Genome wide identification of Fruitless targets suggests a role in upregulating genes important for neural circuit formation

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Vernes, Sonja C ^a,b  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b MAX PLANCK INSTITUTE FOR PSYCHOLINGUISTICS   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; FRU PROTEIN, DROSOPHILA; ISOPROTEIN; NERVE PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ANIMAL; BINDING SITE; BRAIN; CHANNEL GATING; CHROMOSOME MAP; COURTSHIP; CYTOLOGY; DROSOPHILA MELANOGASTER; FEMALE; GENETICS; GENOME; INSECT CHROMOSOME; MALE; METABOLISM; MOLECULAR GENETICS; NERVE CELL; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TRANSCRIPTION INITIATION;

ANIMALS; BINDING SITES; BRAIN; CHROMOSOME MAPPING; CHROMOSOMES, INSECT; COURTSHIP; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENOME; ION CHANNEL GATING; MALE; MOLECULAR SEQUENCE ANNOTATION; NERVE NET; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; PROTEIN BINDING; PROTEIN ISOFORMS; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84897883229     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep04412     Document Type: Article

References (43)

1. Yamamoto, D. The neural and genetic substrates of sexual behavior in Drosophila. Adv Genet 59, 39-66, doi:10.1016/S0065-2660(07)59002-4 (2007).
2. Dauwalder, B. 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 (2011).
3. Villella, A. &Hall, J. C. Neurogenetics of courtship and mating in Drosophila. Adv Genet 62, 67-184, doi:10.1016/S0065-2660(08)00603-2 (2008).
4. Goldman, T. D. & Arbeitman, M. N. Genomic and functional studies of Drosophila sex hierarchy regulated gene expression in adult head and nervous system tissues. PLoS genetics 3, e216, doi:10.1371/journal.pgen.0030216 (2007).
5. Demir, E. & Dickson, B. J. fruitless splicing specifies male courtship behavior in Drosophila. Cell 121, 785-794, doi:10.1016/j.cell.2005.04. 027 (2005). (Pubitemid 40797600)
6. Anand, A. et al.Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158, 1569-1595 (2001). (Pubitemid 32783142)
7. Ito, H. et al. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci U S A 93, 9687-9692 (1996). (Pubitemid 26296670)
8. Manoli, D. S. et al. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436, 395-400, doi:10.1038/nature03859 (2005). (Pubitemid 41059049)
9. Stockinger, P.,Kvitsiani, D., Rotkopf, S., Tirian, L.&Dickson, B. J.Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795-807, doi:10.1016/ j.cell.2005.04.026 (2005). (Pubitemid 40797601)
10. Yu, J. Y., Kanai, M. I., Demir, E., Jefferis, G. S. & Dickson, B. J. Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 20, 1602-1614, doi:10.1016/j.cub.2010.08.025 (2010).
11. Kimura, K., Ote, M., Tazawa, T. & Yamamoto, D. Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature 438, 229-233, doi:10.1038/nature04229 (2005). (Pubitemid 41599875)
12. Goto, J., Mikawa, Y., Koganezawa, M., Ito, H. & Yamamoto, D. Sexually dimorphic shaping of interneuron dendrites involves the hunchback transcription factor. J Neurosci 31, 5454-5459, doi:10.1523/JNEUROSCI.4861- 10.2011 (2011).
13. Gailey, D. A., Taylor, B. J. & Hall, J. C. Elements of the fruitless locus regulate development of the muscle of Lawrence, amale-specific structure in the abdomen of Drosophila melanogaster adults. Development 113, 879-890 (1991). (Pubitemid 21900327)
14. Nojima, T., Kimura, K., Koganezawa, M. & Yamamoto, D. Neuronal synaptic outputs determine the sexual fate of postsynaptic targets. Curr Biol 20, 836-840, doi:10.1016/j.cub.2010.02.064 (2010).
15. Usui-Aoki, K. et al. Formation of themale-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol 2, 500-506, doi:10.1038/35019537 (2000).
16. Ryner, L. C. et al. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87, 1079-1089 (1996). (Pubitemid 26427991)
17. Goodwin, S. F. et al. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154, 725-745 (2000). (Pubitemid 30096594)
18. Lee, G. et al. Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J Neurobiol 43, 404-426 (2000). (Pubitemid 30409628)
19. Billeter, J. C. & Goodwin, S. F. Characterization of Drosophila fruitless-gal4 transgenes reveals expression in male-specific fruitless neurons and innervation of male reproductive structures. J Comp Neurol 475, 270-287, doi:10.1002/ cne.20177 (2004). (Pubitemid 38850024)
