The KRÜPPEL-Like Transcription Factor DATILÓGRAFO Is Required in Specific Cholinergic Neurons for Sexual Receptivity in Drosophila Females

PLoS Biology

Volumn 12, Issue 10, 2014, Pages

  Schinaman, Joseph Moeller ^a   Giesey, Rachel Lynn ^a   Mizutani, Claudia Mieko ^a   Lukacsovich, Tamas ^b   Sousa Neves, Rui ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR; TRANSCRIPTION FACTOR DATILOGRAFO; UNCLASSIFIED DRUG; DATILOGRAFO PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; TRANSCRIPTION FACTOR;

ADULT; ALLELE; ANIMAL TISSUE; ANTENNAL LOBE; ARTICLE; BRAIN REGION; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; COURTSHIP; DATI GENE; DROSOPHILA; FEMALE; GENE; GENE EXPRESSION; LOCOMOTION; MALE; MATING; MUSHROOM BODY; NONHUMAN; PHENOTYPE; POSTERIOR SUPERIOR LATERAL PROTOCEREBRUM; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEXUAL BEHAVIOR; SPINAL CORD; ANIMAL; BRAIN; CHROMOSOME MAP; DROSOPHILA MELANOGASTER; INSECT CHROMOSOME; METABOLISM; PHYSIOLOGY;

ANIMALS; BRAIN; CHOLINERGIC NEURONS; CHROMOSOME MAPPING; CHROMOSOMES, INSECT; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; LOCOMOTION; MALE; MUSHROOM BODIES; SEXUAL BEHAVIOR, ANIMAL; TRANSCRIPTION FACTORS;

EID: 84920399878     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001964     Document Type: Article

References (78)

