Neuropeptide Biology in Drosophila

  • Elke Clynen
  • Ank Reumer
  • Geert Baggerman
  • Inge Mertens
  • Liliane Schoofs
Part of the Advances in Experimental Medicine and Biology book series (volume 692)

Abstract

D rosophila melanogaster is since decades the most important invertebrate model. With the publishing of the genome sequence, Drosophila also became a pioneer in (neuro)peptide research. Neuropeptides represent a major group of signaling molecules that outnumber all other types of neurotransmitters/modulators and hormones. By means of bioinformatics 119 (neuro)peptide precursor genes have been predicted from the Drosophila genome. Using the neuropeptidomics technology 46 neuropeptides derived from 19 of these precursors could be biochemically characterized. At the cellular level, neuropeptides usually exert their action by binding to membrane receptors, many of which belong to the family of G-protein coupled receptors or GPCRs. Such receptors are the major target for many contemporary drugs. In this chapter, we will describe the identification, localization and functional characterization of neuropeptide-receptor pairs in Drosophila melanogaster.

Keywords

Toxicity Recombination Beach Neurol Acetylcholine 

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References

  1. 1.
    Adams MD, Celniker SE, Holt RA et al. The genome sequence of Drosophila melanogaster. Science 2000; 287:2185–2195.PubMedCrossRefGoogle Scholar
  2. 12.
    Baggerman G, Liu F, Wets G et al. Bioinformatic analysis of peptide precursor proteins. Ann NY Acad Sci 2005; 1040:59–65.PubMedCrossRefGoogle Scholar
  3. 3.
    Vanden Broeck J. Neuropeptides and their precursors in the fruitfly, Drosophila melanogaster. Peptides 2001; 22:241–254.CrossRefGoogle Scholar
  4. 4.
    Hewes RS, Taghert PH. Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Gen Res 2001; 11:1126–1142.CrossRefGoogle Scholar
  5. 5.
    Liu F, Baggerman G, D’Hertog W et al. In silico identification of new secretory peptide genes in Drosophila melanogaster. Mol Cell Proteomics 2006; 5:510–522.PubMedGoogle Scholar
  6. 6.
    Liu F, Baggerman G, Schoofs L et al. Uncovering conserved patterns in bioactive peptides in Metazoa. Peptides 2006; 27:3137–3153.PubMedCrossRefGoogle Scholar
  7. 7.
    Clynen E, De Loof A, Schoofs L. The use of peptidomics in endocrine research. Minireview. Gen Comp Endocrinol 2003; 132:1–9.CrossRefGoogle Scholar
  8. 8.
    Baggerman G, Verleyen P, Clynen E et al. Peptidomics J Chromatogr B Analyt Technol Biomed Life Sci 2004; 803:3–16.CrossRefGoogle Scholar
  9. 9.
    Schulz-Knappe P, Zucht HD, Heine C et al. Peptidomics: the comprehensive analysis of peptides in complex biological mixtures. Comb Chem High T Scr 2001; 4:207–217.Google Scholar
  10. 10.
    Baggerman G, Cerstiaens A, De Loof A et al. Peptidomics of the larval Drosophila melanogaster central nervous system. J Biol Chem 2002; 277:40368–40374.PubMedCrossRefGoogle Scholar
  11. 11.
    Baggerman G, Boonen K, Verleyen P et al. Peptidomic analysis of the larval Drosophila melanogaster central nervous system by two-dimensional capillary liquid chromatography quadrupole time-of-flight mass spectrometry. J Mass Spectrom 2005; 40:250–260.PubMedCrossRefGoogle Scholar
  12. 12.
    Schoofs L, Baggerman G. Peptidomics in Drosophila melanogaster. Briefings in functional genomics and proteomics 2003; 2:114–120.PubMedCrossRefGoogle Scholar
  13. 13.
    Zupanc GKH. Peptidergic transmission: from morphological correlates to functional implications. Micron 1996; 27:35–91.PubMedCrossRefGoogle Scholar
  14. 14.
    Bockaert J, Pin JP. Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J 1999; 18:1723–1729.PubMedCrossRefGoogle Scholar
  15. 15.
    Gether U. Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocrine Reviews 2000; 21:90–113.PubMedCrossRefGoogle Scholar
  16. 16.
