A modifier screen in the Drosophila eye reveals that aPKC interacts with Glued during central synapse formation

BMC Genetics

Volumn 10, Issue , 2009, Pages

  Ma, Lisha ^a   Johns, Louise A ^a   Allen, Marcus J ^a  

^a UNIVERSITY OF KENT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; GLUE PROTEIN; PROTEIN KINASE C; DROSOPHILA PROTEIN; GLUED PROTEIN, DROSOPHILA; MICROTUBULE ASSOCIATED PROTEIN; PKC 3 PROTEIN; PKC-3 PROTEIN; REPRESSOR PROTEIN; SUPPRESSOR OF HAIRLESS PROTEIN, DROSOPHILA;

ANIMAL TISSUE; ARTICLE; CELL POLARITY; CHROMOSOME; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE FREQUENCY; GENE LOCUS; GENE MAPPING; GENE MUTATION; GENE OVEREXPRESSION; GENETIC SCREENING; MOTONEURON; NERVE FIBER; NONHUMAN; PHENOTYPE; PROTEIN PROTEIN INTERACTION; SYNAPSE; SYNAPTOGENESIS; ANIMAL; CYTOLOGY; EYE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MUTATION;

DROSOPHILA MELANOGASTER; VERTEBRATA;

ANIMALS; CELL POLARITY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; FEMALE; GENE EXPRESSION REGULATION; GENETIC TESTING; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; PHENOTYPE; PROTEIN KINASE C; REPRESSOR PROTEINS; SYNAPSES;

EID: 71649104478     PISSN: None     EISSN: 14712156     Source Type: Journal    
DOI: 10.1186/1471-2156-10-77     Document Type: Article

References (68)

