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 and Development

Volumn 10, Issue 16, 1996, Pages 2003-2013

  Alexandre, Cyrille ^a   Jacinto, Antonio ^a   Ingham, Philip W ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

cubitus interruptus; decapentaplegic; GLI family; hedgehog signaling; patched promoter; wingless

Indexed keywords

DNA BINDING PROTEIN; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; DROSOPHILA; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE TARGETING; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN SECRETION; REPORTER GENE; SPERMATOGENESIS; TRANSCRIPTION REGULATION;

ANIMALIA; CUBITUS; CUBITUS INTERRUPTUS; ERINACEIDAE; VERTEBRATA;

EID: 0029858774     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.10.16.2003     Document Type: Article

References (73)

1. Alexandre, C., D.A. Grueneberg, and M.Z. Gilman. 1993. Studying heterologous transcription factors in yeast. Methods Companion Methods Enzymol.. 5: 147-155.
2. Ashburner, M. 1989. Drosophila: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. Badiani, P., P. Corbella, D. Kioussis, J. Marvel, and K. Weston. 1994. Dominant interfering alleles define a role for c-Myb in T-cell development. Genes & Dev.. 8: 770-782.
4. Basler, K. and G. Struhl. 1994. Compartment boundaries and the control of Drosophila limb pattern by Hedgehog protein. Nature 368: 208-214.
5. Bender, A. and G.F. Sprague. 1987. Mat α 1, a yeast transcription factor, binds synergistically with a second protein to a set of cell-specific genes. Cell 50: 681-691.
6. Bitgood, M.J., L. Shen, and A.P. McMahon. 1996. Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr. Biol.. 3: 298-304.
7. Blackman, R.K., M. Sanicola, L.A. Raferty, T. Gillevet, and W.M. Gelbart. 1991. An extensive 3′ cis-regulatory region directs the imaginal disc expression of decapentaplegic, a member of the TGF-β family in Drosophila. Development 111: 657-665.
8. Brand, A.H. and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
9. Cadigan, K.M., U. Grossniklaus, and W.J. Gehring. 1994. Localized expression of sloppy paired protein maintains the polarity of Drosophila parasegments. Genes & Dev.. 8: 899-913.
10. Capdevila, J. and I. Guerrero. 1994. Targetted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J.. 13: 4459-4468.
11. Concordet, J.-P., K. Lewis, J. Moore, L.V. Goodrich, R.L. Johnson, M.P. Scott, and P.W. Ingham. 1996. Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122: 2835-2846.
12. Couso, J.-P., M. Bate, and A. Martinez-Arias. 1993. A wingless-dependent polar coordinate system in Drosophila imaginal discs. Science 259: 484-489.
13. Currie, P.D. and P.W. Ingham. 1996. Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature 382: 452-455.
14. Eaton, S. and T.B. Kornberg. 1990. Repression of ci-D in posterior compartments of Drosophila by engrailed. Genes & Dev.. 4: 1068-1077.
15. Echelard, Y., D.J. Epstein, B. St.-Jacques, L. Shen, J. Mohler, J.A. McMahon, and A.P. McMahon. 1993. Sonic hedgehog, a member of a family of putative signaling molecules is implicated in the regulation of CNS and limb polarity. Cell 75: 1417-1430.
16. Fan, C.-M., J.A. Porter, C. Chiang, D.T. Chang, P.A. Beachy, and M. Tessier-Lavigne. 1995. Long-range induction of sclerotome by Sonic hedgehog: A direct role for the amino terminal product of autoproteolytic cleavage and modulation by the cyclic AMP signaling pathway. Cell 81: 457-465.
17. Fausto-Sterling, A. 1978. Pattern formation in the wing veins of the fused mutant (Drosophila melanogaster). Dev. Biol.. 63: 358-369.
18. Fietz, M.J., A. Jacinto, A.M. Taylor, C. Alexandre, and P.W. Ingham. 1995. Secretion of the amino-terminal fragment of the Hedgehog protein is necessary and sufficient for hedgehog signaling in Drosophila. Curr. Biol.. 5: 643-650.
19. Forbes, A.J. 1992. "Segment polarity genes in Drosophila development." D.Phil Thesis. University of Oxford, Oxford, UK.
20. Forbes, A.J., Y. Nakano, A.M. Taylor, and P.W. Ingham. 1993. Genetic analysis of hedgehog signaling in the Drosophila embryo. Development (Suppl.): 115-124.
21. Goodrich, L.V., R.L. Johnson, L. Milenokovic, J.A. McMahon, and M.P. Scott. 1996. Conservation of the hedgehog/ patched signaling pathway from flies to mice: Induction of a mouse patched gene by hedgehog. Genes & Dev.. 10: 310-312.
