Sex-Specific Signaling in the Blood-Brain Barrier Is Required for Male Courtship in Drosophila

PLoS Genetics

Volumn 9, Issue 1, 2013, Pages

  Hoxha, Valbona ^a   Lama, Chamala ^a   Chang, Peter L ^b   Saurabh, Sumit ^a   Patel, Naiya ^a   Olate, Nicole ^a   Dauwalder, Brigitte ^a  

^a University of Houston   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CONTROL; BLOOD BRAIN BARRIER; CONTROLLED STUDY; COURTSHIP; DROSOPHILA MELANOGASTER; FEMALE; FEMINIZATION; GENDER IDENTITY; INTRACELLULAR SIGNALING; MALE; MATING; MOLECULAR INTERACTION; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEX DIFFERENCE;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CENTRAL NERVOUS SYSTEM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; MUTATION; RECEPTORS, G-PROTEIN-COUPLED; SEXUAL BEHAVIOR, ANIMAL; SIGNAL TRANSDUCTION;

EID: 84873494782     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003217     Document Type: Article

References (55)

1. Greenspan RJ, (1995) Understanding the genetic construction of behavior. Sci Am 272: 72-78.
2. Hall JC, (1994) The mating of a fly. Science 264: 1702-1714.
3. Villella A, Hall JC, (2008) Neurogenetics of courtship and mating in Drosophila. Adv Genet 62: 67-184.
4. Belote JM, Baker BS, (1987) Sexual behavior: its genetic control during development and adulthood in Drosophila melanogaster. Proc Natl Acad Sci U S A 84: 8026-8030.
5. McRobert SP, Tompkins L, (1985) The effect of transformer, doublesex and intersex mutations on the sexual behavior of Drosophila melanogaster. Genetics 111: 89-96.
6. Taylor BJ, Villella A, Ryner LC, Baker BS, Hall JC, (1994) Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev Genet 15: 275-296.
7. Demir E, Dickson BJ, (2005) fruitless splicing specifies male courtship behavior in Drosophila. Cell 121: 785-794.
8. Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, 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. Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, et al. (2005) Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature.
10. Rideout EJ, Dornan AJ, Neville MC, Eadie S, Goodwin SF, (2010) Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci 13: 458-466.
11. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, et al. (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87: 1079-1089.
12. Stockinger P, Kvitsiani D, Rotkopf S, Tirian L, Dickson BJ, (2005) Neural circuitry that governs Drosophila male courtship behavior. Cell 121: 795-807.
13. Dauwalder B, (2011) The roles of fruitless and doublesex in the control of male courtship. Int Rev Neurobiol 99: 87-105.
14. Manoli DS, Meissner GW, Baker BS, (2006) Blueprints for behavior: genetic specification of neural circuitry for innate behaviors. Trends Neurosci 29: 444-451.
15. Rideout EJ, Billeter JC, Goodwin SF, (2007) The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr Biol 17: 1473-1478.
16. Yamamoto D, (2007) The neural and genetic substrates of sexual behavior in Drosophila. Adv Genet 59: 39-66.
17. Cachero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GS, (2010) Sexual dimorphism in the fly brain. Curr Biol 20: 1589-1601.
18. Kimura K, (2011) Role of cell death in the formation of sexual dimorphism in the Drosophila central nervous system. Dev Growth Differ 53: 236-244.
19. Yu JY, Kanai MI, Demir E, Jefferis GS, Dickson BJ, (2010) Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 20: 1602-1614.
20. Dauwalder B, Tsujimoto S, Moss J, Mattox W, (2002) The Drosophila takeout gene is regulated by the somatic sex-determination pathway and affects male courtship behavior. Genes Dev 16: 2879-2892.
21. Fujii S, Amrein H, (2002) Genes expressed in the Drosophila head reveal a role for fat cells in sex-specific physiology. Embo J 21: 5353-5363.
22. Lazareva AA, Roman G, Mattox W, Hardin PE, Dauwalder B, (2007) A role for the adult fat body in Drosophila male courtship behavior. PLoS Genet 3: e16 doi:10.1371/journal.pgen.0030016.
23. Arbeitman MN, Fleming AA, Siegal ML, Null BH, Baker BS, (2004) A genomic analysis of Drosophila somatic sexual differentiation and its regulation. Development 131: 2007-2021.
24. Ellis LL, Carney GE, (2010) Socially-responsive gene expression in male Drosophila melanogaster is influenced by the sex of the interacting partner. Genetics 187: 157-169.
