Soluble circulating proteins play an important role in the regulation of mating behavior in Drosophila melanogaster. However, how these factors signal through the blood–brain barrier (bbb) to interact with the sex-specific brain circuits that control courtship is unknown. Here we show that male identity of the blood–brain barrier is necessary and that male-specific factors in the bbb are physiologically required for normal male courtship behavior. Feminization of the bbb of adult males significantly reduces male courtship. We show that the bbb–specific G-protein coupled receptor moody and bbb–specific Go signaling in adult males are necessary for normal courtship. These data identify sex-specific factors and signaling processes in the bbb as important regulators of male mating behavior.
Vyšlo v časopise: Sex-Specific Signaling in the Blood–Brain Barrier Is Required for Male Courtship in. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003217 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003217
1. GreenspanRJ (1995) Understanding the genetic construction of behavior. Sci Am 272 : 72–78.
2. HallJC (1994) The mating of a fly. Science 264 : 1702–1714.
3. VillellaA, HallJC (2008) Neurogenetics of courtship and mating in Drosophila. Adv Genet 62 : 67–184.
4. BeloteJM, BakerBS (1987) Sexual behavior: its genetic control during development and adulthood in Drosophila melanogaster. Proc Natl Acad Sci U S A 84 : 8026–8030.
5. McRobertSP, TompkinsL (1985) The effect of transformer, doublesex and intersex mutations on the sexual behavior of Drosophila melanogaster. Genetics 111 : 89–96.
6. TaylorBJ, VillellaA, RynerLC, BakerBS, HallJC (1994) Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev Genet 15 : 275–296.
7. DemirE, DicksonBJ (2005) fruitless splicing specifies male courtship behavior in Drosophila. Cell 121 : 785–794.
8. ItoH, FujitaniK, UsuiK, Shimizu-NishikawaK, TanakaS, et al. (1996) 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.
9. ManoliDS, FossM, VillellaA, TaylorBJ, HallJC, et al. (2005) Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature
10. RideoutEJ, DornanAJ, NevilleMC, EadieS, GoodwinSF (2010) Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci 13 : 458–466.
11. RynerLC, GoodwinSF, CastrillonDH, AnandA, VillellaA, et al. (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87 : 1079–1089.
12. StockingerP, KvitsianiD, RotkopfS, TirianL, DicksonBJ (2005) Neural circuitry that governs Drosophila male courtship behavior. Cell 121 : 795–807.
13. DauwalderB (2011) The roles of fruitless and doublesex in the control of male courtship. Int Rev Neurobiol 99 : 87–105.
14. ManoliDS, MeissnerGW, BakerBS (2006) Blueprints for behavior: genetic specification of neural circuitry for innate behaviors. Trends Neurosci 29 : 444–451.
15. RideoutEJ, BilleterJC, GoodwinSF (2007) The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr Biol 17 : 1473–1478.
16. YamamotoD (2007) The neural and genetic substrates of sexual behavior in Drosophila. Adv Genet 59 : 39–66.
17. CacheroS, OstrovskyAD, YuJY, DicksonBJ, JefferisGS (2010) Sexual dimorphism in the fly brain. Curr Biol 20 : 1589–1601.
18. KimuraK (2011) Role of cell death in the formation of sexual dimorphism in the Drosophila central nervous system. Dev Growth Differ 53 : 236–244.
19. YuJY, KanaiMI, DemirE, JefferisGS, DicksonBJ (2010) Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 20 : 1602–1614.
20. DauwalderB, TsujimotoS, MossJ, MattoxW (2002) The Drosophila takeout gene is regulated by the somatic sex-determination pathway and affects male courtship behavior. Genes Dev 16 : 2879–2892.
21. FujiiS, AmreinH (2002) Genes expressed in the Drosophila head reveal a role for fat cells in sex-specific physiology. Embo J 21 : 5353–5363.
22. LazarevaAA, RomanG, MattoxW, HardinPE, DauwalderB (2007) A role for the adult fat body in Drosophila male courtship behavior. PLoS Genet 3: e16 doi:10.1371/journal.pgen.0030016.
23. ArbeitmanMN, FlemingAA, SiegalML, NullBH, BakerBS (2004) A genomic analysis of Drosophila somatic sexual differentiation and its regulation. Development 131 : 2007–2021.
24. EllisLL, CarneyGE (2010) Socially-responsive gene expression in male Drosophila melanogaster is influenced by the sex of the interacting partner. Genetics 187 : 157–169.
25. EllisLL, CarneyGE (2010) Mating alters gene expression patterns in Drosophila melanogaster male heads. BMC Genomics 11 : 558.
26. GoldmanTD, ArbeitmanMN (2007) Genomic and functional studies of Drosophila sex hierarchy regulated gene expression in adult head and nervous system tissues. PLoS Genet 3: e216 doi:10.1371/journal.pgen.0030216.
27. AwasakiT, LaiSL, ItoK, LeeT (2008) Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci 28 : 13742–13753.
28. BaintonRJ, TsaiLT, SchwabeT, DeSalvoM, GaulU, et al. (2005) moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 123 : 145–156.
