Two drosophila DEG/ENAC channel subunits have distinct functions in gustatory neurons that activate male courtship

Journal of Neuroscience

Volumn 32, Issue 34, 2012, Pages 11879-11889

  Liu, Tong ^a   Starostina, Elena ^a   Vijayan, Vinoy ^a   Pikielny, Claudio W ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEG CHANNEL; ENAC CHANNEL; PHEROMONE; SODIUM CHANNEL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; COURTSHIP; DROSOPHILA; FEMALE; GENE; GENE EXPRESSION; GENE MUTATION; GENE SILENCING; GUSTATORY NERVOUS SYSTEM; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; NONHUMAN; NOPE GENE; NUCLEOTIDE SEQUENCE; PPK 25 GENE; PRIORITY JOURNAL; REPORTER GENE; SEQUENCE ALIGNMENT;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CHEMORECEPTOR CELLS; COURTSHIP; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GREEN FLUORESCENT PROTEINS; IMMUNOPRECIPITATION; MALE; MUTATION; PHEROMONES; PROTEIN SUBUNITS; RNA, MESSENGER; SENSE ORGANS; SODIUM CHANNELS; TRANSCRIPTION FACTORS; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES;

EID: 84865251370     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1376-12.2012     Document Type: Article

References (68)

1. Benchabane H, Xin N, Tian A, Hafler BP, Nguyen K, Ahmed A, Ahmed Y (2011) Jerky/Earthbound facilitates cell-specific Wnt/Wingless signalling by modulating beta-catenin-TCF activity. EMBO J 30:1444-1458.
2. Benton R (2007) Sensitivity and specificity in Drosophila pheromone perception. Trends Neurosci 30:512-519.
3. Bianchi L (2007) Mechanotransduction: touch and feel at the molecular level as modeled in Caenorhabditis elegans. Mol Neurobiol 36:254-271.
4. Billeter JC, Rideout EJ, Dornan AJ, Goodwin SF (2006) Control of male sexual behavior in Drosophila by the sex determination pathway. Curr Biol 16:R766-R776.
5. Bischof J, Maeda RK, Hediger M, Karch F, Basler K (2007) An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci U S A 104:3312-3317.
6. Boll W, Noll M (2002) The Drosophila Pox neuro gene: control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers. Development 129:5667-5681.
7. Brand AH, Dormand EL (1995) The GAL4 system as a tool for unravelling the mysteries of the Drosophila nervous system. Curr Opin Neurobiol 5:572-578.
8. Butterworth MB, Weisz OA, Johnson JP (2008) Some assembly required: putting the epithelial sodium channel together. J Biol Chem 283:35305-35309.
9. Cameron P, Hiroi M, Ngai J, Scott K (2010) The molecular basis for water taste in Drosophila. Nature 465:91-95.
10. Carattino MD (2011) Structural mechanisms underlying the function of epithelial sodium channel/acid-sensing ion channel. Curr Opin Nephrol Hypertens 20:555-560.
11. Chandrashekar J, Kuhn C, Oka Y, Yarmolinsky DA, Hummler E, Ryba NJ, Zuker CS (2010) The cells and peripheral representation of sodium taste in mice. Nature 464:297-301.
12. Chen Z, Wang Q, Wang Z (2010) The amiloride-sensitive epithelial Na channel PPK28 is essential for Drosophila gustatory water reception. J Neurosci 30:6247-6252.
13. Coscoy S, de Weille JR, Lingueglia E, Lazdunski M (1999) The pretransmembrane 1 domain of acid-sensing ion channels participates in the ion pore. J Biol Chem 274:10129-10132.
14. Dahanukar A, Ray A (2011) Courtship, aggression and avoidance: pheromones, receptors and neurons for social behaviors in Drosophila. Fly (Austin) 5:58-63.
15. Dauwalder B (2011) The roles of fruitless and doublesex in the control of male courtship. Int Rev Neurobiol 99:87-105.
16. Dickson BJ (2008) Wired for sex: the neurobiology of Drosophila mating decisions. Science 322:904-909.
17. Elliott DA, Brand AH (2008) The GAL4 system: a versatile system for the expression of genes. Methods Mol Biol 420:79-95.
18. Ferveur JF (2005) Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35:279-295.