1. Villella A, Hall JC (2008) Neurogenetics of courtship and mating in Drosophila. In: Hall J, Dunlap J, Friedmann T, van Heyningen V, editors. Advances in genetics. Oxford, UK: Academic Press, Vol. 62: . pp. 67–184.
2. Hall JC, (1979) Control of male reproductive behavior by the central nervous system of drosophila: dissection of a courtship pathway by genetic mosaics. Genetics 92: 437–457.
3. Sakai T, Kitamoto T, (2006) Differential roles of two major brain structures, mushroom bodies and central complex, for Drosophila male courtship behavior. J Neurobiol 66: 821–834 doi:10.1002/neu.20262
4. Yu JY, Kanai MI, Demir E, Jefferis GSXE, Dickson BJ, (2010) Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 20: 1602–1614 doi:10.1016/j.cub.2010.08.025
5. Dauwalder B, (2011) The roles of fruitless and doublesex in the control of male courtship. Int Rev Neurobiol 99: 87–105 doi:10.1016/B978-0-12-387003-2.00004-5
6. Jean-François F, (2010) Drosophila female courtship and mating behaviors: sensory signals, genes, neural structures and evolution. Curr Opin Neurobiol 20: 764–769 doi:10.1016/j.conb.2010.09.007
7. Spieth HT, (1974) Courtship behavior in drosophila. Annu Rev Entomol 19: 385–405 doi:10.1146/annurev.en.19.010174.002125
8. Hall JC, (1994) The mating of a fly. Science 264: 1702–1714.
9. Yamamoto D, Jallon JM, Komatsu A, (1997) Genetic dissection of sexual behavior in Drosophila melanogaster. Annu Rev Entomol 42: 551–585.
10. Von Schilcher F, (1976) The function of pulse song and sine song in the courtship of Drosophila melanogaster. Anim Behav 24: 622–625 doi:10.1016/S0003-3472(76)80076-0
11. Sakai T, Isono K, Tomaru M, Fukatami A, Oguma Y, (2002) Light wavelength dependency of mating activity in the Drosophila melanogaster species subgroup. Genes Genet Syst 77: 187–195.
12. Talyn BC, Dowse HB, (2004) The role of courtship song in sexual selection and species recognition by female Drosophila melanogaster. Anim Behav 68: 1165–1180 doi:10.1016/j.anbehav.2003.11.023
13. Grillet M, Dartevelle L, Ferveur J-F, (2006) A Drosophila male pheromone affects female sexual receptivity. Proc Biol Sci 273: 315–323 doi:10.1098/rspb.2005.3332
14. Carhan A, Allen F, Armstrong JD, Hortsch M, Goodwin SF, et al. (2005) Female receptivity phenotype of icebox mutants caused by a mutation in the L1-type cell adhesion molecule neuroglian. Genes Brain Behav 4: 449–465 doi:10.1111/j.1601-183X.2004.00117.x
15. Juni N, Yamamoto D, (2009) Genetic analysis of chaste, a new mutation of Drosophila melanogaster characterized by extremely low female sexual receptivity. J Neurogenet 23: 329–340 doi:10.1080/01677060802471601
16. Suzuki K, Juni N, Yamamoto D, (1997) Enhanced mate refusal in female Drosophila induced by a mutation in the spinster locus. Appl Entomol Zool 32: 235–243.
17. Sakai T, Kasuya J, Kitamoto T, Aigaki T, (2009) The Drosophila TRPA channel, Painless, regulates sexual receptivity in virgin females. Genes Brain Behav 8: 546–557 doi:10.1111/j.1601-183X.2009.00503.x
18. Sakurai A, Koganezawa M, Yasuyama K-I, Emoto K, Yamamoto D, (2013) Select interneuron clusters determine female sexual receptivity in Drosophila. Nat Commun 4: 1825 doi:10.1038/ncomms2837
19. Tompkins L, Hall JC, (1983) Identification of brain sites controlling female receptivity in mosaics of Drosophila melanogaster. Genetics 103: 179–195.
20. Hochman B, Gloor H, Green MM, (1964) Analysis of chromosome 4 in Drosophila Melanogaster. I. Spontaneous and X-Ray-induced lethals. Genetica 35: 109–126.
21. Sousa-Neves R, (2000) The synthesis of a double fourth chromosome marker with y+. Dros Inf Serv 83: 8–10.
22. Sousa-Neves R, Lukacsovich T, Mizutani CM, Locke J, Podemski L, et al. (2005) High-resolution mapping of the Drosophila fourth chromosome using site-directed terminal deficiencies. Genetics 170: 127–138.
23. Sousa-Neves R, Schinaman JM, (2012) A novel genetic tool for clonal analysis of fourth chromosome mutations. Fly (Austin) 6: 49–56.
24. Drapeau M, Long A, (2000) The Copulatron, a multi-chamber apparatus for observing Drosophila courtship behaviors. Dros Inf Serv 83: 194–196.
25. Tompkins L, Hall JC, Hall LM, (1980) Courtship-stimulating volatile compounds from normal and mutant Drosophila. J Insect Physiol 26: 689–697 doi:10.1016/0022-1910(80)90042-6
26. Gargano JW, Martin I, Bhandari P, Grotewiel MS, (2005) Rapid iterative negative geotaxis (RING): a new method for assessing age-related locomotor decline in Drosophila. Exp Gerontol 40: 386–395 doi:10.1016/j.exger.2005.02.005
