Systematic identification of genes that regulate neuronal wiring in the Drosophila visual system

PLoS Genetics

Volumn 4, Issue 5, 2008, Pages

  Berger, Jürg ^a,b,g   Senti, Kirsten André ^c   Senti, Gabriele ^d   Newsome, Timothy P ^e   Åsling, Bengt ^f   Dickson, Barry J ^b   Suzuki, Takashi ^a,b  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c STOCKHOLM UNIVERSITY   (Sweden)

^d SÖDERTÖRN UNIVERSITY   (Sweden)

^e UNIVERSITY OF SYDNEY   (Australia)

^f ASTRAZENECA R AND D   (Sweden)

^g Roche Austria   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CYTOSKELETON; DROSOPHILA; GENE CONTROL; GENE IDENTIFICATION; GENE MAPPING; MOLECULAR CLONING; MUTAGENESIS; NERVE CELL NETWORK; NERVE FIBER TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; VISUAL SYSTEM; ANIMAL; GENETICS; METABOLISM; MUTATION; NERVE FIBER; NERVOUS SYSTEM; PHYSIOLOGY; RETINA;

DROSOPHILA PROTEIN;

ANIMALS; AXONS; CLONING, MOLECULAR; DROSOPHILA; DROSOPHILA PROTEINS; MUTATION; NERVOUS SYSTEM; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; RETINA;

EID: 44949194762     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000085     Document Type: Article

References (101)

