Optomotor-blind expression in glial cells is required for correct axonal projection across the Drosophila inner optic chiasm

Developmental Biology

Volumn 315, Issue 1, 2008, Pages 28-41

  Hofmeyer, Kerstin ^a   Kretzschmar, Doris ^b   Pflugfelder, Gert O ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Axonal pathfinding; Cell migration; Drosophila; Glia; Gliopodia; Optic chiasm; Optomotor blind; T box; Visual system development

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL SURVIVAL; DROSOPHILA; ENHANCER REGION; EYE DEVELOPMENT; GENE; GENE EXPRESSION; GLIA CELL; NERVE PROJECTION; NEUROPIL; NONHUMAN; OPTIC CHIASM; OPTOMOTOR BLIND GENE; PRIORITY JOURNAL;

EID: 39249085073     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.10.011     Document Type: Article

References (82)

1. Akiyama Y., Hosoya T., Poole A.M., and Hotta Y. The gcm-motif: a novel DNA-binding motif conserved in Drosophila and mammals. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 14912-14916
2. Allen N.J., and Barres B.A. Signaling between glia and neurons: focus on synaptic plasticity. Curr. Opin. Neurobiol. 15 (2005) 542-548
3. Auld V. Glia as mediators of growth cone guidance: studies from insect nervous systems. Cell. Mol. Life Sci. 55 (1999) 1377-1385
4. Auld D.S., and Robitaille R. Glial cells and neurotransmission: an inclusive view of synaptic function. Neuron 40 (2003) 389-400
5. Auld D.S., Colomar A., Belair E.L., Castonguay A., Pinard A., Rousse I., Thomas S., and Robitaille R. Modulation of neurotransmission by reciprocal synapse-glial interactions at the neuromuscular junction. J. Neurocytol. 32 (2003) 1003-1015
6. Awasaki T., and Ito K. Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr. Biol. 14 (2004) 668-677
7. Banga S.S., Bloomquist B.T., Brodberg R.K., Pye Q.N., Larrivee D.C., Mason J.M., Boyd J.B., and Pak W.L. Cytogenetic characterization of the 4BC region on the X chromosome of Drosophila melanogaster: localization of the mei-9, norpA and omb genes. Chromosoma 93 (1986) 341-346
8. Booth G.E., Kinrade E.F., and Hidalgo A. Glia maintain follower neuron survival during Drosophila CNS development. Development 127 (2000) 237-244
9. Boschert U., Ramos R.G., Tix S., Technau G.M., and Fischbach K.F. Genetic and developmental analysis of irreC, a genetic function required for optic chiasm formation in Drosophila. J. Neurogenet. 6 (1990) 153-171
10. Braitenberg V. Patterns of projection in the visual system of the fly. I. Retina-lamina projections. Exp. Brain Res. 3 (1967) 271-298
11. Braitenberg V. On Chiasms (1968), Springer Verlag, Berlin-Heidelberg-New York
12. Braitenberg V. Order and orientation of elements in the visual system of the fly. Kybernetik 7 (1970) 235-242
13. Brunner A., Wolf R., Pflugfelder G.O., Poeck B., and Heisenberg M. Mutations in the proximal region of the optomotor-blind locus of Drosophila melanogaster reveal a gradient of neuroanatomical and behavioral phenotypes. J. Neurogenet. 8 (1992) 43-55
14. Brunner A., Twardzik T., and Schneuwly S. The Drosophila giant lens gene plays a dual role in eye and optic lobe development: inhibition of differentiation of ommatidial cells and interference in photoreceptor axon guidance. Mech. Dev. 48 (1994) 175-185
15. Buchanan R.L., and Benzer S. Defective glia in the Drosophila brain degeneration mutant drop-dead. Neuron 10 (1993) 839-850
16. Campbell G., Goring H., Lin T., Spana E., Andersson S., Doe C.Q., and Tomlinson A. RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila. Development 120 (1994) 2957-2966
17. Chotard C., and Salecker I. Neurons and glia: team players in axon guidance. Trends Neurosci. 27 (2004) 655-661
18. Cutforth T., and Gaul U. The genetics of visual system development in Drosophila: specification, connectivity and asymmetry. Curr. Opin. Neurobiol. 7 (1997) 48-54
