Gain-of-Function Screen Identifies a Role of the Src64 Oncogene in Drosophila Mushroom Body Development

Journal of Neurobiology

Volumn 57, Issue 3, 2003, Pages 291-302

  Nicolaï, Maryse ^a,b   Lasbleiz, Christelle ^a   Dura, Jean Maurice ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

^b IRFM   (France)

Author keywords

Brain development; Drosophila; Gain of function screen; Mushroom body; Src64

Indexed keywords

AXON GUIDANCE RECEPTOR; GREEN FLUORESCENT PROTEIN; MICROTUBULE SEVERING PROTEIN; PROTEIN; PROTEIN SRC64; PROTEIN TYROSINE KINASE; RECEPTOR; RNA BINDING PROTEIN; TRAMTRACK TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VESICLE TRAFFICKING PROTEIN;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOLOGY; DROSOPHILA; GENE EXPRESSION; GENE IDENTIFICATION; GENE TARGETING; GENETIC REGULATION; MUSHROOM; MUSHROOM BODY; NERVE CELL; NONHUMAN; ONCOGENE SRC; OPEN READING FRAME; PHENOTYPE; PHYSICAL DEVELOPMENT; PRIORITY JOURNAL;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; GENES, INSECT; MICROSCOPY, CONFOCAL; MUSHROOM BODIES; MUTATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS;

EID: 0242468792     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10277     Document Type: Article

References (63)