1. Clandinin TR, Zipursky SL (2002) Making connections in the fly visual system. Neuron 35: 827-841.
2. Hiesinger PR, Zhai RG, Zhou Y, Koh TW, Mehta SQ, et al. (2006) Activity-independent prespecification of synaptic partners in the visual map of Drosophila. Curr Biol 16: 1835-1843.
3. Clandinin TR, Lee CH, Herman T, Lee RC, Yang AY, et al. (2001) Drosophila LAR regulates R1-R6 and R7 target specificity in the visual system. Neuron 32: 237-248.
4. Newsome TP, Asling B, Dickson BJ (2000) Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127: 851-860.
5. Martin KA, Poeck B, Roth H, Ebens AJ, Ballard LC, et al. (1995) Mutations disrupting neuronal connectivity in the Drosophila visual system. Neuron 14: 229-240.
6. Mast JD, Prakash S, Chen PL, Clandinin TR (2006) The mechanisms and molecules that connect photoreceptor axons to their targets in Drosophila. Semin Cell Dev Biol 17: 42-49.
7. Berger J, Suzuki T, Senti KA, Stubbs J, Schaffner G, et al. (2001) Genetic mapping with SNP markers in Drosophila. Nat Genet 29: 475-481.
8. Moses K, Rubin GM (1991) Glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev 5: 583-593.
9. Newsome TP, Schmidt S, Dietzl G, Keleman K, Asling B, et al. (2000) Trio combines with dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell 101: 283-294.
10. Senti KA, Usui T, Boucke K, Greber U, Uemura T, et al. (2003) Flamingo regulates R8 axon-axon and axon-target interactions in the Drosophila visual system. Curr Biol 13: 828-832.
11. Senti K, Keleman K, Eisenhaber F, Dickson BJ (2000) brakeless is required for lamina targeting of R1-R6 axons in the Drosophila visual system. Development 127: 2291-2301.
12. Maurel-Zaffran C, Suzuki T, Gahmon G, Treisman JE, Dickson BJ (2001) Cell-autonomous and -nonautonomous functions of LAR in R7 photoreceptor axon targeting. Neuron 32: 225-235.
13. Garrity PA, Lee CH, Salecker I, Robertson HC, Desai CJ, et al. (1999) Retinal axon target selection in Drosophila is regulated by a receptor protein tyrosine phosphatase. Neuron 22: 707-717.
14. Garrity PA, Rao Y, Salecker I, McGlade J, Pawson T, et al. (1996) Drosophila photoreceptor axon guidance and targeting requires the dreadlocks SH2/SH3 adapter protein. Cell 85: 639-650.
15. Lee CH, Herman T, Clandinin TR, Lee R, Zipursky SL (2001) N-cadherin regulates target specificity in the Drosophila visual system. Neuron 30: 437-450.
16. Lee RC, Clandinin TR, Lee CH, Chen PL, Meinertzhagen IA, et al. (2003) The protocadherin Flamingo is required for axon target selection in the Drosophila visual system. Nat Neurosci 6: 557-563.
17. Hing H, Xiao J, Harden N, Lim L, Zipursky SL (1999) Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell 97: 853-863.
18. Ruan W, Pang P, Rao Y (1999) The SH2/SH3 adaptor protein dock interacts with the Ste20-like kinase misshapen in controlling growth cone motility. Neuron 24: 595-605.
19. Rao Y, Pang P, Ruan W, Gunning D, Zipursky SL (2000) brakeless is required for photoreceptor growth-cone targeting in Drosophila. Proc Natl Acad Sci U S A 97: 5966-5971.
20. Tomasi T, Hakeda-Suzuki S, Ohler S, Schleiffer A, Suzuki T (2008) The Transmembrane Protein Golden Goal Regulates R8 Photoreceptor Axon-Axon and Axon-Target Interactions. Neuron, in press.
21. Harden N, Lee J, Loh HY, Ong YM, Tan I, et al. (1996) A Drosophila homolog of the Rac- and Cdc42-activated serine/threonine kinase PAK is a potential focal adhesion and focal complex protein that colocalizes with dynamic actin structures. Mol Cell Biol 16: 1896-1908.
22. Saxton WM, Hicks J, Goldstein LS, Raff EC (1991) Kinesin heavy chain is essential for viability and neuromuscular functions in Drosophila, but mutants show no defects in mitosis. Cell 64: 1093-1102.
23. Wills Z, Marr L, Zinn K, Goodman CS, Van Vactor D (1999) Profilin and the Abl tyrosine kinase are required for motor axon outgrowth in the Drosophila embryo. Neuron 22: 291-299.
24. 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.
25. Brenman JE, Gao FB, Jan LY, Jan YN (2001) Sequoia, a tramtrack-related zinc finger protein, functions as a pan-neural regulator for dendrite and axon morphogenesis in Drosophila. Dev Cell 1: 667-677.
26. Pack-Chung E, Kurshan PT, Dickman DK, Schwarz TL (2007) A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport. Nat Neurosci 10: 980-989.
