Drosophila Pheromone-Sensing Neurons Expressing the ppk25 Ion Channel Subunit Stimulate Male Courtship and Female Receptivity

PLoS Genetics

Volumn 10, Issue 3, 2014, Pages

  Vijayan, Vinoy ^a   Thistle, Rob ^b   Liu, Tong ^a,c   Starostina, Elena ^a   Pikielny, Claudio W ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

7 PENTACOSENE; HYDROCARBON; PHEROMONE; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; PPK25 PROTEIN, DROSOPHILA; SODIUM CHANNEL;

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ARTICLE; BEHAVIOR CONTROL; CELL SPECIFICITY; CELL SUBPOPULATION; CONTROLLED STUDY; COURTSHIP; DROSOPHILA; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE MUTATION; GENE SILENCING; GUSTATORY NERVOUS SYSTEM; GUSTATORY NEURON; HEARING; HORMONAL REGULATION; HORMONE SENSITIVITY; MALE; MATING; NERVE CELL; NONHUMAN; PPK23 GENE; PPK25 GENE; SMELLING; ANIMAL; BIOSYNTHESIS; GENETICS; METABOLISM; MUTATION; SEXUAL BEHAVIOR;

ANIMALS; COURTSHIP; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION; MALE; MUTATION; NEURONS; PHEROMONES; SEXUAL BEHAVIOR, ANIMAL; SODIUM CHANNELS;

EID: 84897439483     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004238     Document Type: Article

References (58)