1. Davis GW. The making of a synapse: Target-derived signals and presynaptic differentiation. Neuron 2000, 26(3):551-554. 10.1016/S0896-6273(00)81190-3, 10896150.
2. Jin Y, Garner CC. Molecular mechanisms of presynaptic differentiation. Annu Rev Cell Dev Biol 2008, 24:237-262. 10.1146/annurev.cellbio.23.090506.123417, 18588488.
3. Allen MJ, Godenschwege TA, Tanouye MA, Phelan P. Making an escape: development and function of the Drosophila giant fibre system. Semin Cell Dev Biol 2006, 17(1):31-41. 10.1016/j.semcdb.2005.11.011, 16378740.
4. Godenschwege TA, Hu H, Shan-Crofts X, Goodman CS, Murphey RK. Bi-directional signaling by Semaphorin 1a during central synapse formation in Drosophila. Nat Neurosci 2002, 5(12):1294-1301. 10.1038/nn976, 12436113.
5. Godenschwege TA, Simpson JH, Shan X, Bashaw GJ, Goodman CS, Murphey RK. Ectopic expression in the giant fiber system of Drosophila reveals distinct roles for roundabout (Robo), Robo2, and Robo3 in dendritic guidance and synaptic connectivity. J Neurosci 2002, 22(8):3117-3129.
6. Godenschwege TA, Kristiansen LV, Uthaman SB, Hortsch M, Murphey RK. A conserved role for Drosophila Neuroglian and human L1-CAM in central-synapse formation. Curr Biol 2006, 16(1):12-23. 10.1016/j.cub.2005.11.062, 16401420.
7. Muralidhar MG, Thomas JB. The Drosophila Bendless Gene Encodes a Neural Protein Related to Ubiquitin-Conjugating Enzymes. Neuron 1993, 11(2):253-266. 10.1016/0896-6273(93)90182-Q, 8394720.
8. Murphey RK, Froggett SJ, Caruccio P, Shan-Crofts X, Kitamoto T, Godenschwege TA. Targeted expression of shibire ts and semaphorin 1a reveals critical periods for synapse formation in the giant fiber of Drosophila. Development 2003, 130(16):3671-3682. 10.1242/dev.00598, 12835384.
9. Oh CE, McMahon R, Benzer S, Tanouye MA. Bendless, a Drosophila Gene Affecting Neuronal Connectivity, Encodes a Ubiquitin-Conjugating Enzyme Homolog. Journal Of Neuroscience 1994, 14(5 Pt 2):3166-3179.
10. Uthaman SB, Godenschwege TA, Murphey RK. A mechanism distinct from highwire for the Drosophila ubiquitin conjugase bendless in synaptic growth and maturation. J Neurosci 2008, 28(34):8615-8623. 10.1523/JNEUROSCI.2990-08.2008, 18716220.
11. Allen MJ, Shan X, Murphey RK. A role for Drosophila Drac1 in neurite outgrowth and synaptogenesis in the giant fiber system. Mol Cell Neurosci 2000, 16(6):754-765. 10.1006/mcne.2000.0903, 11124895.
12. Allen MJ, Drummond JA, Sweetman DJ, Moffat KG. Analysis of two P-element enhancer-trap insertion lines that show expression in the giant fibre neuron of Drosophila melanogaster. Genes Brain Behav 2007, 6(4):347-358. 10.1111/j.1601-183X.2006.00263.x, 16879616.
13. Schroer TA. Dynactin. Annu Rev Cell Dev Biol 2004, 20:759-779. 10.1146/annurev.cellbio.20.012103.094623, 15473859.
14. Watermanstorer CM, Holzbaur ELF. The Product Of the Drosophila Gene, Glued, Is the Functional Homolog Of the P150(Glued) Component Of the Vertebrate Dynactin Complex. Journal Of Biological Chemistry 1996, 271(2):1153-1159. 10.1074/jbc.271.2.1153, 8557644.
15. Swaroop A, Paco-Larson ML, Garen A. Molecular genetics of a transposon-induced dominant mutation in the Drosophila locus Glued. Proc Natl Acad Sci USA 1985, 82(6):1751-1755. 397350, 2984667, 10.1073/pnas.82.6.1751.
16. McGrail M, Gepner J, Silvanovich A, Ludmann S, Serr M, Hays TS. Regulation Of Cytoplasmic Dynein Function In-Vivo By the Drosophila Glued Complex. Journal Of Cell Biology 1995, 131(2):411-425. 2199972, 7593168, 10.1083/jcb.131.2.411.
17. Fan SS, Ready DF. Glued participates in distinct microtubule-based activities in Drosophila eye development. Development 1997, 124(8):1497-1507.
18. Murphey RK, Caruccio PC, Getzinger M, Westgate PJ, Phillis RW. Dynein-dynactin function and sensory axon growth during Drosophila metamorphosis: A role for retrograde motors. Dev Biol 1999, 209(1):86-97. 10.1006/dbio.1999.9217, 10208745.
19. Reddy S, Jin P, Trimarchi J, Caruccio P, Phillis R, Murphey RK. Mutant molecular motors disrupt neural circuits in Drosophila. J Neurobiol 1997, 33(6):711-723. 10.1002/(SICI)1097-4695(19971120)33:6<711::AID-NEU1>3.0.CO;2-C, 9369146.
20. Allen MJ, Shan X, Caruccio P, Froggett SJ, Moffat KG, Murphey RK. Targeted expression of truncated glued disrupts giant fiber synapse formation in Drosophila. J Neurosci 1999, 19(21):9374-9384.
21. Reuter JE, Nardine TM, Penton A, Billuart P, Scott EK, Usui T, Uemura T, Luo L. A mosaic genetic screen for genes necessary for Drosophila mushroom body neuronal morphogenesis. Development 2003, 130(6):1203-1213. 10.1242/dev.00319, 12571111.
22. Karim FD, Chang HC, Therrien M, Wassarman DA, Laverty T, Rubin GM. A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetics 1996, 143(1):315-329. 1207264, 8722784.