20. Lee, G., Villella, A., Taylor, B. J. & Hall, J. C. New reproductive anomalies in fruitless-mutant Drosophila males: extreme lengthening of mating durations and infertility correlated with defective serotonergic innervation of reproductive organs. J Neurobiol 47, 121-149, doi:10.1002/neu.1021 (2001).
21. Song, H. J. et al. The fruitless gene is required for the proper formation of axonal tracts in the embryonic central nervous system of Drosophila. Genetics 162, 1703-1724 (2002).
22. Billeter, J. C. et al. Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene. Curr Biol 16, 1063-1076, doi:10.1016/j.cub.2006.04.039 (2006).
23. Ito, H. et al. Fruitless recruits two antagonistic chromatin factors to establish single-neuron sexual dimorphism. Cell 149, 1327-1338, doi:10.1016/ j.cell.2012.04.025 (2012).
24. Ito, H., Sato, K. & Yamamoto, D. Sex-switching of the Drosophila brain by two antagonistic chromatin factors. Fly (Austin) 7, 87-91, doi:10.4161/fly.24018 (2013).
25. Dalton, J. E. et al. Male-specific fruitless isoforms have different regulatory roles conferred by distinct zinc finger DNA binding domains. BMC Genomics 14, 659, doi:10.1186/1471-2164-14-659 (2013).
26. Drapeau, M. D., Radovic, A., Wittkopp, P. J. & Long, A. D. A gene necessary for normal male courtship, yellow, acts downstream of fruitless in the Drosophila melanogaster larval brain. J Neurobiol 55, 53-72, doi:10.1002/neu.10196 (2003). (Pubitemid 36396962)
27. Dauwalder, B., Tsujimoto, S., Moss, J. &Mattox, W. The Drosophila takeout gene is regulated by the somatic sex-determination pathway and affects male courtship behavior. Genes Dev 16, 2879-2892, doi:10.1101/gad.1010302 (2002). (Pubitemid 35334737)
28. Neville, M. C. et al. Male-specific fruitless isoforms target neurodevelopmental genes to specify a sexually dimorphic nervous system. Curr Biol 24, 229-241, doi:10.1016/j.cub.2013.11.035 (2014).
29. de Boer, E. et al. Efficient biotinylation and single-step purification of tagged transcription factors in mammalian cells and transgenic mice. Proc Natl Acad Sci U S A 100, 7480-7485, doi:10.1073/pnas.1332608100 (2003). (Pubitemid 36759995)
30. Zhang, Y. et al.Model-based analysis of ChIP-Seq (MACS). Genome Biol 9, R137, doi:10.1186/gb-2008-9-9-r137 (2008).
31. Zhang, Z. W., Peterson, M. & Liu, H. Essential role of postsynaptic NMDA receptors in developmental refinement of excitatory synapses. Proc Natl Acad Sci U S A 110, 1095-1100, doi:10.1073/pnas.1212971110 (2013).
32. Fayyazuddin, A., Zaheer, M. A., Hiesinger, P. R. & Bellen, H. J. The nicotinic acetylcholine receptor Dalpha7 is required for an escape behavior in Drosophila. PLoS Biol 4, e63, doi:10.1371/journal.pbio.0040063 (2006).
33. Takemura, S. Y. et al. Cholinergic circuits integrate neighboring visual signals in a Drosophila motion detection pathway. Curr Biol 21, 2077-2084, doi:10.1016/ j.cub.2011.10.053 (2011).
34. Iyer, E. P., Iyer, S. C., Sulkowski, M. J. & Cox, D. N. Isolation and purification of Drosophila peripheral neurons by magnetic bead sorting. J Vis Exp, doi:10.3791/ 1599 (2009).
35. Siddall, N. A., Hime, G. R., Pollock, J. A. & Batterham, P. Ttk69-dependent repression of lozenge prevents the ectopic development of R7 cells in the Drosophila larval eye disc. BMC Dev Biol 9, 64, doi:10.1186/1471-213X-9-64 (2009).
36. Taylor, B. J. Differentiation of a male-specific muscle in Drosophila melanogaster does not require the sex-determining genes doublesex or intersex. Genetics 132, 179-191 (1992).
37. Schneider, I. Cell lines derived from late embryonic stages of Drosophila melanogaster. J Embryol Exp Morphol 27, 353-365 (1972).
38. Zhang, Y. et al. Expression in aneuploid Drosophila S2 cells. PLoS Biol 8, e1000320, doi:10.1371/journal.pbio.1000320 (2010).
39. Blankenberg, D. et al. Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol Chapter 19, Unit 19 10 11-21, doi:10.1002/0471142727.mb1910s89 (2010).
40. Lyne, R. et al. FlyMine: an integrated database for Drosophila and Anopheles genomics. Genome Biol 8, R129, doi:10.1186/gb-2007-8-7-r129 (2007).
41. Vernes, S. C. et al. Foxp2 regulates gene networks implicated in neurite outgrowth in the developing brain. PLoS genetics 7, e1002145, doi:10.1371/ journal.pgen.1002145 (2011).
42. Ren, J. et al. DOG 1.0: illustrator of protein domain structures. Cell Res 19, 271-273, doi:10.1038/cr.2009.6 (2009).
43. Hulsen, T., de Vlieg, J. & Alkema, W. BioVenn - a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9, 488, doi:10.1186/1471-2164-9-488 (2008).