    Schlyer S, Horuk R. I want a new drug: G-protein-coupled receptors in drug development. Drug Discovery Today 2006; 11:481–493.PubMedCrossRefGoogle Scholar
  17. 17.
    Drews J. Drug discovery: a historical perspective. Science 2000; 287:1960–1964.PubMedCrossRefGoogle Scholar
  18. 18.
    Mertens I, Vandingenen A, Meeusen T et al. Postgenomic characterization of G-protein-coupled receptors. Pharmacogenomics 2004; 5:657–672.PubMedCrossRefGoogle Scholar
  19. 19.
    Thomsen W, Frazer J, Unett D. Functional assays for screening GPCR targets. Current Opinion in Biotechnology 2005; 16:655–665.PubMedGoogle Scholar
  20. 20.
    Leifert WR, Aloia AL, Bucco O et al. G-protein-coupled receptors in drug discovery: nanosizing using cell-free technologies and molecular biology approaches. J Biomol Screen 2005; 10:765–779.PubMedCrossRefGoogle Scholar
  21. 21.
    Nässel DR, Homberg U. Neuropeptides in interneurons of the insect brain. Cell Tissue Res 2006; 326:1–24.PubMedCrossRefGoogle Scholar
  22. 22.
    Santos JS, Voemel M, Homberg U et al. Three-dimensional charting of peptidergic neurons in the larval ventral nerve cord of the fruit fly, Drosophila melanogaster. J Neurogenet 2006; 20:214–215.Google Scholar
  23. 23.
    Predel R, Wegener C, Russell WK et al. Peptidomics of CNS-associated neurohemal systems of adult Drosophila melanogaster: a mass spectrometric survey of peptides from individual flies. J Comp Neurol 2004; 474:379–392.PubMedCrossRefGoogle Scholar
  24. 24.
    Wegener C, Reinl T, Jansch L et al. Direct mass spectrometric peptide profiling and fragmentation of larval peptide hormone release sites in Drosophila melanogaster reveals tagma-specific peptide expression and differential processing. J Neurochem 2006; 96:1362–1374.PubMedCrossRefGoogle Scholar
  25. 25.
    Neupert S, Johard HAD, Nässel DR et al. Mass spectrometric analysis of peptide content in single circadian pacemaker neurons (large LNVS) in Drosophila melanogaster. J Neurogenet 2006; 20:186–187.Google Scholar
  26. 26.
    Neupert S, Predel R. Analysis of neuropeptide expression in single hugin-neurons using MALDI-TOF MS. J Neurogenet 2006;20:187–187.Google Scholar
  27. 27.
    St Johnston D. The art and design of genetic screens: Drosophila melanogaster. Nat Rev Genet 2002; 3:176–188.PubMedCrossRefGoogle Scholar
  28. 28.
    Adams MD, Sekelsky JJ. From sequence to phenotype: reverse genetics in Drosophila melanogaster. Nat Rev Genet 2002; 3:189–198.PubMedCrossRefGoogle Scholar
  29. 29.
    Rubin GM, Spradling AC. Genetic transformation of Drosophila with transposable element vectors. Science 1982; 218:348–353.PubMedCrossRefGoogle Scholar
  30. 30.
    Spradling AC, Rubin GM. Transposition of cloned P elements into Drosophila germ line chromosomes. Science 1982; 218:341–347.PubMedCrossRefGoogle Scholar
  31. 31.
    Ryder E, Russell S. Transposable elements as tools for genomics and genetics in Drosophila. Brief Funct Genomic Proteomic 2003; 2:57–71.PubMedCrossRefGoogle Scholar
  32. 32.
    Echols H, Gingery R, Moore L. Integrative recombination function of bacteriophage lambda: evidence for a site-specific recombination enzyme. J Mol Biol 1968; 34:251–260.PubMedCrossRefGoogle Scholar
  33. 33.
    Gong WJ, Golic KG. Ends-out, or replacement, gene targeting in Drosophila. Proc Natl Acad Sci USA 2003; 100:2556–2561.PubMedCrossRefGoogle Scholar
  34. 34.
    Rong YS, Golic KG. Gene targeting by homologous recombination in Drosophila. Science 2000; 288:2013–2018.PubMedCrossRefGoogle Scholar
  35. 35.
