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Original Articles

The white Gene of Drosophilamelanogaster Encodes a Protein with a Role in Courtship Behavior

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Pages 243-276 | Received 07 Sep 2007, Published online: 11 Jul 2009

References

  • Balakireva , M. , Stocker , R. F. , Gendre , N. and Ferveur , J. F. 1998 . Voila, a new Drosophila courtship variant that affects the nervous system: behavioral, neural, and genetic characterization . J Neurosci , 18 : 4335 – 4343 .
  • Borycz , J. , Borycz , J. A. , Kubów , A. , Lloyd , V. , & Meinertzhagen , I. A . 2008 . Drosophila ABC transporter mutants white, brown and scarlet have altered contents and distributions of biogenic amines in the brain . J Exp Biol (under review) .
  • Brody , T. and Cravchik , A. 2000 . Drosophila melanogaster G-protein-coupled receptors . J Cell Biol , 150 : F83 – F88 .
  • Bunch , T. A. , Grinblat , Y. and Goldstein , L. S. B. 1988 . Characterization and use of the Drosophila metallothionein promotor in cultured Drosophila melanogaster cells . Nuc Acid Res , 16 : 1043 – 1061 .
  • Campbell , J. L. and Nash , H. A. 2001 . Volatile general anesthetics reveal a neurobiological role for the white and brown genes of Drosophila melanogaster . J Neurobiol , 49 : 339 – 349 .
  • Castanys-Muñoz , E. , Alder-Baerens , N. , Pomorski , T. , Gamarro , F. and Castanys , S. 2007 . A novel ATP-bainding cassette transporter from Leishmania is involved in transport of phosphatidylcholine analogues and resistance to alky-phospholipids . Mol Microbiol , 64 : 1141 – 1153 .
  • Cherbas , L. and Cherbas , P. 2000 . “ Drosophila cell culture and transformation ” . In Drosophila Protocols Cold Spring Harbor , Edited by: Sullivan , W. , Ashburner , M. and Hawley , R. S. 373 – 387 . NY : Cold Spring Harbor Lab Press .
  • Chintapalli , V. R. , Wang , J. and Dow , J. A. 2007 . Using FlyAtlas to identify better Drosophila melanogaster models of human disease . Nat Genet , 39 : 715 – 720 .
  • Cremona , O. and De Camilli , P. 2001 . Phosphoinositides in membrane traffic at the synapse . J Cell Sci , 114 : 1041 – 1052 .
  • Demidenko , Z. , Badenhorst , P. , Jones , T. , Bi , X. and Mortin , M. A. 2001 . Regulated nuclear export of the homeodomain transcription factor Prospero . Development , 128 : 1359 – 1367 .
  • Diegelmann , S. , Zars , M. and Zars , T. 2006 . Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila . Learn Mem , 13 : 72 – 83 .
  • Dittrich , R. , Bossing , T. , Gould , A. P. , Technau , G. M. and Urban , J. 1997 . The differentiation of the serotonergic neurons in the Drosophila ventral nerve cord depends on the combined function of the zinc finger proteins Eagle and Huckebein . Development , 124 : 2515 – 2525 .
  • Dreesen , T. D. , Johnson , D. H. and Henikoff , S. 1988 . The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes . Mol Cell Biol , 8 : 5206 – 5215 .
  • Dudai , Y. , Buxbaum , J. D. , Corfas , G. and Ofarim , M. 1987 . Formamidines interact with Drosophila octopamine receptors, alter the flies’ behaviour and reduce their learning ability . J Comp Physiol , 161 : 739 – 746 .
  • Evans , J. M. , Day , P. J. , Cabrero , P. , Dow , J. A. and Davies , S.-A. 2008 . A new role for a classical gene: White transports cyclic GMP . J Expt Biol , 211 : 890 – 899 .
  • Ewart , G. D. and Howells , A. J. 1998 . ABC transporters involved in transport of eye pigment precursors in Drosophila melanogaster . Meth Enzymol , 292 : 213 – 224 .