19. Dearborn Jr. R., and Kunes S. An axon scaffold induced by retinal axons directs glia to destinations in the Drosophila optic lobe. Development 131 (2004) 2291-2303
20. Dearborn Jr. R., He Q., Kunes S., and Dai Y. Eph receptor tyrosine kinase-mediated formation of a topographic map in the Drosophila visual system. J. Neurosci. 22 (2002) 1338-1349
21. Desplan C., Theis J., and O'Farrell P.H. The sequence specificity of homeodomain-DNA interaction. Cell 54 (1988) 1081-1090
22. Duchek P., Somogyi K., Jekely G., Beccari S., and Rorth P. Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell 107 (2001) 17-26
23. Dumstrei K., Wang F., Nassif C., and Hartenstein V. Early development of the Drosophila brain: V. Pattern of postembryonic neuronal lineages expressing DE-cadherin. J. Comp. Neurol. 455 (2003) 451-462
24. Edenfeld G., Stork T., and Klambt C. Neuron-glia interaction in the insect nervous system. Curr. Opin. Neurobiol. 15 (2005) 34-39
25. Eule, E., Tix, S., Fischbach, K.F., 1995. Glial cells in the optic lobe of Drosophila melanogaster. www.flybrain.org, poster accession no. PP00004.
26. Fan Y., Soller M., Flister S., Hollmann M., Muller M., Bello B., Egger B., White K., Schafer M.A., and Reichert H. The egghead gene is required for compartmentalization in Drosophila optic lobe development. Dev. Biol. 287 (2005) 61-73
27. Fischbach K.F., and Dittrich A.P.M. The optic lobe of Drosophila melanogaster. Part I. A Golgi analysis of wild-type structure. Cell Tissue Res. 258 (1989) 441-475
28. Garen S.H., and Kankel D.R. Golgi and genetic mosaic analyses of visual system mutants in Drosophila melanogaster. Dev. Biol. 96 (1983) 445-466
29. Garrity P.A., Lee C.H., Salecker I., Robertson H.C., Desai C.J., Zinn K., and Zipursky S.L. Retinal axon target selection in Drosophila is regulated by a receptor protein tyrosine phosphatase. Neuron 22 (1999) 707-717
30. Gonzalez F., Romani S., Cubas P., Modolell J., and Campuzano S. Molecular analysis of the asense gene, a member of the achaete-scute complex of Drosophila melanogaster, and its novel role in optic lobe development. EMBO J. 8 (1989) 3553-3562
31. Grimm S., and Pflugfelder G.O. Control of the gene optomotor-blind in Drosophila wing development by decapentaplegic and wingless. Science 271 (1996) 1601-1604
32. Halter D.A., Urban J., Rickert C., Ner S.S., Ito K., Travers A.A., and Technau G.M. The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121 (1995) 317-332
33. Hausen K. Motion sensitive interneurons in the optomotor system of the fly II The horizontal cells: receptive field organization and response characteristics. Biol. Cybern. 46 (1982) 67-79
34. Hausen K., and Wehrhahn C. Neural circuits mediating visual flight control in flies. I. Quantitative comparison of neural and behavioral response characteristics. J. Neurosci. 9 (1989) 3828-3836
35. Heisenberg M., Wonneberger R., and Wolf R. Optomotor-blind H31-A Drosophila mutant of the lobula plate giant neurons. J. Comp. Physiol. 124 (1978) 287-296
36. Hofbauer A., and Campos-Ortega J.A. Proliferation pattern and early differentiation of the optic lobes in Drosophila melanogaster. Roux's Arch. Dev. Biol. 198 (1990) 264-274
37. Hosoya T., Takizawa K., Nitta K., and Hotta Y. glial cells missing: a binary switch between neuronal and glial determination in Drosophila. Cell 82 (1995) 1025-1036
38. Huang Z., and Kunes S. Signals transmitted along retinal axons in Drosophila: hedgehog signal reception and the cell circuitry of lamina cartridge assembly. Development 125 (1998) 3753-3764
39. Ito K., Urban J., and Technau G.M. Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval nerve cord. Roux's Arch. Dev. Biol. 204 (1995) 284-307
40. Jacobs J.R. The midline glia of Drosophila: a molecular genetic model for the developmental functions of glia. Prog. Neurobiol. 62 (2000) 475-508
