Signals transmitted along retinal axons in Drosophila: Hedgehog signal reception and the cell circuitry of lamina cartridge assembly

Development

Volumn 125, Issue 19, 1998, Pages 3753-3764

  Huang, Zhen ^a   Kunes, Samuel ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Cubitus interruptus; Drosophila; Hedgehog; Lamina; Photoreceptor axon

Indexed keywords

SECRETORY PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL CYCLE S PHASE; CELL DIFFERENTIATION; DEVELOPMENTAL GENETICS; DROSOPHILA; EMBRYO; GLIA CELL; NONHUMAN; PRIORITY JOURNAL; RETINA NERVE CELL; SIGNAL TRANSDUCTION;

ANIMALIA; ARACHNIDA; CUBITUS; CUBITUS INTERRUPTUS; ERINACEIDAE; HEXAPODA; INSECTA;

EID: 0031736138     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.125.19.3753     Document Type: Article

References (96)

1. Alcedo, J., Ayzenzon, M., Von Ohlen, T., Noll, M. and Hooper, J. E. (1996). The Drosophila smoothcned gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell 86, 221-232.
2. Alexandre, C., Jacinto, A. and Ingham, P. W. (1996). Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the Cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev. 10, 2003-2013.
3. Aza-Blanc, P., Ramirez-Weber, F. A., Laget, M. P., Sehwartz, C. and Kornberg, T. B. (1997). Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a represser. Cell 89, 1043-1053.
4. Basler, K. and Struhl, G. (1994). Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208-214.
5. Braitenberg, V. (1967). Patterns of projection in the visual system of the fly. I. Retina-lamina projections. Exp. Brain Res. 3, 271-298.
6. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
7. Capdevila, J., Estrada, M. P., Sanchez-Herrero, K. and Guerrero, I. (1994). The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. EMBO J. 13, 71-82.
8. Capdevila, J. and Guerrero, I. (1994). Targeted expression of the signalling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 13, 4459-4468.
9. Chen, Y. and Struhl, G. 0996). Dual roles for patched in sequestering and transducing Hedgehog. Cell 87, 553-563.
10. Chen, Y., Gallaher, N., Goodman, R. H. and Smolik, S. M. (1998). Protein kinase A directly regulates the activity and proteolysis of Cubitus interruptus. Proc. Natl. Acad. Sci. USA 95, 2349-2354.
11. Duminguez, M., Brunner, M., Hafen, E. and Basier, K. (1996). Sending and receiving the hedgehog signal: control by the Drosophila Gli protein Cubitus imerruptus. Science 272, 1621-1625.
12. Dominguez, M. and Hafen, E. (1997). Hedgehog directly controls initiation and propagation of retinal differentiation in the Divsophila eye. Genes Dev. 11, 3254-3264.
13. Eaton, S. and Kornberg, T. B. (1990). Repression of ci-D in posterior compartments of Drosophila by engrailed. Genfs Dev. 4, 1068-1077.
14. Falls, D. L., Rosen, K. M., Corfas, G., Lane, W. S. and Fischbach, G. D. (1993). ARIA, a protein that stimulates acetylcholinc receptor synthesis, is a member of the neu ligand family. Cell 72, 801-815.
15. Fan, C. M., Porter, J. A., Chiang, C., Chang, D. T., Beachy, P. A. and Tessier-Lavlgne, M. (1995). Long-range sclerotome induction by Sonic hedgehog: direct role of the amino-terminal cleavage product and modulation by the cyclic AMP signaling pathway. Cell 81, 457-465.
16. Fischbach, K. F. and Technau, G. (1984). Cell degeneration in the developing optic lobes of the sine, oculis and small-optic-lobes mutants of Drosophila melanogaster. Dev. Biol. 104, 219-239.
17. Glbbs, S. M. and Truman, J. W. (1998). Nitric oxide and cyclic GMP regulate retinal patterning in the optic lobe of Drosophila. Neuron 20, 83-93.
18. Golic, K. G. and Lindquist, S. (1989). The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499-509.
19. Goodrich, L. V., Johnson, R. L., Milenkovic, L., McMahon, J. A. and Scott, M. P. (1996). Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by hedgehog. Genes Dev. 10, 301-312.
20. Goodrich, L. V., Milenkovic, L., Higgins, K. M. and Scott, M. P. (1997). Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 211, 1109-1113.
21. Grimm, S. and Pflugfelder, G. O. (1996). Control of the gene optomotor-blind in Drosophila wing development by decapentaplegic and wingless. Science 271, 1601-1604.
