, Perdew MH, Pak WL. 1991. A Drosophila phospholipase C gene that is expressed in the central nervous system. J Biol Chem. 266:12474-12480.
53. 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.
54. Talluri S, Bhatt A, Smith DP. 1995. Identification of a Drosophila G protein alpha subunit (dGq alpha-3) expressed in chemosensory cells and central neurons. Proc Natl Acad Sci U S A. 92:11475-11479.
55. 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.
56. 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.
57. 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.
58. Usui-Aoki K, Matsumoto K, Koganezawa M, Kohatsu S, Isono K, Matsubayashi H, Yamamoto M, T, Ueda R, Takahashi K, et al. 2005. Targeted expression of Ip3 sponge and Ip3 dsRNA impaires sugar taste sensation in Drosophila. J Neurogenet. 19:123-141.
59. Weinkove D, Neufeld TP, Twardzik T, Waterfield MD, Leevers SJ. 1999. Regulation of imaginal disc cell size, cell number and organ size by Drosophila class I(A) phosphoinositide 3-kinase and its adaptor. Curr Biol. 9:1019-1029.
60. Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS. 2008. Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature. 452: 1007-1011.
61. Wong GT, Gannon KS, Margolskee RF. 1996. Transduction of bitter and sweet taste by gustducin. Nature. 381:796-800.
62. Wong SK. 2003. G protein selectivity is regulated by multiple intracellular regions of GPCRs. Neurosignals. 12:1-12.
63. Xu XZ, Li HS, Guggino WB, Montell C. 1997. Coassembly of TRP and TRPL produces a distinct store-operated conductance. Cell. 89:1155-1164.
64. Xu XZ, Chien F, Butler A, Salkoff L, Montell C. 2000. TRPgamma, a Drosophila TRP-related subunit, forms a regulated cation channel with TRPL. Neuron. 26:647-657.
65. Yoon J, Ben-Ami HC, Hong YS, Park S, Strong LL, Bowman J, Geng C, Baek K, Minke B, Pak WL. 2000. Novel mechanism of massive photoreceptor degeneration caused by mutations in the trp gene of Drosophila. J Neurosci. 20:649-659.
66. 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.