27. Sweeney ST, Hidalgo A, de Belle JS, Keshishian H, (2012) Antibody staining of the central nervous system in adult Drosophila. Cold Spring Harb Protoc 2012: 235–238 doi:10.1101/pdb.prot067397
28. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675 doi:10.1038/nmeth.2089
29. Bolte S, Cordelières FP, (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213–232 doi:10.1111/j.1365-2818.2006.01706.x
30. Preibisch S, Saalfeld S, Tomancak P, (2009) Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25: 1463–1465 doi:10.1093/bioinformatics/btp184
31. Tully T, Quinn WG, (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 157: 263–277.
32. Van Swinderen B, Hall JC, (1995) Analysis of conditioned courtship in dusky-Andante rhythm mutants of Drosophila. Learn Mem 2: 49–61.
33. Podemski L, Sousa-Neves R, Marsh JL, Locke J, (2004) Molecular mapping of deletion breakpoints on chromosome 4 of Drosophila melanogaster. Chromosoma 112: 381–388.
34. Sousa-Neves R, Mizutani CM, Lukacsovich T, Purcell J, Marsh JL, (2005) datilografo (dati) encodes a zinc finger transcription factor required for proper locomotor activity in Drosophila. 46th A Dros Res Conf 46 Suppl: 1044C.
35. Tsuji T, Hasegawa E, Isshiki T, (2008) Neuroblast entry into quiescence is regulated intrinsically by the combined action of spatial Hox proteins and temporal identity factors. Development 135: 3859–3869 doi:10.1242/dev.025189
36. Bastock M, (1956) A gene mutation which changes a behavior pattern. Evolution (N Y) 10: 421–439 doi:10.2307/2407002
37. Chu Y, Yang E, Schinaman JM, Chahda JS, Sousa-Neves R, (2013) Genetic analysis of mate discrimination in Drosophila simulans. Evolution 67: 2335–2347 doi:10.1111/evo.12115
38. Manning A, (1967) The control of sexual receptivity in female Drosophila. Anim Behav 15: 239–250.
39. Berger C, Renner S, Lüer K, Technau GM, (2007) The commonly used marker ELAV is transiently expressed in neuroblasts and glial cells in the Drosophila embryonic CNS. Dev Dyn 236: 3562–3568 doi:10.1002/dvdy.21372
40. Dierick HA, Greenspan RJ, (2007) Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat Genet 39: 678–682 doi:10.1038/ng2029
41. Bicker G, (1999) Introduction to neurotransmitter histochemistry of the insect brain. Microsc Res Tech 45: 63–64 doi:;10.1002/(SICI)1097-0029(19990415)45:2<63::AID-JEMT1>3.0.CO;2-5
42. Littleton JT, Ganetzky B, (2000) Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26: 35–43.
43. Budnik V, White K, (1987) Genetic dissection of dopamine and serotonin synthesis in the nervous system of Drosophila melanogaster. J Neurogenet 4: 309–314.
44. Daniels RW, Gelfand MV, Collins CA, DiAntonio A, (2008) Visualizing glutamatergic cell bodies and synapses in Drosophila larval and adult CNS. J Comp Neurol 508: 131–152 doi:10.1002/cne.21670
45. Waddell S, (2010) Dopamine reveals neural circuit mechanisms of fly memory. Trends Neurosci 33: 457–464 doi:10.1016/j.tins.2010.07.001
46. Watanabe TK, Anderson WW, (1976) Selection for geotaxis in Drosophila melanogaster: heritability, degree of dominance, and correlated responses to selection. Behav Genet 6: 71–86.
47. Balling A, Technau GM, Heisenberg M, (1987) Are the structural changes in adult Drosophila mushroom bodies memory traces? Studies on biochemical learning mutants. J Neurogenet 4: 65–73.
48. McBride SM, Giuliani G, Choi C, Krause P, Correale D, et al. (1999) Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 24: 967–977.
49. Ito K, Awasaki T, (2008) Clonal unit architecture of the adult fly brain. Adv Exp Med Biol 628: 137–158 doi:_10.1007/978-0-387-78261-4_9
50. Das A, Sen S, Lichtneckert R, Okada R, Ito K, et al. (2008) Drosophila olfactory local interneurons and projection neurons derive from a common neuroblast lineage specified by the empty spiracles gene. Neural Dev 3: 33 doi:10.1186/1749-8104-3-33
51. Hayashi S, Ito K, Sado Y, Taniguchi M, Akimoto A, et al. (2002) GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 34: 58–61 doi:10.1002/gene.10137
52. Tanaka NK, Awasaki T, Shimada T, Ito K, (2004) Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 14: 449–457 doi:10.1016/j.cub.2004.03.006
53. Masse NY, Turner GC, Jefferis GSXE, (2009) Olfactory information processing in Drosophila. Curr Biol 19: R700–R713.