41. Jeffery G. Architecture of the optic chiasm and the mechanisms that sculpt its development. Physiol. Rev. 81 (2001) 1393-1414
42. Jones B.W., Fetter R.D., Tear G., and Goodman C.S. Glial cells missing: a genetic switch that controls glial versus neuronal fate. Cell 82 (1995) 1013-1023
43. Klein D.E., Nappi V.M., Reeves G.T., Shvartsman S.Y., and Lemmon M.A. Argos inhibits epidermal growth factor receptor signalling by ligand sequestration. Nature 430 (2004) 1040-1044
44. Kretzschmar D., and Pflugfelder G.O. Glia in development, function, and neurodegeneration of the adult insect brain. Brain Res. Bull. 57 (2002) 121-131
45. Liu E., and Restifo L.L. Identification of a broad complex-regulated enhancer in the developing visual system of Drosophila. J. Neurobiol. 34 (1998) 253-270
46. Martin K.A., Poeck B., Roth H., Ebens A.J., Ballard L.C., and Zipursky S.L. Mutations disrupting neuronal connectivity in the Drosophila visual system. Neuron 14 (1995) 229-240
47. Meinertzhagen I.A., and Hanson T.E. The development of the optic lobe. In: Bate M., and Martinez Arias A. (Eds). The Development of Drosophila melanogaster vol. 2 (1993), Cold Spring Harbor Laboratory Press 1363-1491
48. Merli C., Bergstrom D.E., Cygan J.A., and Blackman R.K. Promoter specificity mediates the independent regulation of neighboring genes. Genes Dev. 10 (1996) 1260-1270
49. Newsome T.P., Asling B., and Dickson B.J. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127 (2000) 851-860
50. Pereanu W., Shy D., and Hartenstein V. Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev. Biol. 283 (2005) 191-203
51. Pflugfelder G.O. Genetic lesions in Drosophila behavioural mutants. Behav. Brain Res. 95 (1998) 3-15
52. Pflugfelder G.O., and Heisenberg M. Optomotor-blind of Drosophila melanogaster: a neurogenetic approach to optic lobe development and optomotor behaviour. Comp. Biochem. Physiol., A Physiol. 110 (1995) 185-202
53. Pflugfelder G.O., Schwarz H., Roth H., Poeck B., Sigl A., Kerscher S., Jonschker B., Pak W.L., and Heisenberg M. Genetic and molecular characterization of the optomotor-blind gene locus in Drosophila melanogaster. Genetics 126 (1990) 91-104
54. Pflugfelder G.O., Roth H., Poeck B., Kerscher S., Schwarz H., Jonschker B., and Heisenberg M. The lethal(1)optomotor-blind gene of Drosophila melanogaster is a major organizer of optic lobe development: isolation and characterization of the gene. PProc. Natl. Acad. Sci. U. S. A. 89 (1992) 1199-2203
55. Pielage J., Steffes G., Lau D.C., Parente B.A., Crews S.T., Strauss R., and Klambt C. Novel behavioral and developmental defects associated with Drosophila single-minded. Dev. Biol. 249 (2002) 283-299
56. Poeck B., Hofbauer A., and Pflugfelder G.O. Expression of the Drosophila optomotor-blind gene transcript in neuronal and glial cells of the developing nervous system. Development 117 (1993) 1017-1029
57. Poeck B., Fischer S., Gunning D., Zipursky S.L., and Salecker I. Glial cells mediate target layer selection of retinal axons in the developing visual system of Drosophila. Neuron 29 (2001) 99-113
58. Porsch M., Sauer M., Schulze S., Bahlo A., Roth M., and Pflugfelder G.O. The relative role of the T-domain and flanking sequences for developmental control and transcriptional regulation in protein chimeras of Drosophila OMB and ORG-1. Mech. Dev. 122 (2005) 81-96
59. Rachidi M., Lopes C., and Benichou J.C. Genetical analysis of visual system disorganizer (vid), a new gene involved in normal development of eye and optic lobe of the brain in Drosophila melanogaster. Genetica 99 (1997) 31-45
60. Ramos R.G., Igloi G.L., Lichte B., Baumann U., Maier D., Schneider T., Brandstatter J.H., Frohlich A., and Fischbach K.F. The irregular chiasm C-roughest locus of Drosophila, which affects axonal projections and programmed cell death, encodes a novel immunoglobulin-like protein. Genes Dev. 7 (1993) 2533-2547