22. Grossniklaus, U., R. Kurth-Pearson, and W.J. Gehring. 1992. The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes & Dev.. 6: 1030-1051.
23. Guillen, I., J.L. Mullor, J. Capdevilla, E. Sanchez-Herrero, G. Morata, and I. Guerrero 1995. The function of engrailed and the specification of Drosophila wing pattern. Development 121: 3447-3456.
24. Hammerschmidt, M., M.J. Bitgood, and A.P. McMahon. 1996. Protein kinase A is a common negative regulator of Hedgehog signaling in the vertebrate embryo. Genes & Dev.. 10: 647-658.
25. Han, K. and J.L. Manley. 1993. Functional domains of the Drosophila Engrailed protein. EMBO J.. 12: 2723-2733.
26. Hidalgo, A. 1991. Interactions between segment polarity genes and the generation of the segmental pattern in Drosophila. Mech. Dev.. 35: 77-87.
27. Hidalgo, A. and P. Ingham. 1990. Cell patterning in the Drosophila segment: Spatial regulation of the segment polarity gene patched. Development 110: 291-302.
28. Hooper, J. 1994. Distinct pathways for autocrine and parcrine Wingless signaling in Drosophila embryos. Nature 372: 461-464.
29. Hui, C.C., D. Slusarski, K.A. Platt, R. Holmgren, and A.L. Joyner. 1994. Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev. Biol.. 162: 402-413.
30. Ingham, P.W. 1993. Localised hedgehog activity controls spatially restricted transcription of wingless in the Drosophila embryo. Nature 366: 560-562.
31. _. 1995. Signaling by hedgehog family proteins in Droso- phila and vertebrate development. Curr. Opin. Genet. Dev.. 5: 492-498.
32. Ingham, P.W. and M.J. Fietz. 1995. Quantitative effects of hedgehog and decapentaplegic activity on the patterning of the Drosophila wing. Curr. Biol.. 5: 432-441.
33. Ingham, P.W., K.R. Howard, and D. Ish-Horowicz. 1985. Transcription pattern of the Drosophila segmentation gene hairy. Nature 318: 439-445.
34. Ingham, P.W., A.M. Taylor, and Y. Nakano. 1991. Role of the Drosophila patched gene in positional signaling. Nature 353: 184-187.
35. Jiang, J. and G. Struhl. 1995. Protein kinase A and Hedgehog signaling in Drosophila limb development. Cell 80: 563-572.
36. Johnson, R.L., E. Laufer, R.D. Riddle, and C.J. Tabin. 1994. Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites. Cell 79: 1165-1173.
37. Johnson, R.L., J.K. Grenier, and M.P. Scott. 1995. Patched overexpression alters wing disc size and pattern - transcriptional and posttranscriptional effects on hedgehog targets. Development 121: 4161-4170.
38. Kinzler, K.W. and B. Vogelstein. 1990. The GL1 gene encodes a nuclear protein which binds specific sequences in the human genome. Mol. Cell. Biol.. 10: 634-642.
39. Krauss, S., J.-P. Concordet, and P.W. Ingham. 1993. A functionally conserved homolog of the Drosophila segment polarity gene hedgehog is expressed in tissues with polarizing activity in Zebrafish embryos. Cell 75: 1431-1444.
40. Lepage, T., S.M. Cohen, F.J. Diaz-Benjumea, and S.M. Parkhurst. 1995. Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning. Nature 373: 711-715.
41. Levin, M., R.L. Johnson, C.D. Stern, M. Kuehn, and C. Tabin. 1995. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82: 803-814.
42. Li, W., J.T. Ohlmeyer, M.E. Lane, and D. Kalderon. 1995. Function of protein kinase A in Hedgehog signal transduction and Drosophila imaginal disc development. Cell 80: 553-562.
43. Licht, J.D., M.J. Grossel, J. Figge, and U.M. Hansen. 1990. Drosophila Krüppel protein is a transcriptional repressor. Nature 346: 76-79.
44. Lindsley, D.L. and G.G. Zimm. 1992. The genome of Drosophila melanogaster. Academic Press, San Diego, CA.
45. Marigo, V., M.P. Scott, R.L. Johnson, L.V. Goodrich, and C. Tabin. 1996. Conservation in hedgehog signaling: Induction of a chicken patched homolog by Sonic hedgehog in the developing limb. Development 122: 1225-1233.
46. Mitchell, P.J. and R. Tjian. 1989. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245: 371-378.
47. Motzny, C.K. and R. Holmgren. 1995. The Drosophila cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways. Mech. Dev.. 52: 137-150.