  • Ewart , G. D. , Cannell , D. , Cox , G. B. and Howells , A. J. 1994 . Mutational analysis of the traffic ATPase (ABC) transporters involved in uptake of eye pigment precursors in Drosophila melanogaster. Implications for structure-function relationships . J Biol Chem , 269 : 10370 – 10377 .
  • Falcon-Perez , J. M. , Romero-Calderón , R. , Brooks , E. S. , Krantz , D. E. and Dell'Angelica , E. C. 2007 . The Drosophila pigmentation gene pink (p) encodes a homolog of human Hermansky-Pudlak syndrome 5 (HPS5) . Traffic , 8 : 154 – 168 .
  • Ferguson , J. , Henriksen , S. , Cohen , H. , Mitchell , G. , Barchas , J. and Dement , W. 1970 . Hypersexuality and behavioral changes in cats caused by administration of p-chlorophenylalanine . Science , 168 : 499 – 501 .
  • Ferveur , J.-F. , Störtkuhl , D. F. , Stocker , R. F. and Greenspan , R. J. 1995 . Genetic feminization of brain structures and changed sexual orientation in male Drosophila . Science , 267 : 902 – 905 .
  • Finley , K. D. , Taylor , B. J. , Milstein , M. and McKeown , M. 1997 . dissatisfaction, a gene involved in sex-specific behavior and neural development of Drosophila melanogaster . Proc Natl Acad Sci U S A , 94 : 913 – 918 .
  • Finley , K. D. , Edeen , P. T. , Foss , M. , Gross , E. , Ghbeish , N. , Palmer , R. H. , Taylor , B. J. and McKeown , M. 1998 . dissatisfaction encodes a tailless-like nuclear receptor expressed in a subset of CNS neurons controlling Drosophila sexual behavior . Neuron , 21 : 1363 – 1374 .
  • Fjose , A. , Polito , L. C. , Weber , U. and Gehring , W. J. 1984 . Developmental expression of the white locus of Drosophila melanogaster . EMBO J , 3 : 2087 – 2094 .
  • Fratta , W. , Biggio , G. and Gessa , G. 1977 . Homosexual mounting behavior induced in male rats and rabbits by a tryptophan free diet . Life Sci , 21 : 379 – 384 .
  • Gailey , D. A. , Jackson , F. R. and Siegel , R. W. 1982 . Male courtship in Drosophila: the conditioned response to immature males and its genetic control . Genetics , 102 : 771 – 782 .
  • Gaines , P. , Tompkins , L. , Woodard , C. T. and Carlson , J. R. 2000 . quick-to-court, a Drosophila mutant with elevated levels of sexual behavior, is defective in a predicted coiled-coil protein . Genetics , 154 : 1627 – 1637 .
  • Gessa , G. L. and Tagliamonte , A. 1974 . “ Possible role of brain serotonin and dopamine incontrolling male sexual behavior ” . In Advances in Biochemical Psychopharmacology , Edited by: Costa , E. , Gessa , G. L. and Sandler , M. Vol. 11 , 217 – 228 . New York : Raven .
  • Goodwill , K. E. , Sabatier , C. and Stevens , R. C. 1998 . Crystal structure of tyrosine hydroxylase with bound cofactor analogue and iron at 2.3 A resolution: self-hydroxylation of Phe300 and the pterin-binding site . Biochemistry , 37 : 13437 – 13445 .
  • Green , M. M. 1996 . The “genesis of the white-eyed mutant” in Drosophila melanogaster: a reappraisal . Genetics , 142 : 329 – 331 .
  • Greer , C. L. , Grygoruk , A. , Patton , D. E. , Ley , B. , Romero-Calderón , R. , Chang , H. Y. , Houshyar , R. , Bainton , R. J. , Diantonio , A. and Krantz , D. E. 2005 . A splice variant of the Drosophila vesicular monoamine transporter contains a conserved trafficking domain and functions in the storage of dopamine, serotonin, and octopamine . J Neurobiol , 64 : 239 – 258 .