    Fire A, Xu S, Montgomery MK et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998; 391:806–811.PubMedCrossRefGoogle Scholar
  36. 36.
    Kennerdell JR, Carthew RW. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 1998; 95:1017–1026.PubMedCrossRefGoogle Scholar
  37. 37.
    Ashburner M, Golic KG, Hawley RS. Drosophila: a laboratory handbook. 2005; second edition.Google Scholar
  38. 38.
    Renn SC, Park JH, Rosbash M et al. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 1999; 99:791–802.PubMedCrossRefGoogle Scholar
  39. 39.
    Park Y, Filippov V, Gill SS et al. Deletion of the ecdysis-triggering hormone gene leads to lethal ecdysis deficiency. Development 2002; 129:493–503.PubMedGoogle Scholar
  40. 40.
    Lee G, Park JH. Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 2004; 167:311–323.PubMedCrossRefGoogle Scholar
  41. 41.
    Dulcis D, Levine RB, Ewer J. Role of the neuropeptide CCAP in Drosophila cardiac function. J Neurobiol 2005; 64:259–274.PubMedCrossRefGoogle Scholar
  42. 42.
    Park JH, Schroeder AJ, Helfrich-Forster C et al. Targeted ablation of CCAP neuropeptide-containing neurons of Drosophila causes specific defects in execution and circadian timing of ecdysis behavior. Development 2003; 130:2645–2656.PubMedCrossRefGoogle Scholar
  43. 43.
    Baker JD, McNabb SL, Truman JW. The hormonal coordination of behavior and physiology at adult ecdysis in Drosophila melanogaster. J Exp Biol 1999; 202:3037–3048.PubMedGoogle Scholar
  44. 44.
    Yoshii T, Heshiki Y, Ibuki-Ishibashi T et al. Temperature cycles drive Drosophila circadian oscillation in constant light that otherwise induces behavioural arrhythmicity. Eur J Neurosci 2005; 22:1176–1184.PubMedCrossRefGoogle Scholar
  45. 45.
    Wen T, Parrish CA, Xu D et al. Drosophila neuropeptide F and its receptor, NPFR1, define a signaling pathway that acutely modulates alcohol sensitivity. Proc Natl Acad Sci USA 2005; 102:2141–2146.PubMedCrossRefGoogle Scholar
  46. 46.
    Wu Q, Wen T, Lee G et al. Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system. Neuron 2003; 39:147–161.PubMedCrossRefGoogle Scholar
  47. 47.
    Meng X, Wahlstrom G, Immonen T et al. The Drosophila hugin gene codes for myostimulatory and ecdysis-modifying neuropeptides. Mech Dev 2002; 117:5–13.PubMedCrossRefGoogle Scholar
  48. 48.
    Taylor CA, Winther AM, Siviter RJ et al. Identification of a proctolin preprohormone gene (Proct) of Drosophila melanogaster: expression and predicted prohormone processing. J Neurobiol 2004; 58:379–391.PubMedCrossRefGoogle Scholar
  49. 49.
    Winther AM, Acebes A, Ferrus A. Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Mol Cell Neurosci 2006; 31:399–406.PubMedCrossRefGoogle Scholar
  50. 50.
    Gotz KG. Visual guidance in Drosophila. Basic Life Sci 1980; 16:391–407.PubMedGoogle Scholar
  51. 51.
    Lee KS, You KH, Choo JK et al. Drosophila short neuropeptide F regulates food intake and body size. J Biol Chem 2004; 279:50781–50789.PubMedCrossRefGoogle Scholar
  52. 52.
    Hammond SM, Bernstein E, Beach D et al. An RNA-directed nuclease mediates posttranscriptional gene silencing in Drosophila cells. Nature 2000; 404:293–296.PubMedCrossRefGoogle Scholar
  53. 53.
    Bernstein E, Caudy AA, Hammond SM et al. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001; 409:363–366.PubMedCrossRefGoogle Scholar
  54. 54.
    Breer H, Sattelle DB. Molecular properties and functions of insect acetylcholine receptors. J Insect Physiol 1987; 33:771–790.CrossRefGoogle Scholar
  55. 55.