27. Hakeda-Suzuki S, Ng J, Tzu J, Dietzl G, Sun Y, et al. (2002) Rac function and regulation during Drosophila development. Nature 416: 438-442.
28. Awasaki T, Saito M, Sone M, Suzuki E, Sakai R, et al. (2000) The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 26: 119-131.
29. Liebl EC, Forsthoefel DJ, Franco LS, Sample SH, Hess JE, et al. (2000) Dosage-sensitive, reciprocal genetic interactions between the Abl tyrosine kinase and the putative GEF trio reveal trio's role in axon pathfinding. Neuron 26: 107-118.
30. Bateman J, Shu H, Van Vactor D (2000) The guanine nucleotide exchange factor trio mediates axonal development in the Drosophila embryo. Neuron 26: 93-106.
31. Mizuno T, Tsutsui K, Nishida Y (2002) Drosophila myosin phosphatase and its role in dorsal closure. Development 129: 1215-1223.
32. Tan C, Stronach B, Perrimon N (2003) Roles of myosin phosphatase during Drosophila development. Development 130: 671-681.
33. Lee A, Treisman JE (2004) Excessive Myosin activity in mbs mutants causes photoreceptor movement out of the Drosophila eye disc epithelium. Mol Biol Cell 15: 3285-3295.
34. Steneberg P, Englund C, Kronhamn J, Weaver TA, Samakovlis C (1998) Translational readthrough in the hdc mRNA generates a novel branching inhibitor in the drosophila trachea. Genes Dev 12: 956-967.
35. Makino N, Yamato T, Inoue H, Furukawa T, Abe T, et al. (2001) Isolation and characterization of the human gene homologous to the Drosophila headcase (hdc) gene in chromosome bands 6q23-q24, a region of common deletion in human pancreatic cancer. DNA Seq 11: 547-553.
36. Weaver TA, White RA (1995) headcase, an imaginal specific gene required for adult morphogenesis in Drosophila melanogaster. Development 121: 4149-4160.
37. Chien CC, Chang CC, Yang SH, Chen SH, Huang CJ (2006) A homologue of the Drosophila headcase protein is a novel tumor marker for early-stage colorectal cancer. Oncol Rep 15: 919-926.
38. Bai J, Uehara Y, Montell DJ (2000) Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 103: 1047-1058.
39. Anzick SL, Kononen J, Walker RL, Azorsa DO, Tanner MM, et al. (1997) AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science 277: 965-968.
40. Kuang SQ, Liao L, Wang S, Medina D, O'Malley BW, et al. (2005) Mice lacking the amplified in breast cancer 1/steroid receptor coactivator-3 are resistant to chemical carcinogen-induced mammary tumorigenesis. Cancer Res 65: 7993-8002.
41. Sato M, Umetsu D, Murakami S, Yasugi T, Tabata T (2006) DWnt4 regulates the dorsoventral specificity of retinal projections in the Drosophila melanogaster visual system. Nat Neurosci 9: 67-75.
42. Kunes S, Wilson C, Steller H (1993) Independent guidance of retinal axons in the developing visual system of Drosophila. J Neurosci 13: 752-767.
43. Yang XJ (2004) Lysine acetylation and the bromodomain: a new partnership for signaling. Bioessays 26: 1076-1087.
44. Thompson KA, Wang B, Argraves WS, Giancotti FG, Schranck DP, et al. (1994) BR140, a novel zinc-finger protein with homology to the TAF250 subunit of TFIID. Biochem Biophys Res Commun 198: 1143-1152.
45. Chamberlin HM, Thomas JH (2000) The bromodomain protein LIN-49 and trithorax-related protein LIN-59 affect development and gene expression in Caenorhabditis elegans. Development 127: 713-723.
46. Cavodeassi F, Diez Del Corral R, Campuzano S, Dominguez M (1999) Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development 126: 4933-4942.
47. Dominguez M, de Celis JF (1998) A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye. Nature 396: 276-278.
48. Chotard C, Leung W, Salecker I (2005) glial cells missing and gcm2 cell autonomously regulate both glial and neuronal development in the visual system of Drosophila. Neuron 48: 237-251.
49. Poeck B, Fischer S, Gunning D, Zipursky SL, Salecker I (2001) Glial cells mediate target layer selection of retinal axons in the developing visual system of Drosophila. Neuron 29: 99-113.
50. Suh GS, Poeck B, Chouard T, Oron E, Segal D, et al. (2002) Drosophila JAB1/CSN5 acts in photoreceptor cells to induce glial cells. Neuron 33: 35-46.
51. Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC, et al. (2004) A standardized kinesin nomenclature. J Cell Biol 167: 19-22.