1. Butenandt A, Beckmann R, Stamm D, Hecker E, (1959) Concerning the sexual attractant of the silkmoth Bombyx mori. Purification and composition Z Naturforschg 14b: 283-284.
2. Dickson BJ, (2008) Wired for sex: the neurobiology of Drosophila mating decisions. Science 322: 904-909.
3. Villella A, Hall JC, (2008) Neurogenetics of courtship and mating in Drosophila. Adv Genet 62: 67-184.
4. Wicker-Thomas C, (2007) Pheromonal communication involved in courtship behavior in Diptera. J Insect Physiol 53: 1089-1100.
5. Yew J, Cody R, Kravitz E, (2008) Cuticular hydrocarbon analysis of an awake behaving fly using direct analysis in real-time time-of-flight mass spectrometry. Proc Natl Acad Sci USA 105 (20) (): 7135-40.
6. Vosshall L, (2008) Scent of a Fly. Neuron 59: 685-689.
7. Wang L, Han X, Mehren J, Hiroi M, Billeter J-C, et al. (2011) Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat Neurosci 14 (6) (): 757-62.
8. Grosjean Y, Rytz R, Farine J-P, Abuin L, Cortot J, et al. (2011) An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478: 236-240.
9. Krstic D, Boll W, Noll M, (2009) Sensory integration regulating male courtship behavior in Drosophila. PLoS ONE 4: e4457.
10. Starostina E, Liu T, Vijayan V, Zheng Z, Siwicki KK, et al. (2012) A Drosophila DEG/ENaC Subunit Functions Specifically in Gustatory Neurons Required for Male Courtship Behavior. J Neurosci 32: 4665-4674.
11. Liu T, Starostina E, Vijayan V, Pikielny CW, (2012) Two Drosophila DEG/ENaC channel subunits have distinct functions in gustatory neurons that activate male courtship. J Neurosci 32: 11879-11889.
12. 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.
13. 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.
14. Toda H, Zhao X, Dickson BJ, (2012) The Drosophila Female Aphrodisiac Pheromone Activates ppk23+ Sensory Neurons to Elicit Male Courtship Behavior. Cell Reports pp. 1-9.
15. Manoli DS, Fan P, Fraser EJ, Shah NM, (2013) Neural control of sexually dimorphic behaviors. Current Opinion in Neurobiology 23: 330-338.
16. 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 USA 102: 12831-12836.
17. Pikielny CW, (2012) Sexy DEG/ENaC channels involved in gustatory detection of fruit fly pheromones. Sci Signal 5: pe48.
18. Tompkins L, Hall JC, Hall LM, (1980) Courtship-stimulating volatile compounds from normal and mutant Drosophila. J Insect Physiol 26: 689-697.
19. Sureau G, Ferveur JF, (1999) Co-adaptation of pheromone production and behavioural responses in Drosophila melanogaster males. Genet Res 74: 129-137.
20. Tian L, Hires S, Mao T, Huber D, Chiappe M, et al. (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Meth 6 (12) (): 875-81.
21. Billeter J-C, Atallah J, Krupp JJ, Millar JG, Levine JD, (2009) Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461: 987-991.
22. 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.
23. Siwicki KK, Riccio P, Ladewski L, Marcillac F, Dartevelle L, Cross SA, Ferveur JF, (2005) The role of cuticular pheromones in courtship conditioning of Drosophila males. Learn Mem 12: 636-645.
24. Antony C, Davis T, Carlson D, Pechine J, Jallon J, (1985) Compared behavioral responses of maleDrosophila melanogaster (Canton S) to natural and synthetic aphrodisiacs. Journal of chemical ecology 11: 1617-1629.
25. Grillet M, Dartevelle L, Ferveur J-F, (2006) A Drosophila male pheromone affects female sexual receptivity. Proc Biol Sci 273: 315-323.
26. Kurtovic A, Widmer A, Dickson BJ, (2007) A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446: 542-546.
27. Ronderos DS, Smith DP, (2010) Activation of the T1 neuronal circuit is necessary and sufficient to induce sexually dimorphic mating behavior in Drosophila melanogaster. J Neurosci 30: 2595-2599.
28. Gailey DA, Lacaillade RC, Hall JC, (1986) Chemosensory elements of courtship in normal and mutant, olfaction-deficient Drosophila melanogaster. Behav Genet 16: 375-405.
29. Schilcher F, Manning A, (1975) Courtship song and mating speed in hybrids betweenDrosophila melanogaster and Drosophila simulans. Behav Genet 5 (4) (): 395-404.
30. Talyn BC, Dowse HB, (2004) The role of courtship song in sexual selection and species recognition by female Drosophila melanogaster. Animal Behaviour 68: 1165-1180.
31. Göpfert MC, Robert D, (2001) Biomechanics. Turning the key on Drosophila audition. Nature 411: 908.
32. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG, (2000) The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103: 805-813.
33. Fergestad T, Sale H, Bostwick B, Schaffer A, Ho L, et al. (2010) A Drosophila behavioral mutant, down and out (dao), is defective in an essential regulator of Erg potassium channels. Proc Natl Acad Sci USA 107: 5617-5621.
34. Possidente DR, Murphey RK, (1989) Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Developmental Biology 132: 448-457.
35. Sweeney ST, Broadie K, Keane J, Niemann H, O'Kane CJ, (1995) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14: 341-351.
36. Hallem EA, Ho MG, Carlson JR, (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117: 965-979.
37. Kitamoto T, (2001) Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47: 81-92.
38. Mathew D, Martelli C, Kelley-Swift E, Brusalis C, Gershow M, et al. (2013) Functional diversity among sensory receptors in a Drosophila olfactory circuit. Proc Natl Acad Sci USA 110: E2134-E2143.
39. Ha TS, Smith DP, (2006) A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J Neurosci 26: 8727-8733.
40. van der Goes van Naters W, Carlson JR, (2007) Receptors and neurons for fly odors in Drosophila. Curr Biol 17: 606-612.
41. Liu W, Liang X, Gong J, Yang Z, Zhang Y-H, et al. (2011) Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat Neurosci 14: 896-902.
42. Su C-Y, Menuz K, Reisert J, Carlson JR, (2012) Non-synaptic inhibition between grouped neurons in an olfactory circuit. Nature 492: 66-71.
43. Miyamoto T, Amrein H, (2008) Suppression of male courtship by a Drosophila pheromone receptor. Nat Neurosci 11: 874-876.
44. Fan P, Manoli DS, Ahmed OM, Chen Y, Agarwal N, et al. (2013) Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell 154: 89-102.
45. Lacaille F, Hiroi M, Twele R, Inoshita T, Umemoto D, et al. (2007) An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS ONE 2: e661.
46. Lacaille F, Everaerts C, Ferveur J-F, (2009) Feminization and alteration of Drosophila taste neurons induce reciprocal effects on male avoidance behavior. Behav Genet 39: 554-563.
47. Ferveur J-F, (2010) Drosophila female courtship and mating behaviors: sensory signals, genes, neural structures and evolution. Current Opinion in Neurobiology 20: 764-769.
48. Robertson H, (1983) Chemical stimuli eliciting courtship by males inDrosophila melanogaster. Cellular and Molecular Life Sciences 39: 333-335.
49. Bro-Jørgensen J, (2010) Dynamics of multiple signalling systems: animal communication in a world in flux. Trends Ecol Evol (Amst) 25: 292-300.
50. Dahanukar A, Ray A, (2011) Courtship, aggression and avoidance: pheromones, receptors and neurons for social behaviors in Drosophila. Fly 5: 58-63.
51. Haga S, Hattori T, Sato T, Sato K, Matsuda S, et al. (2010) The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor. Nature 466: 118-122.
52. Sakurai T, Mitsuno H, Haupt SS, Uchino K, Yokohari F, et al. (2011) A Single Sex Pheromone Receptor Determines Chemical Response Specificity of Sexual Behavior in the Silkmoth Bombyx mori. PLoS Genet 7: e1002115.
53. Ben-Shahar Y (2011) Sensory Functions for Degenerin/Epithelial Sodium Channels (DEG/ENaC). Advances in Genetics. Advances in Genetics. Elsevier, Vol. 76. pp. 1-26.
54. Eastwood AL, Goodman MB, (2012) Insight into DEG/ENaC channel gating from genetics and structure. Physiology (Bethesda, Md) 27: 282-290.
55. Pfeiffer BD, Ngo T-TB, Hibbard KL, Murphy C, Jenett A, et al. (2010) Refinement of tools for targeted gene expression in Drosophila. Genetics 186: 735-755.
56. Hall JC, (1978) Courtship among males due to a male-sterile mutation in Drosophila melanogaster. Behav Genet 8: 125-141.
57. 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 USA 102: 16550-16557.
58. Benchabane H, Xin N, Tian A, Hafler BP, Nguyen K, et al. (2011) Jerky/Earthbound facilitates cell-specific Wnt/Wingless signalling by modulating β-catenin-TCF activity. EMBO J 30: 1444-1458.