23. Carrera P, Abrell S, Kerber B, Walldorf U, Preiss A, Hoch M, Jackle H. A modifier screen in the eye reveals control genes for Kruppel activity in the Drosophila embryo. Proc Natl Acad Sci USA 1998, 95(18):10779-10784. 27972, 9724781, 10.1073/pnas.95.18.10779.
24. Mahoney MB, Parks AL, Ruddy DA, Tiong SY, Esengil H, Phan AC, Philandrinos P, Winter CG, Chatterjee R, Huppert K. Presenilin-based genetic screens in Drosophila melanogaster identify novel notch pathway modifiers. Genetics 2006, 172(4):2309-2324. 1456381, 16415372, 10.1534/genetics.104.035170.
25. Thomas BJ, Wassarman DA. A fly's eye view of biology. Trends Genet 1999, 15(5):184-190. 10.1016/S0168-9525(99)01720-5, 10322485.
26. Thaker HM, Kankel DR. Mosaic analysis gives an estimate of the extent of genomic involvement in the development of the visual system in Drosophila melanogaster. Genetics 1992, 131(4):883-894. 1205099, 1516819.
27. Harte PJ, Kankel DR. Genetic-Analysis Of Mutations At the Glued Locus and Interacting Loci In Drosophila-Melanogaster. Genetics 1982, 101(3-4):477-501. 1201873, 6816671.
28. Brand AH, Perrimon N. Targeted Gene-Expression As a Means Of Altering Cell Fates and Generating Dominant Phenotypes. Development 1993, 118(2):401-415.
29. Kramer JM, Staveley BE. GAL4 causes developmental defects and apoptosis when expressed in the developing eye of Drosophila melanogaster. Genet Mol Res 2003, 2(1):43-47.
30. Blagburn JM, Alexopoulos H, Davies JA, Bacon JP. Null mutation in shaking-B eliminates electrical, but not chemical, synapses in the Drosophila giant fiber system: a structural study. J Comp Neurol 1999, 404(4):449-458. 10.1002/(SICI)1096-9861(19990222)404:4<449: AID-CNE3 3.0.CO;2-D, 9987990.
31. Jacobs K, Todman MG, Allen MJ, Davies JA, Bacon JP. Synaptogenesis in the giant-fibre system of Drosophila: interaction of the giant fibre and its major motorneuronal target. Development 2000, 127(23):5203-5212.
32. Koto M, Tanouye MA, Ferrus A, Thomas JB, Wyman RJ. The Morphology Of the Cervical Giant Fiber Neuron Of Drosophila. Brain Research 1981, 221(2):213-217. 10.1016/0006-8993(81)90772-1, 6793208.
33. Phelan P, Nakagawa M, Wilkin MB, Moffat KG, O'Kane CJ, Davies JA, Bacon JP. Mutations in shaking-B prevent electrical synapse formation in the Drosophila giant fiber system. J Neurosci 1996, 16(3):1101-1113.
34. Harte PJ, Kankel DR. Analysis of visual system development in Drosophila melanogaster: mutations at the Glued locus. Dev Biol 1983, 99(1):88-102. 10.1016/0012-1606(83)90256-7, 6413280.
35. Whited JL, Cassell A, Brouillette M, Garrity PA. Dynactin is required to maintain nuclear position within postmitotic Drosophila photoreceptor neurons. Development 2004, 131(19):4677-4686. 2714772, 15329347, 10.1242/dev.01366.
36. Hoskins RA, Phan AC, Naeemuddin M, Mapa FA, Ruddy DA, Ryan JJ, Young LM, Wells T, Kopczynski C, Ellis MC. Single nucleotide polymorphism markers for genetic mapping in Drosophila melanogaster. Genome Res 2001, 11(6):1100-1113. 311062, 11381036, 10.1101/gr.GR-1780R.
37. Martin SG, Dobi KC, St Johnston D. A rapid method to map mutations in Drosophila. Genome Biol 2001, 2(9):RESEARCH0036. 56897, 11574055, 10.1186/gb-2001-2-9-research0036.
38. Chen D, Berger J, Fellner M, Suzuki T. FLYSNPdb: a high-density SNP database of Drosophila melanogaster. Nucleic acids research 2009, (37 Database):D567-570. 2686552, 18784187, 10.1093/nar/gkn583.
39. Ryder E, Blows F, Ashburner M, Bautista-Llacer R, Coulson D, Drummond J, Webster J, Gubb D, Gunton N, Johnson G. The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster. Genetics 2004, 167(2):797-813. 1470913, 15238529, 10.1534/genetics.104.026658.
40. Bellen HJ, Levis RW, Liao G, He Y, Carlson JW, Tsang G, Evans-Holm M, Hiesinger PR, Schulze KL, Rubin GM. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 2004, 167(2):761-781. 1470905, 15238527, 10.1534/genetics.104.026427.
41. Hacker U, Nystedt S, Barmchi MP, Horn C, Wimmer EA. piggyBac-based insertional mutagenesis in the presence of stably integrated P elements in Drosophila. Proc Natl Acad Sci USA 2003, 100(13):7720-7725. 164654, 12802016, 10.1073/pnas.1230526100.
42. Horn C, Offen N, Nystedt S, Hacker U, Wimmer EA. piggyBac-based insertional mutagenesis and enhancer detection as a tool for functional insect genomics. Genetics 2003, 163(2):647-661. 1462455, 12618403.
43. Schuldiner O, Berdnik D, Levy JM, Wu JS, Luginbuhl D, Gontang AC, Luo L. piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Developmental cell 2008, 14(2):227-238. 2268086, 18267091, 10.1016/j.devcel.2007.11.001.