  • Grosjean , Y. , Balakireva , M. , Dartevelle , L. and Ferveur , J. F. 2001 . PGal4 excision reveals the pleiotropic effects of voila, a Drosophila locus that affects development and courtship behaviour . Genet Res , 77 : 239 – 250 .
  • Grumbling , G. , Strelets , V. , & The FlyBase Consortium . 2006 . FlyBase: anatomical data, images, and queries . Nucl Acids Res , 34 , D484 – D488 . Online document at: http://flybase.org/ (Accessed Aug 1, 2008)
  • Hall , J. C. 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 .
  • Hall , J. C. 1994 . The mating of a fly . Science , 264 : 1702 – 1714 .
  • Hardie , R. C. 1987 . Is histamine a neurotransmitter in insect photoreceptors? . J Comp Physiol A , 161 : 201 – 213 .
  • Hazelrigg , T. 1987 . The Drosophila white gene: a molecular update . Trends Genet , 3 : 43 – 47 .
  • Hirsch , H. V. B. and Tompkins , L. 1994 . The flexible fly: experience-dependent development of complex behaviors in Drosophila melanogaster . J Exp Biol , 195 : 1 – 18 .
  • Hoyer , S. C. , Eckart , A. , Herrel , A. , Zars , T. , Fischer , S. A. , Hardie , S. L. and Heisenberg , M. 2008 . Octopamine in male aggression of Drosophila . Curr Biol , 18 : 159 – 167 .
  • Hyde , S. C. , Emsley , P. , Hartshorn , M. J. , Mimmack , M. M. , Gileadi , U. , Pearce , S. R. , Gallagher , M. P. , Gill , D. R. , Hubbard , R. E. and Higgins , C.F. 1990 . Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance, and bacterial transport . Nature , 346 : 362 – 365 .
  • Jedlitschky , G. , Tirschmann , K. , Lubenow , L. E. , Nieuwenhuis , H. K. , Akkerman , J. W. , Greinacher , A. and Kroemer , K. K. 2004 . The nucleotide transporter MRP4 (ABCC4) is highly expressed in human platelets and present in dense granules, indicated a role in mediator storage . Blood , 104 : 3603 – 3610 .
  • Joh , T. H. 1997 . “ Tryptophan hydroxylase: molecular biology and regulation ” . In Serotonergic Neurons and 5-HT Receptors in the CNS Handbook of Experimental Pharmacology , Edited by: Baumgarten , H. G. and Gothert , M. Vol. 129 , 117 – 129 . Berlin : Springer-Verlag .
  • Kitamoto , T. 2002 . Conditional disruption of synaptic transmission induces male-male courtship behavior in Drosophila . Proc Natl Acad Sci U S A , 99 : 13232 – 13237 .
  • Kretzschmar , D. , Poeck , B. , Roth , H. , Ernst , R. , Keller , A. , Porsch , M. , Strauss , R. and Pflugfelder , G. O. 2000 . Defective pigment granule biogenesis and aberrant behavior caused by mutations in the Drosophila AP-3 adaptin gene ruby . Genetics , 155 : 213 – 223 .
  • Krsmanovic , T. , Pawelec , A. , Sydor , T. and Kölling , R. 2005 . Control of Ste6 recycling by ubiquitination in the early endocytic pathway in yeast . Mol Biol Cell , 16 : 2809 – 2821 .
  • Kumer , S. C. and Vrana , K. E. 1996 . Intricate regulation of tyrosine hydroxylase activity and gene expression . J Neurochem , 67 : 443 – 462 .
  • Kwon , N. S. , Nathan , C. F. and Stuehr , D. J. 1989 . Reduced biopterin as a cofactor in the generation of nitrogen oxides by murine macrophages . J Biol Chem , 264 : 20496 – 20501 .