54. Jefferis GSXE, Potter CJ, Chan AM, Marin EC, Rohlfing T, et al. (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128: 1187–1203 doi:10.1016/j.cell.2007.01.040
55. Ruta V, Datta SR, Vasconcelos ML, Freeland J, Looger LL, et al. (2010) A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468: 686–690 doi:10.1038/nature09554
56. Couto A, Alenius M, Dickson BJ, (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15: 1535–1547 doi:10.1016/j.cub.2005.07.034
57. Sachse S, Rueckert E, Keller A, Okada R, Tanaka NK, et al. (2007) Activity-dependent plasticity in an olfactory circuit. Neuron 56: 838–850 doi:10.1016/j.neuron.2007.10.035
58. Yu H-H, Kao C-F, He Y, Ding P, Kao J-C, et al. (2010) A complete developmental sequence of a Drosophila neuronal lineage as revealed by twin-spot MARCM. PLoS Biol 8 doi:10.1371/journal.pbio.1000461
59. Jefferis GS, Marin EC, Stocker RF, Luo L, (2001) Target neuron prespecification in the olfactory map of Drosophila. Nature 414: 204–208 doi:10.1038/35102574
60. Okada R, Awasaki T, Ito K, (2009) Gamma-aminobutyric acid (GABA)-mediated neural connections in the Drosophila antennal lobe. J Comp Neurol 514: 74–91 doi:10.1002/cne.21971
61. Parrish JZ, Emoto K, Kim MD, Jan YN, (2007) Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu Rev Neurosci 30: 399–423 doi:10.1146/annurev.neuro.29.051605.112907
62. Beskow A, Grimberg KB, Bott LC, Salomons FA, Dantuma NP, et al. (2009) A conserved unfoldase activity for the p97 AAA-ATPase in proteasomal degradation. J Mol Biol 394: 732–746 doi:10.1016/j.jmb.2009.09.050
63. Yen H-CS, Elledge SJ, (2008) Identification of SCF ubiquitin ligase substrates by global protein stability profiling. Science 322: 923–929 doi:10.1126/science.1160462
64. Martini A, La Starza R, Janssen H, Bilhou-Nabera C, Corveleyn A, et al. (2002) Recurrent rearrangement of the Ewing's sarcoma gene, EWSR1, or its homologue, TAF15, with the transcription factor CIZ/NMP4 in acute leukemia. Cancer Res 62: 5408–5412.
65. La Starza R, Aventin A, Crescenzi B, Gorello P, Specchia G, et al. (2005) CIZ gene rearrangements in acute leukemia: report of a diagnostic FISH assay and clinical features of nine patients. Leukemia 19: 1696–1699.
66. Braun A, Chen J, Waloszek D, Maas A, (2007) First early cambrian radiolaria. Geol Soc London, Spec Publ 286: 143–149 doi:10.1144/SP286.10
67. Roth RB, Hevezi P, Lee J, Willhite D, Lechner SM, et al. (2006) Gene expression analyses reveal molecular relationships among 20 regions of the human CNS. Neurogenetics 7: 67–80 doi:10.1007/s10048-006-0032-6
68. Lukk M, Kapushesky M, Nikkilä J, Parkinson H, Goncalves A, et al. (2010) A global map of human gene expression. Nat Biotechnol 28: 322–324 doi:10.1038/nbt0410-322
69. Nakamoto T, Shiratsuchi A, Oda H, Inoue K, Matsumura T, et al. (2004) Impaired spermatogenesis and male fertility defects in CIZ/Nmp4-disrupted mice. Genes Cells 9: 575–589 doi:10.1111/j.1356-9597.2004.00746.x
70. Gu H, O'Dowd DK, (2006) Cholinergic synaptic transmission in adult Drosophila Kenyon cells in situ. J Neurosci 26: 265–272 doi:10.1523/JNEUROSCI.4109-05.2006
71. Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenböck G, (2007) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128: 601–612 doi:10.1016/j.cell.2006.12.034
72. Olsen SR, Bhandawat V, Wilson RI, (2007) Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54: 89–103 doi:10.1016/j.neuron.2007.03.010
73. Silbering AF, Okada R, Ito K, Galizia CG, (2008) Olfactory information processing in the Drosophila antennal lobe: anything goes? J Neurosci 28: 13075–13087 doi:10.1523/JNEUROSCI.2973-08.2008
74. Huang J, Zhang W, Qiao W, Hu A, Wang Z, (2010) Functional connectivity and selective odor responses of excitatory local interneurons in Drosophila antennal lobe. Neuron 67: 1021–1033 doi:10.1016/j.neuron.2010.08.025
75. Parnas M, Lin AC, Huetteroth W, Miesenböck G, (2013) Odor discrimination in Drosophila: from neural population codes to behavior. Neuron 79: 932–944 doi:10.1016/j.neuron.2013.08.006
76. Bastock M, Manning A, (1955) The courtship of Drosophila melanogaster. Behaviour 8: 85–111.
77. Ewing AW, (1964) The influence of wing area on the courting behavior of Drosophila melanogaster. Anim Behav 12: 316–320.
78. Liang L, Li Y, Potter CJ, Yizhar O, Deisseroth K, et al. (2013) GABAergic projection neurons route selective olfactory inputs to specific higher-order neurons. Neuron 79: 917–931 doi:10.1016/j.neuron.2013.06.014