52. Yang JT, Saxton WM, Goldstein LS (1988) Isolation and characterization of the gene encoding the heavy chain of Drosophila kinesin. Proc Natl Acad Sci U S A 85: 1864-1868.
53. Barkus RV, Klyachko O, Horiuchi D, Dickson BJ, Saxton WM (2008) Identification of an Axonal Kinesin-3 Motor for Fast Anterograde Vesicle Transport that Facilitates Retrograde Transport of Neuropeptides. Mol Biol Cell 19: 274-283.
54. Ting CY, Herman T, Yonekura S, Gao S, Wang J, et al. (2007) Tiling of r7 axons in the Drosophila visual system is mediated both by transduction of an activin signal to the nucleus and by mutual repulsion. Neuron 56: 793-806.
55. Treisman JE, Ito N, Rubin GM (1997) misshapen encodes a protein kinase involved in cell shape control in Drosophila. Gene 186: 119-125.
56. Mazo AM, Huang DH, Mozer BA, Dawid IB (1990) The trithorax gene, a trans-acting regulator of the bithorax complex in Drosophila, encodes a protein with zinc-binding domains. Proc Natl Acad Sci U S A 87: 2112-2116.
57. Brunk BP, Martin EC, Adler PN (1991) Drosophila genes Posterior Sex Combs and Suppressor two of zeste encode proteins with homology to the murine bmi-1 oncogene. Nature 353: 351-353.
58. Beckstead R, Ortiz JA, Sanchez C, Prokopenko SN, Chambon P, et al. (2001) Bonus, a Drosophila homolog of TIF1 proteins, interacts with nuclear receptors and can inhibit betaFTZ-F1-dependent transcription. Mol Cell 7: 753-765.
59. Gregory SL, Kortschak RD, Kalionis B, Saint R (1996) Characterization of the dead ringer gene identifies a novel, highly conserved family of sequence-specific DNA-binding proteins. Mol Cell Biol 16: 792-799.
60. Leclerc V, Tassan JP, O'Farrell PH, Nigg EA, Leopold P (1996) Drosophila Cdk8, a kinase partner of cyclin C that interacts with the large subunit of RNA polymerase II. Mol Biol Cell 7: 505-513.
61. Mangs AH, Speirs HJ, Goy C, Adams DJ, Markus MA, et al. (2006) XE7: a novel splicing factor that interacts with ASF/SF2 and ZNF265. Nucleic Acids Res 34: 4976-4986.
62. Sonoda J, Wharton RP (2001) Drosophila Brain Tumor is a translational repressor. Genes Dev 15: 762-773.
63. Arama E, Dickman D, Kimchie Z, Shearn A, Lev Z (2000) Mutations in the beta-propeller domain of the Drosophila brain tumor (brat) protein induce neoplasm in the larval brain. Oncogene 19: 3706-3716.
64. Moberg KH, Mukherjee A, Veraksa A, Artavanis-Tsakonas S, Hariharan IK (2004) The Drosophila F box protein archipelago regulates dMyc protein levels in vivo. Curr Biol 14: 965-974.
65. Moberg KH, Bell DW, Wahrer DC, Haber DA, Hariharan IK (2001) Archipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature 413: 311-316.
66. Mathew D, Gramates LS, Packard M, Thomas U, Bilder D, et al. (2002) Recruitment of scribble to the synaptic scaffolding complex requires GUK-holder, a novel DLG binding protein. Curr Biol 12: 531-539.
67. Brooks SP, Ebenezer ND, Poopalasundaram S, Lehmann OJ, Moore AT, et al. (2004) Identification of the gene for Nance-Horan syndrome (NHS). J Med Genet 41: 768-771.
68. Burdon KP, McKay JD, Sale MM, Russell-Eggitt IM, Mackey DA, et al. (2003) Mutations in a novel gene, NHS, cause the pleiotropic effects of Nance-Horan syndrome, including severe congenital cataract, dental anomalies, and mental retardation. Am J Hum Genet 73: 1120-1130.
69. Katoh M (2004) Identification and characterization of human GUKH2 gene in silico. Int J Oncol 24: 1033-1038.
70. Daubresse G, Deuring R, Moore L, Papoulas O, Zakrajsek I, et al. (1999) The Drosophila kismet gene is related to chromatin-remodeling factors and is required for both segmentation and segment identity. Development 126: 1175-1187.
71. Crews ST, Thomas JB, Goodman CS (1988) The Drosophila single-minded gene encodes a nuclear protein with sequence similarity to the per gene product. Cell 52: 143-151.
72. Siebel CW, Fresco LD, Rio DC (1992) The mechanism of somatic inhibition of Drosophila P-element pre-mRNA splicing: multiprotein complexes at an exon pseudo-59 splice site control U1 snRNP binding. Genes Dev 6: 1386-1401.
73. Goodrich JS, Clouse KN, Schupbach T (2004) Hrb27C, Sqd and Otu cooperatively regulate gurken RNA localization and mediate nurse cell chromosome dispersion in Drosophila oogenesis. Development 131: 1949-1958.
74. Stewart RJ, Pesavento PA, Woerpel DN, Goldstein LS (1991) Identification and partial characterization of six members of the kinesin superfamily in Drosophila. Proc Natl Acad Sci U S A 88: 8470-8474.