  • Lazareva , A. A. , Roman , G. , Mattox , W. , Harding , P. E. and Dauwalder , B. 2007 . A role for the adult fat body in Drosophila male courtship behavior . PLoS Genet , 3 : 115 – 122 .
  • Lee , G. and Hall , J. C. 2001 . Abnormalities of male-specific FRU protein and serotonin expression in the CNS of fruitless mutants in Drosophila . J Neurosci , 21 : 513 – 526 .
  • Livingstone , M. and Tempel , B. 1983 . Genetic dissection of monoamine neurotransmitter synthesis in Drosophila . Nature , 303 : 67 – 70 .
  • Lloyd , V. K. , Ramaswami , M. and Krämer , H. 1998 . Not just pretty eyes: Drosophila eye color mutations and lysosomal delivery . Trends Cell Biol , 8 : 257 – 259 .
  • Lloyd , V. K. , Sinclair , D. A. , Wennberg , R. , Warner , T. S. , Honda , B. M. and Grigliatti , T. A. 1999 . A genetic and molecular characterization of the garnet gene of Drosophila melanogaster . Genome , 42 : 1183 – 1193 .
  • Lloyd , V. K. , Sinclair , D. A. R. , Alperyn , M. and Grigliatti , T. A. 2002 . Enhancer of garnet/δAP-3 is a cryptic allele of the white gene and identifies the intracellular transport system for the white protein . Genome , 45 : 296 – 312 .
  • Lorkowski , S. , Kratz , M. , Wenner , C. , Schmidt , R. , Weitkamp , B. , Fobker , M. , Reinhardt , J. , Rauterberg , J. , Galinski , E. A. and Cullen , P. 2001 . Expression of the ATP-binding cassette transporter gene ABCG1 (ABC8) in Tangier disease . Biochem Biophys Res Comm , 283 : 821 – 830 .
  • Mackenzie , S. M. , Howells , A. J. , Cox , G. B. and Ewart , G. D. 2000 . Subcellular localisation of the white/scarlet ABC transporter to pigment granule membranes within the compound eye of Drosophila melanogaster . Genetica , 108 : 239 – 252 .
  • McRobert , S. P. and Tompkins , L. 1988 . Two consequences of homosexual courtship performed by Drosophila melanogaster and Drosophila affinis males . Evolution , 42 : 1093 – 1097 .
  • McRobert , S. P. , Tompkins , L. , Barr , N. B. , Bradner , J. , Lucas , D. , Rattigan , D. M. and Tannous , A. F. 2003 . Mutations in raised Drosophila melanogaster affect experience-dependent aspects of sexual behavior in both sexes . Behav Genet , 33 : 347 – 356 .
  • Mehren , J. E. , Ejima , A. and Griffith , L. C. 2004 . Unconventional sex: fresh approaches to courtship learning . Curr Opin Neurobiol , 14 : 745 – 750 .
  • Morgan , T. H. 1910 . Sex-limited inheritance in Drosophila . Science , 32 : 120 – 122 .
  • Mount , S. M. 1987 . Sequence similarity . Nature , 325 : 487
  • Nakamura , M. , Ueno , S. , Sano , A. and Tanabe , H. 1999 . Polymorphisms of the human homologue of the Drosophila white gene are associated with mood and panic disorders . Mol Psychiatry , 4 : 155 – 162 .
  • Narayanan , R. , Krämer , H. and Ramaswami , M. 2000 . Drosophila endosomal proteins hook and deep orange regulate synapse size but not synaptic vesicle recycling . J Neurobiol , 45 : 105 – 119 .
  • Neckameyer , W. S. 1998 . Dopamine and mushroom bodies in Drosophila: experience-dependent and -independent aspects of sexual behavior . Learn Mem , 5 : 157 – 165 .
  • Nilsson , E. E. , Asztalos , Z. , Lukacsovich , T. , Awano , W. , Usui-aoki , K. and Yamamoto , D. 2000 . Fruitless is in the regulatory pathway by which ectopic mini-white and transformer induce bisexual courtship in Drosophila . J Neurogenet , 13 : 213 – 232 .