22. Halter, D. A., Urban, J., Rickert, C., Ner, S. S., Ito, K., Travers, A. A. and Technau, G. M. (1995). The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121, 317-332.
23. Hammerschmidt, M., Brook, A. and McMahon, A. P. (1997). The world according to hedgehog. Trends Genet. 13, 14-21.
24. Heberlein, U., Wolff, T. and Rubin, G. (1993). The TGF-β homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75, 913-926.
25. Heberlein, U, Singh, C. M., Luk, A. Y. and Donohoe, T. J. (1995). Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373, 709-711.
26. Heisenberg, M. (1972). Behavioural diagnostics: a way to analyze visual mutants in Drosophila. In Information Processing in the Visual System, (ed. R. Wehner), pp. 265-268, Berlin: Springer Verlag.
27. Hepker, J., Wang, Q. T., Motzny, C. K., Holmgren, R. and Orenic, T. V. (1997). Drosophila cubitus intemtptits forms a negative feedback loop with patched and regulates expression of Hedgehog target genes. Development 124, 549-558.
28. Hidalgo, A. and Ingham, P. (1990). Cell patterning in the Drosophila segment: spatial regulation of the segment polarity gene patched. Development 110, 291-301.
29. Hooper, J. E. and Scott, M. P. (1989). The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell 59, 751-765.
30. Huang, Z and Kunes, S. (1996). Hedgehog, transmitted along retinal axons, triggers neurogenesis in the developing visual centers of the Drosophila brain. Cell 86, 411-422.
31. Ingham, P. W. (1995). Signalling by hedgehog family prottifota in Drosophila and vertebrate development. Curr. Opin. Genet. Dev. 5, 492-498.
32. Ingham, P. W. and Hidalgo, A. (1993). Regulation of wingless transcription in the Drosophila embryo. Development 117, 283-291.
33. Ingham, P. W., Taylor, A. M. and Nakano, Y. (1991). Role of the Drosophila patched gene in positional signalling, Nature 353, 184-187.
34. Jiang, J. and Struhl, G. (1995). Protein kinase A and Hedgehog signaling in Drosophila limb development. Cell 80, 563-572.
35. Johnson, R. L., Grenier, J. K. and Scott, M. P. (1995). patched overex pression alters wing disc size and pattern: transcriptional and post-transcriptional effects on hedgehog targets. Development 121, 4161-4170.
36. Kaphingst, K. and Kunes, S. (1994). Pattern formation in the visual centers of the Drosophila brain: wingless acts via decapentaplegic to specify the dorsoventral axis. Cell 78, 437-448.
37. Kelly, J. P. and Cowan, W. M. (1972). Studies on the development of the chick optic tectum. 3. Effects of early eye removal. Brain Res. 42, 263-288.
38. Kunes, S. and Steller, H. (1993). Topography in the Drosophila visual system. Curr. Opin. Neurobiol. 3, 53-59.
39. Kunes, S., Wilson, C. and Steller, H. (1993). Independent guidance of retinal axons in the developing visual system of Drosophila. J. Neurosci. 13, 752-767.
40. Lecuit, T., Brook, W. J., Ng, M., Calleja, M., Sun, H. and Cohen, S.M. (1996). Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381, 387-393.
41. Lee, J. J., von Kessler, D. P., Parks, S. and Beachy, P.A. (1992). Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71, 33-50.
42. Lepage, T., Cohen, S. M., Diaz-Benjumea, F. J. and Parkhurst, S. M. (1995). Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning. Nature 373, 711-715.
43. Li, W., Ohlmeyer, J. T., Lane, M. E. and Kalderon, D. (1995). Function of protein kinase A in Hedgehog signal transduction and Drosophila imaginal disc development. Cell 80, 553-562.
44. Ma, C., Zhou, Y., Beachy, P. A. and Moses, K. (1993). The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75, 927-938.
45. Macagno, E. R. (1979). Cellular interactions and pattern formation in the development of the visual system of Daphnia magna (Crustacea, Brachiopoda). I. Interactions between embryonic retinular fibers and laminar neurons. Dev. Biol. 73, 206-238.
46. Mardon, G., Solomon, N. M. and Rubin, G. M. (1994). dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila, Development 120, 3473-3486.
47. Marigo, V., Davey, R. A., Zuo, Y., Cunningham, J. M. and Tabin, C. J. (1996a). Biochemical evidence that Patched is the Hedgehog receptor. Nature 384, 176-179.