1. Abdelilah-Seyfried S, Chan YM, Zeng C, Justice NJ, Younger-Shepherd S, Sharp LE, Barbel S, Meadows SA, Jan LY, Jan YN. 2000. A gain-of-function screen for genes that affect the development of the Drosophila adult external sensory organ. Genetics 155:733-752.
2. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Gabor GL, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J, Brokstein P, Brottier P, Burtis KC, Busam DA, Butler H, Cadieu E, Center A, Chandra I, Cherry JM, Cawley S, Dahlke C, Davenport LB, Davies P, de Pablos B, Delcher A, Deng Z, Mays AD, Dew I, Dietz SM, Dodson K, Doup LE, Downes M, Dugan-Rocha S, Dunkov BC, Dunn P, Durbin KJ, Evangelista CC, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian AE, Garg NS, Gelbart WM, Glasser K, Glodek A, Gong F, Gorrell JH, Gu Z, Guan P, Harris M, Harris NL, Harvey D, Heiman TJ, Hernandez JR, Houck J, Hostin D, Houston KA, Howland TJ, Wei MH, Ibegwam C, et al. 2000. The genome sequence of Drosophila melanogaster. Science 287:2185-2195.
3. Awasaki T, Saito M, Sone M, Suzuki E, Sakai R, Ito K, Hama C. 2000. The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 26:119-131.
4. Billuart P, Winter CG, Maresh A, Zhao X, Luo L. 2001. Regulating axon branch stability: the role of p190 RhoGAP in repressing a retraction signaling pathway. Cell 107:195-207.
5. Blume-Jensen P, Hunter T. 2001. Oncogenic kinase signalling. Nature 411:355-365.
6. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
7. Cheng Y, Endo K, Wu K, Rodan AR, Heberlein U, Davis RL. 2001. Drosophila fasciclin II is required for the formation of odor memories and for normal sensitivity to alcohol. Cell 105:757-768.
8. Clark IE, Dobi KC, Duchow HK, Vlasak AN, Gavis ER. 2002. A common translational control mechanism functions in axial patterning and neuroendocrine signaling in Drosophila. Development 129:3325-3334.
9. Connolly JB, Roberts IJ, Armstrong JD, Kaiser K, Forte M, Tully T, O'Kane CJ. 1996. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274:2104-2107.
10. Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL. 1998. Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5:38-51.
11. Davis RL. 1996. Physiology and biochemistry of Drosophila learning mutants. Physiol Rev 76:299-317.
12. de Belle JS, Heisenberg M. 1994. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692-695.
13. Dean KA, Aggarwal AK, Wharton RP. 2002. Translational repressors in Drosophila. Trends Genet 18:572-577.
14. Dodson GS, Guarnieri DJ, Simon MA. 1998. Src64 is required for ovarian ring canal morphogenesis during Drosophila oogenesis. Development 125:2883-2892.
15. Dubnau J, Chiang AS, Grady L, Barditch J, Gossweiler S, McNeil J, Smith P, Buldoc F, Scott R, Certa U, Broger C, Tully T. 2003. The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr Biol 13:286-296.
16. Dura JM, Preat T, Tully T. 1993. Identification of linotte, a new gene affecting learning and memory in Drosophila melanogaster. J Neurogenet 9:1-14.
17. Fauvarque MO, Dura JM. 1993. Polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila. Genes Dev 7:1508-1520.
18. Gavis ER. 2001. Over the rainbow to translational control. Nat Struct Biol 8:387-389.
19. Giesen K, Hummel T, Stollewerk A, Harrison S, Travers A, Klambt C. 1997. Glial development in the Drosophila CNS requires concomitant activation of glial and repression of neuronal differentiation genes. Development 124:2307-2316.
20. Guan Z, Prado A, Melzig J, Heisenberg M, Nash HA, Raabe T. 2000. Mushroom body defect, a gene involved in the control of neuroblast proliferation in Drosophila, encodes a coiled-coil protein. Proc Natl Acad Sci USA 97:8122-8127.
21. Guichet A, Wucherpfennig T, Dudu V, Etter S, Wilsch-Brauniger M, Hellwig A, Gonzalez-Gaitan M, Huttner WB, Schmidt AA. 2002. Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction. EMBO J 21:1661-1672.
22. Heisenberg M. 1998. What do the mushroom bodies do for the insect brain? An introduction. Learn Mem 5:1-10.
23. Heisenberg M, Borst A, Wagner S, Byers D. 1985. Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1-30.
24. Hitier R, Chaminade M, Preat T. 2001. The Drosophila castor gene is involved in postembryonic brain development. Mech Dev 103:3-11.
25. Huang AM, Rubin GM. 2000. A misexpression screen identifies genes that can modulate RAS1 pathway signaling in Drosophila melanogaster. Genetics 156:1219-1230.
26. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D. 1997. The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124:761-771.
27. Jauch E, Melzig J, Brkulj M, Raabe T. 2002. In vivo functional analysis of Drosophila protein kinase casein kinase 2 (CK2) beta-subunit. Gene 298:29-39.
28. Kraut R, Menon K, Zinn K. 2001. A gain-of-function screen for genes controlling motor axon guidance and synaptogenesis in Drosophila. Curr Biol 11:417-430.
29. Kurusu M, Nagao T, Walldorf U, Flister S, Gehring WJ, Furukubo-Tokunaga K. 2000. Genetic control of development of the mushroom bodies, the associative learning centers in the Drosophila brain, by the eyeless, twin of eyeless, and Dachshund genes. Proc Natl Acad Sci USA 97:2140-2144.
30. Kurusu M, Awasaki T, Masuda-Nakagawa LM, Kawauchi H, Ito K, Furukubo-Tokunaga K. 2002. Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. Development 129:409-419.