  • Nolte , D. J. 1952 . The eye pigmentary system of Drosophila: III. The action of eye-color genes . J Genet , 51 : 142 – 186 .
  • Nolte , D. J. 1961 . The pigment granules of the compound eyes of Drosophila . Heredity , 16 : 25 – 38 .
  • Ooi , C. E. , Moreira , J. E. , Dell'Angelica , E. C. , Poy , G. , Wassarman , D. A. , & Bonifacino , J. S . 1997 . Altered expression of a novel adaptin leads to defective pigment granule biogenesis in the Drosophila eye color mutant garnet . EMBO J , 16 , 4508 – 4518 . [COMP: Per alpha order, move Ooi et al between Odorizzi et al and Pepling & Mount]
  • Odorizzi , G. , Cowles , C. R. and Emr , S. D. 1998 . The AP-3 complex: a coat of many colours . Trends Cell Biol , 8 : 282 – 288 .
  • Pepling , M. and Mount , S. M. 1990 . Sequence of a cDNA from the Drosophila melanogaster white gene . Nucl Acids Res , 18 : 1633
  • Phillips , J. P. and Forrest , H. S. 1980 . “ Ommochromes and pteridines ” . In The Biology and Genetics of Drosophila , Edited by: Ashburner , M. and Wright , S. 541 – 623 . London/New York : Academic Press .
  • Pirrotta , V. 1988 . “ Vectors for P-element transformation in Drosophila ” . In Vectors: A Survey of Molecular Cloning Vectors and their Uses , Edited by: Rodriguez , R. L. and Denhart , D. T. 437 – 456 . London : Butterworths .
  • Rabinow , L. , Nguyen-Huynh , A. T. and Birchler , J. A. 1991 . A trans-acting regulatory gene that inversely affects the expression of the white, brown, and scarlet loci in Drosophila . Genetics , 129 : 463 – 480 .
  • Regnier-Vigouroux , A. and Huttner , W. B. 1993 . Biogenesis of small synaptic vesicles and synaptic-like microvesicles . Neurochem Res , 18 : 59 – 64 .
  • Sambrook , J. , Fritsch , E. F. , & Maniatis , T . 1989 . In: C. Nolan Molecular Cloning: A Laboratory Manual New York : Cold Spring Harbor Laboratory Press .
  • Sarthy , P. V. 1991 . Histamine: a neurotransmitter candidate for Drosophila photoreceptors . J Neurochem , 57 : 1757 – 1768 .
  • Savvateeva , E. , Popov , A. , Kamyshev , N. , Bragina , J. , Heisenberg , M. , Senitz , D. , Kornhuber , J. and Riederer , P. 2000 . Age-dependent memory loss, synaptic pathology, and altered brain plasticity in the Drosophila mutant cardinal accumulating 3-hydroxykynurenine . J Neural Trans , 107 : 581 – 601 .
  • Schmitz , G. , Langmann , T. and Heimerl , S. 2001 . Role of ABCG1 and other ABCG family members in lipid metabolism . J Lipid Res , 42 : 1513 – 1520 .
  • Schraermeyer , U. and Dohms , M. 1993 . Atypical granules in the eyes of the white mutant of Drosophila melanogaster are lysosome-related organelles . Pig Cell Res , 6 : 73 – 84 .
  • Schwaerzel , M. , Monastirioti , M. , Scholz , H. , Friggi-Grelin , F. , Birman , S. and Heisenberg , M. 2003 . Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila . J Neurosci , 23 : 10495 – 10502 .
  • Scott , D. and Richmond , R. C. 1988 . Pheromones exchanged during mating: a mechanism for mate assessment in Drosophila . Animal Behav , 36 : 1164 – 1173 .