48. Marigo, V., Scott, M. P., Johnson, R. L., Goodrich, L. V. and Tabin, C. J. (1996b). Conservation in hedgehog signaling: Induction of a chicken patched homolog by Sonic hedgehog in the developing limb. Development 122, 1225-1233.
49. Martin, K. A., Poeck, B., Roth, H., Ebens, A. J., Ballard, L. C. and Zipursky, S. L. (1995). Mutations disrupting neuronal connectivity in the Drosophila visual system. Neuron 14, 229-240.
50. Meinertzhagen, I. A. and Hanson, T. E. (1993). The development of the optic lobe. In The Development of Drosophila melanogaster. (ed. M. Bate and A. Martinez-Arias). pp. 1363-1491. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press
51. Meinertzhagen, I. A. and O'Neil, S. D. (1991). Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J. Comp. Neurol. 305, 232-263.
52. Mohler, J. and Vani, K. (1992). Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila. Development 115, 957-971.
53. Motzny, C. K. and Holmgren, R. (1995). The Drosophila Cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways. Mech. Dev. 52, 137-150.
54. Nakano, Y., Guerrero, I., Hidalgo, A., Taylor, A., Whittle, J. R. and Ingham, P. W. (1989). A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched. Nature 341, 508-513.
55. Nellen, D., Burke, R., Struhl, G. and Basler, K. (1996). Direct and long-range action of a DPP morphogen gradient. Cell 85, 357-368.
56. Nusslein-Volhard, C. and Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature 287, 795-801.
57. Nusslein-Volhard, C., Wieschaus, E. and Kluding, H. (1984). Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. zygotic loci on the second chromosome. Roux's Arch. Dev. Biol. 193, 267-282.
58. Oland, L. A. and Tolbert, L. P. (1996). Multiple factors shape development of olfactory glomcruli: insights from an insect model system. J. Neurobiol. 30, 92-109.
59. Orenic, T. V., Slusarski, D. C., Kroll, K. L. and Holmgren, R. A. (1990). Cloning and characterization of the segment polarity gene cubitus interruptus Dominant of Dmsophila. Genes Dev. 4, 1053-1067.
60. Pan, D. and Rubin, G. M. (1995). cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs. Cell 80, 543-552.
61. Perez, S. E. and Steller, H. (1996). Migration of glial cells into the retinal axon target field in Drosophila melanogaster. J, Neurobiol. 30, 359-373.
62. Pflugfelder, G. O., Schwarz, H., Roth, H., Poeck, B., Sigl, A., Kerseher, S., Jonschker, B., Pak, W. L. and Heisenberg, M. (1990). Genetic and molecular characterization of the optomotor-blind gene locus in Drosophila melanogaster. Genetics 126, 91-104.
63. Phillips, R. G., Roberts, I. J. H., Ingham. P. W. and Whittle, J. R. S. (1990). The Drosophila segment polarity gene patched is involved in a position-signalling mechanism in imaginal discs. Development 110, 105-114.
64. Pignoni, F. and Zipursky, S. L. (1997). Induction of Drosophila eye development by decapentaplegic. Development 124, 271-278.
65. Poeck, B., Hofbauer, A. and Pflugfelder, G. O. (1993). Expression of the Drosophila optomotor-blind gene transcript in neuronal and glial cells of the developing nervous system. Development 117, 1017-1029
66. Power, M. E. (1943). The effect of reduction in numbers of ommatidia upon the brain of Drosophila melanogaster. J. Exp. Zool. 94, 33-72.
67. Ready, D. F., Hanson, T. E. and Benzer, S. (1976). Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol. 53, 217-240.
68. Robbins, D. J., Nybakken, K. E., Kobayashi, R., Sisson, J. C., Bishop, J. M. and Therond, P. P. (1997). Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein Costal2. Cell 90, 225-234.
69. Rupp, F., Payan, D. G., Magill-Solc, C., Cowan, D. M. and Scheller, R. H. (1991), Structure and expression of a rat agrin. Neuron 6, 811 -823
70. Sanchez-Herrero, E., Couso, J. P., Capdevlla, J. and Guerrero, I. (1996). The fu gene discriminates between pathways to control dpp expression in Drosophila imaginai discs. Mech. Dev. 55, 159-170.
71. Setleck, S. B. and Steller, H. (1991). The influence of retinal innervation on neurogenesis in the first optic ganglion of Drosophila. Neuron 6, 83-99.
72. 1-S transition in postembryonic neuronal precursors by axon ingrowth. Nature 355, 253-255.