44. Iyadurai SJ, Robinson JT, Ma L, He Y, Mische S, Li MG, Brown W, Guichard A, Bier E, Hays TS. Dynein and Star interact in EGFR signaling and ligand trafficking. Journal of cell science 2008, 121(Pt 16):2643-2651. 2633900, 18653542, 10.1242/jcs.027144.
45. McGrail M, Gepner J, Silvanovich A, Ludmann S, Serr M, Hays TS. Regulation of cytoplasmic dynein function in vivo by the Drosophila Glued complex. J Cell Biol 1995, 131(2):411-425. 2199972, 7593168, 10.1083/jcb.131.2.411.
46. Macara IG. Parsing the polarity code. Nature reviews 2004, 5(3):220-231. 10.1038/nrm1332, 14991002.
47. Wiggin GR, Fawcett JP, Pawson T. Polarity proteins in axon specification and synaptogenesis. Developmental cell 2005, 8(6):803-816. 10.1016/j.devcel.2005.05.007, 15935771.
48. Wodarz A. Molecular control of cell polarity and asymmetric cell division in Drosophila neuroblasts. Current opinion in cell biology 2005, 17(5):475-481. 10.1016/j.ceb.2005.08.005, 16099639.
49. Shi SH, Jan LY, Jan YN. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 2003, 112(1):63-75. 10.1016/S0092-8674(02)01249-7, 12526794.
50. Nishimura T, Kato K, Yamaguchi T, Fukata Y, Ohno S, Kaibuchi K. Role of the PAR-3-KIF3 complex in the establishment of neuronal polarity. Nature cell biology 2004, 6(4):328-334. 10.1038/ncb1118, 15048131.
51. Schwamborn JC, Puschel AW. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat Neurosci 2004, 7(9):923-929. 10.1038/nn1295, 15286792.
52. Rolls MM, Albertson R, Shih HP, Lee CY, Doe CQ. Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia. J Cell Biol 2003, 163(5):1089-1098. 2173607, 14657233, 10.1083/jcb.200306079.
53. Rolls MM, Doe CQ. Baz, Par-6 and aPKC are not required for axon or dendrite specification in Drosophila. Nat Neurosci 2004, 7(12):1293-1295. 10.1038/nn1346, 15543144.
54. Drier EA, Tello MK, Cowan M, Wu P, Blace N, Sacktor TC, Yin JC. Memory enhancement and formation by atypical PKM activity in Drosophila melanogaster. Nat Neurosci 2002, 5(4):316-324. 10.1038/nn820, 11914720.
55. Ruiz-Canada C, Ashley J, Moeckel-Cole S, Drier E, Yin J, Budnik V. New synaptic bouton formation is disrupted by misregulation of microtubule stability in aPKC mutants. Neuron 2004, 42(4):567-580. 10.1016/S0896-6273(04)00255-7, 15157419.
56. Etienne-Manneville S, Hall A. Cell polarity: Par6, aPKC and cytoskeletal crosstalk. Current opinion in cell biology 2003, 15(1):67-72. 10.1016/S0955-0674(02)00005-4, 12517706.
57. Suzuki A, Ohno S. The PAR-aPKC system: lessons in polarity. Journal of cell science 2006, 119(Pt 6):979-987. 10.1242/jcs.02898, 16525119.
58. Wodarz A. Establishing cell polarity in development. Nature cell biology 2002, 4(2):E39-44. 10.1038/ncb0202-e39, 11835058.
59. Cau J, Hall A. Cdc42 controls the polarity of the actin and microtubule cytoskeletons through two distinct signal transduction pathways. Journal of cell science 2005, 118(Pt 12):2579-2587. 10.1242/jcs.02385, 15928049.
60. Etienne-Manneville S, Hall A. Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 2003, 421(6924):753-756. 10.1038/nature01423, 12610628.
61. Harris TJ, Peifer M. aPKC controls microtubule organization to balance adherens junction symmetry and planar polarity during development. Developmental cell 2007, 12(5):727-738. 1950292, 17488624, 10.1016/j.devcel.2007.02.011.
62. Grabham PW, Seale GE, Bennecib M, Goldberg DJ, Vallee RB. Cytoplasmic dynein and LIS1 are required for microtubule advance during growth cone remodeling and fast axonal outgrowth. J Neurosci 2007, 27(21):5823-5834. 10.1523/JNEUROSCI.1135-07.2007, 17522326.
63. Zheng Y, Wildonger J, Ye B, Zhang Y, Kita A, Younger SH, Zimmerman S, Jan LY, Jan YN. Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nature cell biology 2008, 10(10):1172-1180. 2588425, 18758451, 10.1038/ncb1777.
64. Allen MJ, Drummond JA, Moffat KG. Development of the giant fiber neuron of Drosophila melanogaster. J Comp Neurol 1998, 397(4):519-531. 10.1002/(SICI)1096-9861(19980810)397:4<519::AID-CNE5>3.0.CO;2-4, 9699913.
65. Freeman M. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 1996, 87(4):651-660. 10.1016/S0092-8674(00)81385-9, 8929534.
66. Tanouye MA, Wyman RJ. Motor outputs of giant nerve fiber in Drosophila. J Neurophysiol 1980, 44(2):405-421.
67. Gorczyca M, Hall JC. Identification of a cholinergic synapse in the giant fiber pathway of Drosophila using conditional mutations of acetylcholine synthesis. J Neurogenet 1984, 1(4):289-313. 10.3109/01677068409107093, 6443123.
68. Parks AL, Cook KR, Belvin M, Dompe NA, Fawcett R, Huppert K, Tan LR, Winter CG, Bogart KP, Deal JE. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet 2004, 36(3):288-292. 10.1038/ng1312, 14981519.