  • Sevrioukov , E. A , He , J.-P. , Moghrabi , N. , Suio , A. and Kramer , H. 1999 . A role for the deep orange and carnation eye-color genes in lysosomal delivery in Drosophila . Molec Cell , 4 : 479 – 486 .
  • Shestopal , S. A. , Makunin , I. V. , Belyaeva , E. S. , Ashburner , M. and Zhimulev , I. F. 1997 . Molecular characterization of the deep orange (dor) gene of Drosophila melanogaster . Molec Gen Genet , 253 : 642 – 648 .
  • Shoup , J. R. 1966 . The development of pigment granules in the eyes of wild-type and mutant Drosophila melanogaster . J Cell Biol , 29 : 223 – 249 .
  • Simpson , F. , Peden , A. A. , Christopoulou , L. and Robinson , M. S. 1997 . Characterization of the adaptor-related protein complex, AP-3 . J Cell Biol , 137 : 835 – 845 .
  • Spieth , H. T. 1974 . Courtship behaviour in Drosophila . Ann Rev Entomol , 19 : 385 – 405 .
  • Sriram , V. , Krishnan , K. S. and Mayor , S. 2003 . deep-orange and carnation define distinct stages in late endosomal biogenesis in Drosophila melanogaster . J Cell Biol , 161 : 593 – 607 .
  • Stark , W. S. and Sapp , R. 1988 . Eye-color pigment granules in wild-type and mutant Drosophila melanogaster . Can J Zool , 66 : 1301 – 1308 .
  • Sullivan , D. T. , Grillo , S. L. and Kitos , R. J. 1974 . Subcellular localization of the first three enzymes of the ommochrome synthetic pathway in Drosophila melanogaster . J Exp Zool , 188 : 225 – 234 .
  • Sullivan , D. T. and Sullivan , M. C. 1975 . Transport defects as the physiological basis for eye-color mutants of Drosophila melanogaster . Biochem Genet , 13 : 603 – 613 .
  • Sullivan , D. T. , Bell , L. A. , Paton , D. R. and Sullivan , M. C. 1979 . Purine transport by malpighian tubules of pteridine-deficient eye color mutants . Biochem Genet , 17 : 565 – 573 .
  • Sullivan , D. T. , Bell , L. A. , Paton , D. R. and Sullivan , M. C. 1980 . Genetic and functional analysis of tryptophan transport in Malpighian tubules of Drosophila . Biochem Genet , 18 : 1109 – 1130 .
  • Syrzycka , M. , McEachern , L. A. , Kinneard , J. , Prabhu , K. , Fitzpatrick , K. , Schulze , S. , Rawls , J. M. , Lloyd , V. , Sinclair , D. A. R. and Honda , B. M. 2007 . The pink gene encodes the Drosophila orthologue of the human Hermansky-Pudlak syndrome 5 (HPS5) gene . Genome , 50 : 548 – 556 .
  • Tagliamonte , A. , Tagliamonte , P. , Gessa , G. L. and Brodie , B. B. 1969 . Compulsive sexual activity induced by p-chlorophenylalanine in normal and pinealectomized male rats . Science , 166 : 1433 – 1435 .
  • Tearle , R. G. , Belote , J. M. , McKeown , M. , Baker , B. S. and Howells , A. J. 1989 . Cloning and characterization of the scarlet gene of Drosophila melanogaster . Genetics , 122 : 595 – 606 .
  • Tempel , B. L. , Bonini , N. , Dawson , D. R. and Quinn , W. G. 1983 . Reward learning in normal and mutant Drosophila . Proc Natl Acad Sci U S A , 80 : 1482 – 1486 .
  • Villella , A. and Hall , J. C. 1996 . Courtship anomalies caused by doublesex mutations in Drosophila melanogaster . Genetics , 143 : 331 – 344 .
  • Zhang , S.-D. and Odenwald , W. F. 1995 . Misexpression of the white (w) gene triggers male-male courtship in Drosophila . Proc Natl Acad Sci , 92 : 5525 – 5529 .

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