25. Ellis LL, Carney GE, (2010) Mating alters gene expression patterns in Drosophila melanogaster male heads. BMC Genomics 11: 558.
26. Goldman TD, Arbeitman MN, (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. Awasaki T, Lai SL, Ito K, Lee T, (2008) Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci 28: 13742-13753.
28. Bainton RJ, Tsai LT, Schwabe T, DeSalvo M, Gaul U, et al. (2005) moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 123: 145-156.
29. Schwabe T, Bainton RJ, Fetter RD, Heberlein U, Gaul U, (2005) GPCR signaling is required for blood-brain barrier formation in Drosophila. Cell 123: 133-144.
30. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, et al. (2008) Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28: 587-597.
31. Abbott NJ, (2005) Dynamics of CNS barriers: evolution, differentiation, and modulation. Cell Mol Neurobiol 25: 5-23.
32. Banerjee S, Pillai AM, Paik R, Li J, Bhat MA, (2006) Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila. J Neurosci 26: 3319-3329.
33. Baumgartner S, Littleton JT, Broadie K, Bhat MA, Harbecke R, et al. (1996) A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87: 1059-1068.
34. Blauth K, Banerjee S, Bhat MA, (2010) Axonal ensheathment and intercellular barrier formation in Drosophila. Int Rev Cell Mol Biol 283: 93-128.
35. Faivre-Sarrailh C, Banerjee S, Li J, Hortsch M, Laval M, 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. DeSalvo MK, Mayer N, Mayer F, Bainton RJ, (2011) Physiologic and anatomic characterization of the brain surface glia barrier of Drosophila. Glia 59: 1322-1340.
37. Mayer F, Mayer N, Chinn L, Pinsonneault RL, Kroetz D, et al. (2009) Evolutionary conservation of vertebrate blood-brain barrier chemoprotective mechanisms in Drosophila. J Neurosci 29: 3538-3550.
38. Baker BS, Ridge KA, (1980) Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94: 383-423.
39. Ferveur JF, Stortkuhl KF, Stocker RF, Greenspan RJ, (1995) Genetic feminization of brain structures and changed sexual orientation in male Drosophila [see comments]. Science 267: 902-905.
40. McKeown M, Belote JM, Boggs RT, (1988) Ectopic expression of the female transformer gene product leads to female differentiation of chromosomally male Drosophila. Cell 53: 887-895.
41. Anand A, Villella A, Ryner LC, Carlo T, Goodwin SF, 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. Sepp KJ, Schulte J, Auld VJ, (2001) Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev Biol 238: 47-63.
43. McGuire SE, Roman G, Davis RL, (2004) Gene expression systems in Drosophila: a synthesis of time and space. Trends Genet 20: 384-391.
44. Chang PL, Dunham JP, Nuzhdin SV, Arbeitman MN, (2011) Somatic sex-specific transcriptome differences in Drosophila revealed by whole transcriptome sequencing. BMC Genomics 12: 364.
45. Parks S, Wieschaus E, (1991) The Drosophila gastrulation gene concertina encodes a G alpha-like protein. Cell 64: 447-458.
46. Katada T, Tamura M, Ui M, (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. Ferris J, Ge H, Liu L, Roman G, (2006) G(o) signaling is required for Drosophila associative learning. Nat Neurosci 9: 1036-1040.
48. Fitch CL, de Sousa SM, O'Day PM, Neubert TA, Plantilla CM, et al. (1993) Pertussis toxin expression in Drosophila alters the visual response and blocks eating behaviour. Cell Signal 5: 187-207.
49. Hopkins RS, Stamnes MA, Simon MI, Hurley JB, (1988) Cholera toxin and pertussis toxin substrates and endogenous ADP-ribosyltransferase activity in Drosophila melanogaster. Biochim Biophys Acta 970: 355-362.
50. Schaefer M, Petronczki M, Dorner D, Forte M, Knoblich JA, (2001) Heterotrimeric G proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell 107: 183-194.
51. Wolfgang WJ, Roberts IJ, Quan F, O'Kane C, Forte M, (1996) Activation of protein kinase A-independent pathways by Gs alpha in Drosophila. Proc Natl Acad Sci U S A 93: 14542-14547.
52. Wolfgang WJ, Hoskote A, Roberts IJ, Jackson S, Forte M, (2001) Genetic analysis of the Drosophila Gs(alpha) gene. Genetics 158: 1189-1201.
53. Li W, Ohlmeyer JT, Lane ME, Kalderon D, (1995) Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development. Cell 80: 553-562.
54. Moss J, Yost DA, Stanley SJ, (1983) Amino acid-specific ADP-ribosylation. J Biol Chem 258: 6466-6470.
55. Strock J, Diverse-Pierluissi MA, (2004) Ca2+ channels as integrators of G protein-mediated signaling in neurons. Mol Pharmacol 66: 1071-1076.