29. SchwabeT, BaintonRJ, FetterRD, HeberleinU, GaulU (2005) GPCR signaling is required for blood-brain barrier formation in Drosophila. Cell 123 : 133–144.
30. StorkT, EngelenD, KrudewigA, SiliesM, BaintonRJ, et al. (2008) Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28 : 587–597.
31. AbbottNJ (2005) Dynamics of CNS barriers: evolution, differentiation, and modulation. Cell Mol Neurobiol 25 : 5–23.
32. BanerjeeS, PillaiAM, PaikR, LiJ, BhatMA (2006) Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila. J Neurosci 26 : 3319–3329.
33. BaumgartnerS, LittletonJT, BroadieK, BhatMA, HarbeckeR, et al. (1996) A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87 : 1059–1068.
34. BlauthK, BanerjeeS, BhatMA (2010) Axonal ensheathment and intercellular barrier formation in Drosophila. Int Rev Cell Mol Biol 283 : 93–128.
35. Faivre-SarrailhC, BanerjeeS, LiJ, HortschM, LavalM, et al. (2004) Drosophila contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function. Development 131 : 4931–4942.
36. DeSalvoMK, MayerN, MayerF, BaintonRJ (2011) Physiologic and anatomic characterization of the brain surface glia barrier of Drosophila. Glia 59 : 1322–1340.
37. MayerF, MayerN, ChinnL, PinsonneaultRL, KroetzD, et al. (2009) Evolutionary conservation of vertebrate blood–brain barrier chemoprotective mechanisms in Drosophila. J Neurosci 29 : 3538–3550.
38. BakerBS, RidgeKA (1980) Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94 : 383–423.
39. FerveurJF, StortkuhlKF, StockerRF, GreenspanRJ (1995) Genetic feminization of brain structures and changed sexual orientation in male Drosophila [see comments]. Science 267 : 902–905.
40. McKeownM, BeloteJM, BoggsRT (1988) Ectopic expression of the female transformer gene product leads to female differentiation of chromosomally male Drosophila. Cell 53 : 887–895.
41. AnandA, VillellaA, RynerLC, CarloT, GoodwinSF, et al. (2001) Molecular Genetic Dissection of the Sex-Specific and Vital Functions of the Drosophila melanogaster Sex Determination Gene fruitless. Genetics 158 : 1569–1595.
42. SeppKJ, SchulteJ, AuldVJ (2001) Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev Biol 238 : 47–63.
43. McGuireSE, RomanG, DavisRL (2004) Gene expression systems in Drosophila: a synthesis of time and space. Trends Genet 20 : 384–391.
44. ChangPL, DunhamJP, NuzhdinSV, ArbeitmanMN (2011) Somatic sex-specific transcriptome differences in Drosophila revealed by whole transcriptome sequencing. BMC Genomics 12 : 364.
45. ParksS, WieschausE (1991) The Drosophila gastrulation gene concertina encodes a G alpha-like protein. Cell 64 : 447–458.
46. KatadaT, TamuraM, UiM (1983) The A protomer of islet-activating protein, pertussis toxin, as an active peptide catalyzing ADP-ribosylation of a membrane protein. Arch Biochem Biophys 224 : 290–298.
47. FerrisJ, GeH, LiuL, RomanG (2006) G(o) signaling is required for Drosophila associative learning. Nat Neurosci 9 : 1036–1040.
48. FitchCL, de SousaSM, O'DayPM, NeubertTA, PlantillaCM, et al. (1993) Pertussis toxin expression in Drosophila alters the visual response and blocks eating behaviour. Cell Signal 5 : 187–207.
49. HopkinsRS, StamnesMA, SimonMI, HurleyJB (1988) Cholera toxin and pertussis toxin substrates and endogenous ADP-ribosyltransferase activity in Drosophila melanogaster. Biochim Biophys Acta 970 : 355–362.
50. SchaeferM, PetronczkiM, DornerD, ForteM, KnoblichJA (2001) Heterotrimeric G proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell 107 : 183–194.
51. WolfgangWJ, RobertsIJ, QuanF, O'KaneC, ForteM (1996) Activation of protein kinase A-independent pathways by Gs alpha in Drosophila. Proc Natl Acad Sci U S A 93 : 14542–14547.
52. WolfgangWJ, HoskoteA, RobertsIJ, JacksonS, ForteM (2001) Genetic analysis of the Drosophila Gs(alpha) gene. Genetics 158 : 1189–1201.
53. LiW, OhlmeyerJT, LaneME, KalderonD (1995) Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development. Cell 80 : 553–562.
54. MossJ, YostDA, StanleySJ (1983) Amino acid-specific ADP-ribosylation. J Biol Chem 258 : 6466–6470.
55. StrockJ, Diverse-PierluissiMA (2004) Ca2+ channels as integrators of G protein-mediated signaling in neurons. Mol Pharmacol 66 : 1071–1076.
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