    Rauh JJ, Lummis SC, Sattelle DB. Pharmacological and biochemical properties of insect GABA receptors. Trends Pharmacol Sci 1990; 11:325–329.PubMedCrossRefGoogle Scholar
  56. 56.
    Raymond-Delpech V, Matsuda K, Sattelle BM et al. Ion channels: molecular targets of neuroactive insecticides. Invert Neurosci 2005; 5:119–133.PubMedCrossRefGoogle Scholar
  57. 57.
    Kubiak TM, Larsen MJ, Burton KJ et al. Cloning and functional expression of the first Drosophila melanogaster sulfakinin receptor DSK-R1. Biochem Biophys Res Commun 2002; 291:313–320.PubMedCrossRefGoogle Scholar
  58. 58.
    Radford JC, Davies SA, Dow JAT. Systematic G-protein-coupled receptor analysis in Drosophila melanogaster identifies a leucokinin receptor with novel roles. J Biol Chem 2002; 277:38810–38817.PubMedCrossRefGoogle Scholar
  59. 59.
    Johnson EC, Bohn LM, Barak L et al. Identification of Drosophila neuropeptide receptors by G protein-coupled receptors-bèta-arrestin2 interactions. J Biol Chem 2003; 278:52172–52178.PubMedCrossRefGoogle Scholar
  60. 60.
    Birse RT, Johnson EC, Taghert PH et al. Widely distributed Drosophila G-protein-coupled receptor (CG7887) is activated by endogenous tachykinin-related peptides. J Neurobiol 2006; 66:33–46.PubMedCrossRefGoogle Scholar
  61. 61.
    Rosenkilde C, Cazzamali G, Williamson M et al. Molecular cloning, functional expression and gene silencing of two Drosophila receptors for the Drosophila neuropeptide pyrokinin-2. Biochem Biophys Res Commun 2003; 309:485–494.PubMedCrossRefGoogle Scholar
  62. 62.
    Jorgensen LM, Hauser F, Cazzamali G et al. Molecular identification of the first SIFamide receptor. Biochem Biophys Res Commun 2006; 340:696–701.PubMedCrossRefGoogle Scholar
  63. 63.
    Garczynski SF, Brown MR, Shen P et al. Characterization of a functional neuropeptide F receptor from Drosophila melanogaster. Peptides 2002; 23:773–780.PubMedCrossRefGoogle Scholar
  64. 64.
    Feng GP, Reale V, Chatwin H et al. Functional characterization of a neuropeptide F-like receptor from Drosophila melanogaster. Eur J Neurosci 2003; 18:227–238.PubMedCrossRefGoogle Scholar
  65. 65.
    Mertens I, Meeusen T, Huybrechts R et al. Characterization of the short neuropeptide F receptor from Drosophila melanogaster. Biochem Biophys Res Commun 2002; 297:1140–1148.PubMedCrossRefGoogle Scholar
  66. 66.
    Meeusen T, Mertens I, Clynen E et al. Identification in Drosophila melanogaster of the invertebrate G protein-coupled FMRFamide receptor. Proc Natl Acad Sci USA 2002; 99:15363–15368.PubMedCrossRefGoogle Scholar
  67. 67.
    Iversen A, Cazzamali G, Williamson M et al. Molecular cloning and functional expression of a Drosophila receptor for the neuropeptides capa-1 and-2. Biochem Biophys Res Commun 2002; 299:628–633.PubMedCrossRefGoogle Scholar
  68. 68.
    Park Y, Kim YJ, Adams ME. Identification of G protein-coupled receptors for Drosophila PRXamide peptides, CCAP, corazonin and AKH supports a theory of ligand-receptor co-evolution. Proc Natl Acad Sci USA 2002; 99:11423–11428.PubMedCrossRefGoogle Scholar
  69. 69.
    Iversen A, Cazzamali G, Williamson M et al. Molecular identification of the first insect ecdysis triggering hormone receptors. Biochem Biophys Res Commun 2002; 299:924–931.PubMedCrossRefGoogle Scholar
  70. 70.
    Johnson EC, Garczynski SF, Park D et al. Identification and characterization of a G protein-coupled receptor for the neuropeptide proctolin in Drosophila melanogaster. Proc Natl Acad Sci USA 2003; 100:6198–6203.PubMedCrossRefGoogle Scholar
  71. 71.