19. Frank KD, Zimmerman WF (1969) Action spectra for phase-shifts of a circadian rhythm in Drosophila. Science 163:688-689.
20. Grosjean Y, Rytz R, Farine JP, Abuin L, Cortot J, Jefferis GS, Benton R (2011) An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478:236-240.
21. Gründer S, Firsov D, Chang SS, Jaeger NF, Gautschi I, Schild L, Lifton RP, Rossier BC (1997) A mutation causing pseudohypoaldosteronism type 1 identifies a conserved glycine that is involved in the gating of the epithelial sodium channel. EMBO J 16:899-907.
22. Gründer S, Jaeger NF, Gautschi I, Schild L, Rossier BC (1999) Identification of a highly conserved sequence at the N-terminus of the epithelial Na channel alpha subunit involved in gating. Pflugers Arch 438:709-715.
23. Hall JC (1978) Courtship among males due to a male-sterile mutation in Drosophila melanogaster. Behav Genet 8:125-141.
24. Hong K, Mano I, Driscoll M (2000) In vivo structure-function analyses of Caenorhabditis elegans MEC-4, a candidate mechanosensory ion channel subunit. J Neurosci 20:2575-2588.
25. Jasti J, Furukawa H, Gonzales EB, Gouaux E (2007) Structure of acidsensing ion channel 1 at 1.9 A resolution and low pH. Nature 449:316-323.
26. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5-W9.
27. Kashlan OB, Kleyman TR (2011) ENaC structure and function in the wake of a resolved structure of a family member. Am J Physiol Renal Physiol 301:F684-F696.
28. Kellenberger S, Schild L (2002) Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev 82:735-767.
29. Krstic D, Boll W, Noll M (2009) Sensory integration regulating male courtship behavior in Drosophila. PLoS One 4:e4457.
30. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF (1999) Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543-552.
31. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWil-liam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
32. Levine JD, Millar JG (2009) Chemical signalling: laser on the fly reveals a new male-specific pheromone. Curr Biol 19:R653-R655.
33. Lin H, Mann KJ, Starostina E, Kinser RD, Pikielny CW (2005) A Drosophila deg/ENaC channel subunit is required for male response to female pheromones. Proc Natl Acad Sci U S A 102:12831-12836.
34. Liu L, Leonard AS, Motto DG, Feller MA, Price MP, Johnson WA, Welsh MJ (2003) Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron 39:133-146.
35. Liu T, Dartevelle L, Yuan C, Wei H, Wang Y, Ferveur JF, Guo A (2008) Increased dopamine level enhances male-male courtship in Drosophila. J Neurosci 28:5539-5546.
36. Lu B, LaMora A, Sun Y, Welsh MJ, Ben-Shahar Y (2012) ppk23-dependent chemosensory functions contribute to courtship behavior in Drosophila melanogaster. PLoS Genet 8:e1002587.
37. Markstein M, Pitsouli C, Villalta C, Celniker SE, Perrimon N (2008) Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat Genet 40:476-483.
38. Mellert DJ, Knapp JM, Manoli DS, Meissner GW, Baker BS (2010) Midline crossing by gustatory receptor neuron axons is regulated by fruitless, doublesex and the Roundabout receptors. Development 137:323-332.
39. Meltzer RH, Kapoor N, Qadri YJ, Anderson SJ, Fuller CM, Benos DJ (2007) Heteromeric assembly of acid-sensitive ion channel and epithelial sodium channel subunits. J Biol Chem 282:25548-25559.
40. Meunier N, Ferveur JF, Marion-Poll F (2000) Sex-specific non-pheromonal taste receptors in Drosophila. Curr Biol 10:1583-1586.
41. Meunier N, Marion-Poll F, Rospars JP, Tanimura T (2003) Peripheral coding of bitter taste in Drosophila. J Neurobiol 56:139-152.
42. Miyamoto T, Amrein H (2008) Suppression of male courtship by a Drosophila pheromone receptor. Nat Neurosci 11:874-876.
43. Ni JQ, Liu LP, Binari R, Hardy R, Shim HS, Cavallaro A, Booker M, Pfeiffer BD, Markstein M, Wang H, Villalta C, Laverty TR, Perkins LA, Perrimon N (2009) A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics 182:1089-1100.