75. Ray K, Perez SE, Yang Z, Xu J, Ritchings BW, et al. (1999) Kinesin-II is required for axonal transport of choline acetyltransferase in Drosophila. J Cell Biol 147: 507-518.
76. Iwai Y, Usui T, Hirano S, Steward R, Takeichi M, et al. (1997) Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19: 77-89.
77. Usui T, Shima Y, Shimada Y, Hirano S, Burgess RW, et al. (1999) Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98: 585-595.
78. Streuli M, Krueger NX, Tsai AY, Saito H (1989) A family of receptor-linked protein tyrosine phosphatases in humans and Drosophila. Proc Natl Acad Sci U S A 86: 8698-8702.
79. Takagi S, Hirata T, Agata K, Mochii M, Eguchi G, et al. (1991) The A5 antigen, a candidate for the neuronal recognition molecule, has homologies to complement components and coagulation factors. Neuron 7: 295-307.
80. Leung-Hagesteijn C, Spence AM, Stern BD, Zhou Y, Su MW, et al. (1992) UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell 71: 289-299.
81. Cooley L, Verheyen E, Ayers K (1992) chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell 69: 173-184.
82. Sluss HK, Han Z, Barrett T, Davis RJ, Ip YT (1996) A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev 10: 2745-2758.
83. Riesgo-Escovar JR, Jenni M, Fritz A, Hafen E (1996) The Drosophila Jun-N-terminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye. Genes Dev 10: 2759-2768.
84. Glover CV, Shelton ER, Brutlag DL (1983) Purification and characterization of a type II casein kinase from Drosophila melanogaster. J Biol Chem 258: 3258-3265.
85. Saxena A, Padmanabha R, Glover CV (1987) Isolation and sequencing of cDNA clones encoding alpha and beta subunits of Drosophila melanogaster casein kinase II. Mol Cell Biol 7: 3409-3417.
86. Desai CJ, Garrity PA, Keshishian H, Zipursky SL, Zinn K (1999) The Drosophila SH2-SH3 adapter protein Dock is expressed in embryonic axons and facilitates synapse formation by the RP3 motoneuron. Development 126: 1527-1535.
87. Ang LH, Kim J, Stepensky V, Hing H (2003) Dock and Pak regulate olfactory axon pathfinding in Drosophila. Development 130: 1307-1316.
88. Noselli S, Agnes F (1999) Roles of the JNK signaling pathway in Drosophila morphogenesis. Curr Opin Genet Dev 9: 466-472.
89. Liu ZP, Galindo RL, Wasserman SA (1997) A role for CKII phosphorylation of the cactus PEST domain in dorsoventral patterning of the Drosophila embryo. Genes Dev 11: 3413-3422.
90. Willert K, Brink M, Wodarz A, Varmus H, Nusse R (1997) Casein kinase 2 associates with and phosphorylates dishevelled. Embo J 16: 3089-3096.
91. Trott RL, Kalive M, Paroush Z, Bidwai AP (2001) Drosophila melanogaster casein kinase II interacts with and phosphorylates the basic helix-loop-helix proteins m5, m7, and m8 derived from the Enhancer of split complex. J Biol Chem 276: 2159-2167.
92. Akten B, Jauch E, Genova GK, Kim EY, Edery I, et al. (2003) A role for CK2 in the Drosophila circadian oscillator. Nat Neurosci 6: 251-257.
93. Xu B, English JM, Wilsbacher JL, Stippec S, Goldsmith EJ, et al. (2000) WNK1, a novel mammalian serine/threonine protein kinase lacking the catalytic lysine in subdomain II. J Biol Chem 275: 16795-16801.
94. Wilson FH, Disse-Nicodeme S, Choate KA, Ishikawa K, Nelson-Williams C, et al. (2001) Human hypertension caused by mutations in WNK kinases. Science 293: 1107-1112.
95. Lee BH, Min X, Heise CJ, Xu BE, Chen S, et al. (2004) WNK1 phosphorylates synaptotagmin 2 and modulates its membrane binding. Mol Cell 15: 741-751.
96. Wolff T, Martin KA, Rubin GM, Zipursky SL (1997) The Development of the Drosophila Visual System. In: Cowan WM, Jessell TM, Zipursky SL, eds. Molecular and Cellular Approaches to Neural Development. Oxford: Oxford University Press. pp 474-508.
97. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
98. Rorth P (1996) A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc Natl Acad Sci U S A 93: 12418-12422.
99. Steneberg P, Samakovlis C (2001) A novel stop codon readthrough mechanism produces functional Headcase protein in Drosophila trachea. EMBO Rep 2: 593-597.
100. Fujita SC, Zipursky SL, Benzer S, Ferrus A, Shotwell SL (1982) Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci U S A 79: 7929-7933.
101. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.