    Egerod K, Reynisson E, Hauser F et al. Molecular cloning and functional expression of the first two specific insect myosuppressin receptors. Proc Natl Acad Sci USA 2003; 100:9808–9813.PubMedCrossRefGoogle Scholar
  72. 72.
    Cazzamali G, Torp M, Hauser F et al. The Drosophila gene CG9918 codes for a pyrokinin-1 receptor. Biochem Biophys Res Commun 2005; 335:14–19.PubMedCrossRefGoogle Scholar
  73. 73.
    Birgul N, Weise C, Kreienkamp HJ et al. Reverse physiology in Drosophila: identification of a novel allatostatin-like neuropeptide and its cognate receptor structurally related to the mammalian somatostatin/ galanin/opioid receptor family. EMBO J 1999; 18:5892–5900.PubMedCrossRefGoogle Scholar
  74. 74.
    Larsen MJ, Burton KJ, Zantello MR et al. Type A allatostatins from Drosophila melanogaster and Diplotera puncata activate two Drosophila allatostatin receptors, DAR-1 and DAR-2, expressed in CHO cells. Biochem Biophys Res Commun 2001; 286:895–901.PubMedCrossRefGoogle Scholar
  75. 75.
    Kreienkamp HJ, Larusson HJ, Witte I et al. Functional annotation of two orphan G-protein-coupled receptors, Drostar1 and-2, from Drosophila melanogaster and their ligands by reverse pharmacology. Journal of Biological Chemistry 2002; 277:39937–39943.PubMedCrossRefGoogle Scholar
  76. 76.
    Staubli F, Jorgensen TJD, Cazzamali G et al. Molecular identification of the insect adipokinetic hormone receptors. Proc Natl Acad Sci USA 2002; 99:3446–3451.PubMedCrossRefGoogle Scholar
  77. 77.
    Cazzamali G, Saxild NPE, Grimmelikhuijzen CJP. Molecular cloning and functional expression of a Drosophila corazonin receptor. Biochem Biophys Res Commun 2002; 298:31–36.PubMedCrossRefGoogle Scholar
  78. 78.
    Cazzamali G, Hauser F, Kobberup S et al. Molecular identification of a Drosophila G protein-coupled receptor specific for crustacean cardioactive peptide. Biochem Biophys Res Commun 2003; 303:146–152.PubMedCrossRefGoogle Scholar
  79. 79.
    Mendive FM, Van Loy T, Claeysen S et al. Drosophila molting neurohormone bursicon is a heterodimer and the natural agonist of the orphan receptor DLGR2. Febs Letters 2005; 579:2171–2176.PubMedCrossRefGoogle Scholar
  80. 80.
    Luo CW, Dewey EM, Sudo S et al. Bursicon, the insect cuticle-hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2. Proc Natl Acad Sci USA 2005; 102:2820–2825.PubMedCrossRefGoogle Scholar
  81. 81.
    Sudo S, Kuwabara Y, Park JI et al. Heterodimeric fly glycoprotein hormone-alpha 2 (GPA2) and glycoprotein hormone-beta 5 (GPB5) activate fly leucine-rich repeat-containing G protein-coupled receptor-1 (DLGR1) and stimulation of human thyrotropin receptors by chimeric fly GPA2 and human GPB5. Endocrinology 2005; 146:3596–3604.PubMedCrossRefGoogle Scholar
  82. 82.
    Johnson EC, Bohn LM, Taghert PH. Drosophila CG8422 encodes a functional diuretic hormone receptor. J Exp Biol 2004; 207:743–748.PubMedCrossRefGoogle Scholar
  83. 83.
    Mertens I, Vandingenen A, Johnson EC et al. PDF receptor signalling in Drosophila contributes to both circadian and geotaxic behaviors. Neuron 2005.Google Scholar
  84. 84.
    Lear BC, Merrill CE, Lin JM et al. A G protein-coupled receptor, groom-of-PDF, is required for PDF neuron action in circadian behavior. Neuron 2005; 48:221–227.PubMedCrossRefGoogle Scholar
  85. 85.
    Hyun S, Lee Y, Hong ST et al. Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron 2005; 48:267–278.PubMedCrossRefGoogle Scholar
  86. 86.