48. Nellen, D., R. Burke, G. Struhl, and K. Basler. 1996. Direct and long-range action of a DPP morphogen gradient. Cell 85: 357-368.
49. Nüsslein-Volhard, C. and E. Wieschaus. 1980. Mutations affecting segment number and polarity in Drosophila. Nature 287: 795-801.
50. Orenic, T., J. Chidsey, and R. Holmgren. 1987. Cell and cubitus interruptus Dominant: Two segment polarity genes on the fourth chromosome in Drosophila. Dev. Biol.. 124: 50-56.
51. Orenic, T.V., D.C. Slusarski, K.L. Kroll, and R.A. Holmgren. 1990. Cloning and characterization of the segment polarity gene cubitus interruptus Dominant of Drosophila. Genes & Dev.. 4: 1053-1067.
52. Pan, D. and G.M. Rubin. 1995. cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs. Cell 80: 543-552.
53. Pavletich, N.P. and C.O. Pabo. 1993. Crystal structure of a five-finger GLI-DNA complex: New perspectives on zinc fingers. Science 261: 1701-1707.
54. Perrimon, N. 1995. Hedgehog and beyond. Cell 80: 517-520.
55. Riddle, R., R.L. Johnson, E. Laufer, and C. Tabin. 1993. Sonic Hedgehog mediates the polarizing activity of the ZPA. Cell 75: 1401-1416.
56. Rijsewijk, F., M. Schuermann, E. Wagenaar, P. Parren, D. Weigel, and R. Nusse. 1987. The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50: 649-657.
57. Roberts, D.J., R.L. Johnson, A.C. Burke, C.E. Nelson, B.A. Morgan, and C. Tabin. 1995. Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 121: 3163-3174.
58. Roelink, H., A. Augsburger, J. Heemskerk, V. Korzh, S. Norlin, A. Ruiz i Altaba, Y. Tanabe, M. Placzek, T. Edlund, T.M. Jessell, and J. Dodd. 1994. Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76: 761-775.
59. Roelink, H., J. Porter, C. Chiang, Y. Tanabe, D.T. Chang, P.A. Beachy, and T.M. Jessell. 1995. Floor plate and motor neuron induction by different concentrations of the amino terminal cleavage product of Sonic hedgehog autoproteolysis. Cell 81: 445-455.
60. Ruppert, J.M., B. Vogelstein, K. Arheden, and K.W. Kinzler. 1990. GL13 encodes a 190-Kilodalton protein with multiple regions of GLI similarity. Mol. Cell. Biol.. 10: 5408-5415.
61. Sanicola, M., J. Sekelsky, S. Elson, and W.M. Gelbart. 1995. Drawing a stripe in Drosophila imaginal discs: Negative regulation of decapentaplegic and patched expression by engrailed. Genetics 139: 745-756.
62. Schwartz, C., J. Locke, C. Nishida, and T.B. Kornberg. 1995. Analysis of cubitus interruptus regulation in Drosophila embryos and imaginal discs. Development 121: 1625-1635.
63. Slusarski, D.C., C.K. Motzny, and R. Holmgren. 1995. Mutations that alter the timing and pattern of cubitus interruptus gene expression in Drosophila melanogaster. Genetics 139: 229-240.
64. Speicher, S.A., U. Thomas, U. Hinz, and E. Knust. 1994. The Serrate locus of Drosophila and its role in morphogenesis of imaginal discs: Control of cell proliferation. Development 120: 535-544.
65. Stern, C. and M. Kodani. 1955. Studies on the position effect at the cubitus interruptus locus of Drosophila melanogaster. Genetics 40: 343-373.
66. Struhl, G. and K. Basler. 1993. Organizing activity of wingless protein in Drosophila. Cell 72: 527-540.
67. Tabata, T. and T.B. Kornberg. 1994. Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 76: 89-102.
68. Thérond, P.P., J.D. Knight, T.B. Kornberg, and J.M. Bishop. 1996. Phosphorylation of the fused protein kinase in response to signaling from hedgehog. Proc. Nat. Acad. Sci.. 93: 4224-4228.
69. Triezenberg, S.J., R.C. Kingsbury, and S.L. McKnight. 1988. Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression. Genes & Dev.. 2: 718-729.
70. van den Heuvel, M., R. Nusse, P. Johnston, and P.A. Lawrence. 1989. Distribution of the wingless gene product: A protein involved in cell-cell communication. Cell 59: 739-749.
71. Vortkamp, A., K. Lee, B. Lanske, G.V. Segre, H.M. Kronenberg, and C.J. Tabin. 1996. Indian hedgehog and parathyroid hormone-related protein regulate the rate of cartilage differentiation. Science (in press).
72. Zarkower, D. and J. Hodgkin. 1992. Molecular analysis of the C. elegans sex-determining gene tra-1: A gene encoding two zinc finger proteins. Cell 70: 237-249.
73. _. 1993. Zinc fingers in sex determination: Only one of the two C. elegans Tra-1 proteins binds DNA in vitro. Nucleic Acids Res.. 21: 3691-3698.