73. Singer, M. A., Penton, A., Twombly, V., Hoffmann, F. M. and Gelbart, W. M. (1997). Signaling through both type I DPP receptors is required for anterior-posterior patterning of the entire Drosophila wing. Development 124, 79-89.
74. Sisson, J. C., Ho, K. S., Suyama, K. and Scott, M. P. (1997), Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell 90, 235-245.
75. Slusarski, D. C., Motzny, C. K. and Holmgren, R. (1995). Mutations that alter the timing and pattern of cubitus interrupts gene expression in Drosophila melanogaster. Genetics 139, 229-240.
76. Smith, M. A., Magill-Solc, C, Rupp, F., Yao, Y.-M. M, Schilling, J. W., Snow, I. and McMahan, U. J. (1992). Isolation and characterization of an agrin homolog in the marine ray. Mol. Cell. Neurosci. 3, 406-417.
77. Stone, D. M., Hynes, M., Armanini, M., Swanson, T.A., Gu, Q., Johnson, R. L., Scott, M. P., Pennica, D., Goddard, A., Phillips, H., Noll, M., Hooper, J. E., de Sauvage, F. and Rosenthal, A. (1996). The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384, 129-134.
78. Strutt, D. I., Wiersdorff, V. and Mlodzik, M. (1995). Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A. Nature 373, 705-709.
79. Strutt, D. I. and Mlodzik, M. (1997). Hedgehog is an indirect regulator of morphogenetic furrow progression in the Drosophila eye disc. Development 124, 3233-3240.
80. Sun, Y. H., Tsai, C. J., Green, M. M., Chao, J. L., Yu, C. T., Jaw, T. J., Yeh, J. Y, and Bolshakov, V. N. (1995). White as a reporter gene to detect transcriptional silencers specifying position-specific gene expression during Drosophila melanogaster eye development. Genetics 141, 1075-1086.
81. Tabata, T., Eaton, S. and Kornberg, T. B. (1992). The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev. 6, 2635-2645.
82. Tabata, T. and Kornberg, T. B. (1994). Hedgehog is a signalling protein with a key role in patterning Drosophila imaginal discs. Cell 76, 89-102.
83. Tashiro, S., Michlue, T., Higashijima, S., Zenno, S., Ishimaru, S., Takahashi, F., Orihara, M., Kojima, T. and Saigo, K. (1993). Structure and expression of hedgehog, a Drosophila segment-polarity gene required for cell-cell communication, Gene 124, 183-189.
84. Trujillo-Cenoz, O. and Melamed, J. (1973). The development of the retina-lamina complex in muscoid flies. J. Ultrastruct. Res. 42, 554-581.
85. Truman, J. W. and Bate, M. (1988). Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol. 125, 145-157.
86. Tsim, K. W., Ruegg, M. A., Escher, G., Kroger, S. and McMahan, U. J. (1992). cDNA that encodes active agrin. Neuron 8, 677-689.
87. van den Heuvel, M. and Ingham, P. W. (1996). smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature 382, 547-551.
88. Vincent, J. P., Girdham, C. H. and O'Farrell, P, H. (1994), A cell-autonomous, ubiquitous marker for the analysis of Drosophila genetic mosaics. Dev. Biol. 164, 328-331.
89. Von Ohlen, T. and Hooper, J. E. (1997). Hedgehog signaling regulates transcription through Gli/Ci binding sites in the wingless enhancer. Mech. Dev. 68, 149-156.
90. Von Ohlen, T., Lessing, D., Nusse, R. and Hooper, J. E. (1997). Hedgehog signaling regulates transcription through Cubitus interruptus, a sequence-specific DNA binding protein. P roc. Natl. Acad. Sci. USA 94, 2404-2409.
91. Vortkamp, A., Lee, K., Lanske, B., Segre, G. V., Kronenberg, H. M. and Tabin, C. J. (1996). Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273, 613-622.
92. Winberg, M., Perez, S. and Steller, H. (1992). Generation and early differentiation of glial cells in the first optic ganglion of Drosophila melanogaster. Development 115, 903-911.
93. Xiong, W. C, Okano, H., Patel, N. H., Blendy, J. A. and Montell, C. (1994). repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 8, 981-994.
94. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Dmsophifa tissues. Development 117, 1223-1237.
95. Yamagata, M., Herman, J, P. and Sanes, J. R. (1995). Lamina-specific expression of adhesion molecules in developing chick optic tectum, J. Neurosci. 15, 4556-4571,
96. Zecca, M., Basler, K. and Struhl, G. (1995). Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121, 2265-2278.