    Johnson EC, Shafer OT, Trigg JS et al. A novel diuretic hormone receptor in Drosophila: evidence for conservation of CGRP signaling. J Exp Biol 2005; 208:1239–1246.PubMedCrossRefGoogle Scholar
  87. 87.
    Cvejic S, Zhu Z, Felice SJ et al. The endogenous ligand Stunted of the GPCR Methuselah extends lifespan in Drosophila. Nat Cell Biol 2004; Epub.Google Scholar
  88. 88.
    Rorth P. A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc Natl Acad Sci USA 1996; 93:12418–12422.PubMedCrossRefGoogle Scholar
  89. 89.
    Staudt N, Molitor A, Somogyi K et al. Gain-of-function screen for genes that affect Drosophila muscle pattern formation. PLoS Genet 2005; 1:e55.PubMedCrossRefGoogle Scholar
  90. 90.
    Roseman RR, Johnson EA, Rodesch CK et al. A P element containing suppressor of hairy-wing binding regions has novel properties for mutagenesis in Drosophila melanogaster. Genetics 1995; 141:1061–1074.PubMedGoogle Scholar
  91. 91.
    Bellen HJ, Levis RW, Liao G et al. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 2004; 167:761–781.PubMedCrossRefGoogle Scholar
  92. 92.
    Lukacsovich T, Asztalos Z, Awano W et al. Dual-tagging gene trap of novel genes in Drosophila melanogaster. Genetics 2001; 157:727–742.PubMedGoogle Scholar
  93. 93.
    Bier E, Vaessin H, Shepherd S et al. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev 1989; 3:1273–1287.PubMedCrossRefGoogle Scholar
  94. 94.
    Torok T, Tick G, Alvarado M et al. P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes. Genetics 1993; 135:71–80.PubMedGoogle Scholar
  95. 95.
    Beinert N, Werner M, Dowe G et al. Systematic gene targeting on the X chromosome of Drosophila melanogaster. Chromosoma 2004; 113:271–275.PubMedCrossRefGoogle Scholar
  96. 96.
    Mlodzik M, Hiromi Y. Enhancer trap method in Drosophila: its application to neurobiology. 1992; 397–414.Google Scholar
  97. 97.
    Thibault ST, Singer MA, Miyazaki WY et al. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 2004; 36:283–287.PubMedCrossRefGoogle Scholar
  98. 98.
    Huet F, Lu JT, Myrick KV et al. A deletion-generator compound element allows deletion saturation analysis for genomewide phenotypic annotation. Proc Natl Acad Sci USA 2002; 99:9948–9953.PubMedCrossRefGoogle Scholar
  99. 99.
    Golic KG, Golic MM. Engineering the Drosophila genome: chromosome rearrangements by design. Genetics 1996; 144:1693–1711.PubMedGoogle Scholar
  100. 100.
    Deak P, Omar MM, Saunders RD et al. P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster: correlation of physical and cytogenetic maps in chromosomal region 86E–87F. Genetics 1997; 147:1697–1722.PubMedGoogle Scholar
  101. 101.
    Bellotto M, Bopp D, Senti KA et al. Maternal-effect loci involved in Drosophila oogenesis and embryogenesis: P element-induced mutations on the third chromosome. Int J Dev Biol 2002; 46:149–157.PubMedGoogle Scholar
  102. 102.
    Oh SW, Kingsley T, Shin HH et al. A P-element insertion screen identified mutations in 455 novel essential genes in Drosophila. Genetics 2003; 163:195–201.PubMedGoogle Scholar
  103. 103.
    Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 118:401–415.PubMedGoogle Scholar
  104. 104.
    Toba G, Ohsako T, Miyata N et al. The gene search system. A method for efficient detection and rapid molecular identification of genes in Drosophila melanogaster. Genetics 1999; 151:725–737.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  • Elke Clynen
    • 2
  • Ank Reumer
    • 2
  • Geert Baggerman
    • 2
  • Inge Mertens
    • 2
  • Liliane Schoofs
    • 1
  1. 1.Department of Animal Physiology and NeurobiologyK.U. LeuvenLeuvenBelgium
  2. 2.Research Unit Functional Genomics and ProteomicsKatholieke Universitet LeuvenLeuvenBelgium

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