61. Rangarajan R., Gong Q., and Gaul U. Migration and function of glia in the developing Drosophila eye. Development 126 (1999) 3285-3292
62. Rao Y., Pang P., Ruan W., Gunning D., and Zipursky S.L. brakeless is required for photoreceptor growth-cone targeting in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 5966-5971
63. Restifo L.L., and White K. Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of the central nervous system in Drosophila. Dev. Biol. 148 (1991) 174-194
64. Rossler W., Oland L.A., Higgins M.R., Hildebrand J.G., and Tolbert L.P. Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. J. Neurosci. 19 (1999) 9865-9877
65. Ruan W., Pang P., and Rao Y. The SH2/SH3 adaptor protein dock interacts with the Ste20-like kinase misshapen in controlling growth cone motility. Neuron 24 (1999) 595-605
66. Ruan W., Long H., Vuong D.H., and Rao Y. Bifocal is a downstream target of the Ste20-like serine/threonine kinase misshapen in regulating photoreceptor growth cone targeting in Drosophila. Neuron 36 (2002) 831-842
67. Saint Marie R.L., and Carlson S.D. The fine structure of neuroglia in the lamina ganglionaris of the housefly, Musca domestica L. J. Neurocytol. 12 (1983) 213-241
68. Schier A.F., and Gehring W.J. Direct homeodomain-DNA interaction in the autoregulation of the fushi tarazu gene. Nature 356 (1992) 804-807
69. Schneider T., Reiter C., Eule E., Bader B., Lichte B., Nie Z., Schimansky T., Ramos R.G., and Fischbach K.F. Restricted expression of the irreC-rst protein is required for normal axonal projections of columnar visual neurons. Neuron 15 (1995) 259-271
70. Schreiber J., Sock E., and Wegner M. The regulator of early gliogenesis glial cells missing is a transcription factor with a novel type of DNA-binding domain. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 4739-4744
71. Senti K., Keleman K., Eisenhaber F., and Dickson B.J. brakeless is required for lamina targeting of R1-R6 axons in the Drosophila visual system. Development 127 (2000) 2291-2301
72. Sepp K.J., Schulte J., and Auld V.J. Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev. Biol. 238 (2001) 47-63
73. Sivasankaran R., Vigano M.A., Muller B., Affolter M., and Basler K. Direct transcriptional control of the Dpp target omb by the DNA binding protein Brinker. EMBO J. 19 (2000) 6162-6172
74. Suh G.S., Poeck B., Chouard T., Oron E., Segal D., Chamovitz D.A., and Zipursky S.L. Drosophila JAB1/CSN5 acts in photoreceptor cells to induce glial cells. Neuron 33 (2002) 35-46
75. Tayler T.D., and Garrity P.A. Axon targeting in the Drosophila visual system. Curr. Opin. Neurobiol. 13 (2003) 90-95
76. Tayler T.D., Robichaux M.B., and Garrity P.A. Compartmentalization of visual centers in the Drosophila brain requires Slit and Robo proteins. Development 131 (2004) 5935-5945
77. Tix S., Eule E., Fischbach K.F., and Benzer S. Glia in the chiasms and medulla of the Drosophila melanogaster optic lobes. Cell Tissue Res. 289 (1997) 397-409
78. Watts R.J., Schuldiner O., Perrino J., Larsen C., and Luo L. Glia engulf degenerating axons during developmental axon pruning. Curr. Biol. 14 (2004) 678-684
79. Xiong W.C., and Montell C. Defective glia induce neuronal apoptosis in the repo visual system of Drosophila. Neuron 14 (1995) 581-590
80. Younossi-Hartenstein A., Nassif C., Green P., and Hartenstein V. Early neurogenesis of the Drosophila brain. J. Comp. Neurol. 370 (1996) 313-329
81. Younossi-Hartenstein A., Salvaterra P.M., and Hartenstein V. Early development of the Drosophila brain: IV. Larval neuropile compartments defined by glial septa. J. Comp. Neurol. 455 (2003) 435-450
82. Yuasa Y., Okabe M., Yoshikawa S., Tabuchi K., Xiong W.C., Hiromi Y., and Okano H. Drosophila homeodomain protein REPO controls glial differentiation by cooperating with ETS and BTB transcription factors. Development 130 (2003) 2419-2428