44. Possidente DR, Murphey RK (1989) Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Dev Biol 132:448-457.
45. Qadri YJ, Rooj AK, Fuller CM (2012) ENaCs and ASICs as therapeutic targets. Am J Physiol Cell Physiol 302:C943-C965.
46. Qian S, Capovilla M, Pirrotta V (1991) The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes. EMBO J 10:1415-1425.
47. Riggleman B, Wieschaus E, Schedl P (1989) Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene. Genes Dev 3:96-113.
48. Ronderos DS, Smith DP (2009) Diverse signaling mechanisms mediate volatile odorant detection in Drosophila. Fly (Austin) 3.
49. Root CM, Masuyama K, Green DS, Enell LE, Nässel DR, Lee CH, Wang JW (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59:311-321.
50. Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable elements. Science 218:348-353.
51. Salinas M, Lazdunski M, Lingueglia E (2009) Structural elements for the generation of sustained currents by the acid pain sensor ASIC3. J Biol Chem 284:31851-31859.
52. Sherwood TW, Lee KG, Gormley MG, Askwith CC (2011) Heteromeric acid-sensing ion channels (ASICs) composed of ASIC2b and ASIC1a display novel channel properties and contribute to acidosis-induced neuronal death. J Neurosci 31:9723-9734.
53. Siwicki KK, Kravitz EA (2009) Fruitless, doublesex and the genetics of social behavior in Drosophila melanogaster. Curr Opin Neurobiol 19:200-206.
54. Starostina E, Liu T, Vijayan V, Zheng Z, Siwicki KK, Pikielny CW (2012) A Drosophila DEG/ENaC subunit functions specifically in gustatory neurons required for male courtship behavior. J Neurosci 32:4665-4674.
55. Stockinger P, Kvitsiani D, Rotkopf S, Tirián L, Dickson BJ (2005) Neural circuitry that governs Drosophila male courtship behavior. Cell 121:795-807.
56. Stowers L, Logan DW (2010) Sexual dimorphism in olfactory signaling. Curr Opin Neurobiol 20:770-775.
57. Tavernarakis N, Driscoll M (2000) Caenorhabditis elegans degenerins and vertebrate ENaC ion channels contain an extracellular domain related to venom neurotoxins. J Neurogenet 13:257-264.
58. Tavernarakis N, Everett JK, Kyrpides NC, Driscoll M (2001) Structural and functional features of the intracellular amino terminus of DEG/ENaC ion channels. Curr Biol 11:R205-R208.
59. Thistle R, Cameron P, Ghorayshi A, Dennison L, Scott K (2012) Contact chemoreceptors mediate male-male repulsion and male-female attraction during Drosophila courtship. Cell 149:1140-1151.
60. Toda H, Zhao X, Dickson BJ (2012) The Drosophila female aphrodisiac pheromone activates ppk23 sensory neurons to elicit male courtship behavior. Cell Rep 1:599-607.
61. Tunstall NE, Warr CG (2012) Chemical communication in insects: the peripheral odour coding system of Drosophila melanogaster. Adv Exp Med Biol 739:59-77.
62. Villella A, Hall JC (2008) Neurogenetics of courtship and mating in Drosophila. Adv Genet 62:67-184.
63. Villella A, Ferri SL, Krystal JD, Hall JC (2005) Functional analysis of fruitless gene expression by transgenic manipulations of Drosophila courtship. Proc Natl Acad Sci U S A 102:16550-16557.
64. Voglis G, Tavernarakis N (2008) A synaptic DEG/ENaC ion channel mediates learning in C. elegans by facilitating dopamine signalling. EMBO J 27:3288-3299.
65. Vosshall LB (2008) Scent of a fly. Neuron 59:685-689.
66. Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505-533.
67. Wesch D, Althaus M, Miranda P, Cruz-Muros I, Fronius M, González- Hernández T, Clauss WG, Alvarez de la Rosa D, Giraldez T (2012) Differential N termini in epithelial Na channel delta-subunit isoforms modulate channel trafficking to the membrane. Am J Physiol Cell Physiol 302:C868-C879.
68. Wicker-Thomas C (2007) Pheromonal communication involved in courtship behavior in Diptera. J Insect Physiol 53:1089-1100.