31. Kussick SJ, Basler K, Cooper JA. 1993. Ras1-dependent signaling by ectopically-expressed Drosophila src gene product in the embryo and developing eye. Oncogene 8:2791-2803.
32. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
33. Lee T, Lee A, Luo L. 1999. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126:4065-4076.
34. Lee T, Marticke S, Sung C, Robinow S, Luo L. 2000a. Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 28:807-818.
35. Lee T, Winter C, Marticke SS, Lee A, Luo L. 2000b. Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25:307-316.
36. Lindsley DL, Zimm GG. 1992. The genome of Drosophila melanogaster. San Diego: Academic Press. 1133 p.
37. Liu L, Wolf R, Ernst R, Heisenberg M. 1999. Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 400:753-756.
38. Liu Z, Steward R, Luo L. 2000. Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration and axonal transport. Nat Cell Biol 2:776-783.
39. Martini SR, Roman G, Meuser S, Mardon G, Davis RL. 2000. The retinal determination gene, dachshund, is required for mushroom body cell differentiation. Development 127:2663-2672.
40. McBride SM, Giuliani G, Choi C, Krause P, Correale D, Watson K, Baker G, Siwicki KK. 1999. Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 24:967-977.
41. Melzig J, Rein KH, Schafer U, Pfister H, Jackle H, Heisenberg M, Raabe T. 1998. A protein related to p21-activated kinase (PAK) that is involved in neurogenesis in the Drosophila adult central nervous system. Curr Biol 8:1223-1226.
42. Monnier V, Girardot F, Cheret C, Andres O, Tricoire H. 2002. Modulation of oxidative stress resistance in Drosophila melanogaster by gene overexpression. Genesis 34:76-79.
43. Moreau-Fauvarque C, Taillebourg E, Boissoneau E, Mesnard J, Dura JM. 1998. The receptor tyrosine kinase gene linotte is required for neuronal pathway selection in the Drosophila mushroom bodies. Mech Dev 78:47-61.
44. Moreau-Fauvarque C, Taillebourg E, Preat T, Dura JM. 2002. Mutation of linotte causes behavioral defects independently of pigeon in Drosophila. Neuroreport 13:1-4.
45. Ng J, Nardine T, Harms M, Tzu J, Goldstein A, Sun Y, Dietzl G, Dickson BJ, Luo L. 2002. Rac GTPases control axon growth, guidance and branching. Nature 416:442-447.
46. Noveen A, Daniel A, Hartenstein V. 2000. Early development of the Drosophila mushroom body: the roles of eyeless and dachshund. Development 127:3475-3488.
47. Pascual A, Preat T. 2001. Localization of long-term memory within the Drosophila mushroom body. Science 294:1115-1117.
48. Reuter JE, Nardine TM, Penton A, Billuart P, Scott EK, Usui T, Uemura T, Luo L. 2003. A mosaic genetic screen for genes necessary for Drosophila mushroom body neuronal morphogenesis. Development 130:1203-1213.
49. Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz DM, Benz WK, Engels WR. 1988. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118:461-470.
50. Rorth P. 1996. A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc Natl Acad Sci USA 93:12418-12422.
51. Rorth P, Szabo K, Bailey A, Laverty T, Rehm J, Rubin GM, Weigmann K, Milan M, Benes V, Ansorge W, Cohen SM. 1998. Systematic gain-of-function genetics in Drosophila. Development 125:1049-1057.
52. Scott EK, Lee T, Luo L. 2001. Enok encodes a Drosophila putative histone acetyltransferase required for mushroom body neuroblast proliferation. Curr Biol 11:99-104.
53. Simon AF, Boquet I, Synguelakis M, Preat T. 1998. The Drosophila putative kinase linotte (derailed) prevents central brain axons from converging on a newly described interhemispheric ring. Mech Dev 76:45-55.
54. Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K. 1998. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11-37.
55. Tettamanti M, Armstrong JD, Endo K, Yang MY, Furukubo-Tokunaga K, Kaiser K, Reichert H. 1997. Early development of the Drosophila mushroom bodies, brain centres for associative learning and memory. Dev Genes Evol 207:242-252.
56. Thomas SM, Brugge JS. 1997. Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13:513-609.
57. Van De Bor V, Giangrande A. 2002. Glide/gcm: at the crossroads between neurons and glia. Curr Opin Genet Dev 12:465-472.
58. Wang J, Zugates CT, Liang IH, Lee CH, Lee T. 2002. Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 33:559-571.
59. Wharton RP, Sonoda J, Lee T, Patterson M, Murata Y. 1998. The Pumilio RNA-binding domain is also a translational regulator. Mol Cell 1:863-872.
60. Wills Z, Bateman J, Korey CA, Comer A, Van Vactor D. 1999. The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 22:301-312.
61. Winberg ML, Noordermeer JN, Tamagnone L, Comoglio PM, Spriggs MK, Tessier-Lavigne M, Goodman CS. 1998. Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95:903-916.
62. Yang MY, Armstrong JD, Vilinsky I, Strausfeld NJ, Kaiser K. 1995. Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15:45-54.
63. Zhao W, Cavallaro S, Gusev P, Alkon DL. 2000. Nonreceptor tyrosine protein kinase pp60c-src in spatial learning: synapse-specific changes in its gene expression, tyrosine phosphorylation, and protein-protein interactions. Proc Natl Acad Sci USA 97:8098-8103.