Interaction between wingless and notch signaling pathways mediated by dishevelled

Science

Volumn 271, Issue 5257, 1996, Pages 1826-1832

  Axelrod, Jeffrey D ^a,b   Matsuno, Kenji ^c   Artavanis Tsakonas, Spyros ^c   Perrimon, Norbert ^c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA BINDING; DROSOPHILA; EMBRYO DEVELOPMENT; GENETIC ANALYSIS; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0029670476     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.271.5257.1826     Document Type: Article

References (73)

1. N. R. Ramaknshna and A. M. C. Brown, Dev. Suppl., 95 (1993), R Nusse and H E Varmus, Cell 69, 1073 (1992); A. P. McMahon, Trends Genet. 8, 236 (1992).
2. N. R. Ramaknshna and A. M. C. Brown, Dev. Suppl., 95 (1993), R Nusse and H E Varmus, Cell 69, 1073 (1992); A. P. McMahon, Trends Genet. 8, 236 (1992).
3. N. R. Ramaknshna and A. M. C. Brown, Dev. Suppl., 95 (1993), R Nusse and H E Varmus, Cell 69, 1073 (1992); A. P. McMahon, Trends Genet. 8, 236 (1992).
4. E. Siegfried and N. Pemmon, Bioessays 16, 393 (1994), A Martinez-Anas, in The Development of Drosophila melanogaster, M. Bate and A. Martinez-Arias, Eds (Cold Spnng Harbor Laboratory Press, Cold Spnng Harbor, NY, 1993), vol. 1, pp. 517-608.
5. E. Siegfried and N. Pemmon, Bioessays 16, 393 (1994), A Martinez-Anas, in The Development of Drosophila melanogaster, M. Bate and A. Martinez-Arias, Eds (Cold Spnng Harbor Laboratory Press, Cold Spnng Harbor, NY, 1993), vol. 1, pp. 517-608.
6. S. Sokol, J. Klingensmith, N. Perrimon, K. Itoh, Development 121, 1637 (1995); D. J. Sussman et al., Dev Biol 166, 73 (1994).
7. S. Sokol, J. Klingensmith, N. Perrimon, K. Itoh, Development 121, 1637 (1995); D. J. Sussman et al., Dev Biol 166, 73 (1994).
8. J. Klingensmith, R. Nusse, N. Perrimon, Genes Dev, 8, 118 (1994).
9. H Thiesen et al , Development 120, 347 (1994).
10. E Siegfried, L A. Perkins, T.M. Capaci, N. Perrimon, Nature 345, 825 (1990), M. Bourouis et al., EMBO J. 9. 2877 (1990); L. Ruel, V. Pantesco, Y. Lutz, P Simpson, M. Bourouis, ibid. 12, 1657 (1993), E. Siegfried, T. B Chou, N. Perrimon, Cell 71, 1167 (1992).
11. E Siegfried, L A. Perkins, T.M. Capaci, N. Perrimon, Nature 345, 825 (1990), M. Bourouis et al., EMBO J. 9. 2877 (1990); L. Ruel, V. Pantesco, Y. Lutz, P Simpson, M. Bourouis, ibid. 12, 1657 (1993), E. Siegfried, T. B Chou, N. Perrimon, Cell 71, 1167 (1992).
12. E Siegfried, L A. Perkins, T.M. Capaci, N. Perrimon, Nature 345, 825 (1990), M. Bourouis et al., EMBO J. 9. 2877 (1990); L. Ruel, V. Pantesco, Y. Lutz, P Simpson, M. Bourouis, ibid. 12, 1657 (1993), E. Siegfried, T. B Chou, N. Perrimon, Cell 71, 1167 (1992).
13. E Siegfried, L A. Perkins, T.M. Capaci, N. Perrimon, Nature 345, 825 (1990), M. Bourouis et al., EMBO J. 9. 2877 (1990); L. Ruel, V. Pantesco, Y. Lutz, P Simpson, M. Bourouis, ibid. 12, 1657 (1993), E. Siegfried, T. B Chou, N. Perrimon, Cell 71, 1167 (1992).
14. M. Peifer, S. Orsulic, L -M. Pai, J. Loureiro, Dev. Suppl., 163 (1993).
15. E. Siegfried, E. L. Wilder, N Perrimon, Nature 367, 76 (1994)
16. J. Noordermeer, J. Klingensmith, N Perrimon, R. Nusse, ibid, p 80.
17. J. P. Couso, M Bate, A. Martinez-Arias, Science 259, 484 (1993).
18. J A. Williams, S. W Paddock, S. B Carroll, Development 117, 571 (1993).
19. N E. Baker, ibid 102, 489 (1988).
20. R. G. Phillips and J. R S. Whittle, ibid. 118, 427 (1993)
21. J. P Couso, S. Bishop, A. Martinez-Arias, ibid. 120, 621 (1994).
22. J. A. Williams, S. W. Paddock, K. Vorwerk, S B. Carroll, Nature 368, 299 (1994).
23. F. J. Diaz-Benjumea and S M. Cohen, Development 121, 4215 (1995).
24. P. Cubas, J.-P. de Cells, S. Campuzano, J. Modolell, Genes Dev 5, 996 (1991); J. B. Skeath and S. B. Carroll, ibid., p 984.
25. P. Cubas, J.-P. de Cells, S. Campuzano, J. Modolell, Genes Dev 5, 996 (1991); J. B. Skeath and S. B. Carroll, ibid., p 984.
26. V. Hartenstein and J. W. Posakony, Dev Biol 142, 13 (1990); D. L Shellenbarger and J. D. Monter, ibid. 62, 432 (1978).
27. V. Hartenstein and J. W. Posakony, Dev Biol 142, 13 (1990); D. L Shellenbarger and J. D. Monter, ibid. 62, 432 (1978).
28. N. E. Baker, ibid. 125, 96 (1988).
29. H. K. Hing, X. Sun, S. Artavanis-Tsakonas, Mech Dev. 47, 261 (1994)
30. J. P. Couso and A. Martinez-Arias, Cell 79, 259 (1994).
31. M. Gonzáles-Gartán and H. Jäokle, Development 121, 2313 (1995).
32. S. Artavanis-Tsakonas, K. Matsuno, M. E. Fortini, Science 268, 225 (1995).
33. K. A Wharton, K. M. Johansen, T. Xu, S. Artavanis-Tsakonas, Cell 43, 567 (1985); S. Kidd, M. R Kelly, M. W. Young, Mol. Cell. Biol. 6, 3094 (1986).
34. K. A Wharton, K. M. Johansen, T. Xu, S. Artavanis-Tsakonas, Cell 43, 567 (1985); S. Kidd, M. R Kelly, M. W. Young, Mol. Cell. Biol. 6, 3094 (1986).
35. I. Rebay et al., Cell 67, 687 (1991).
36. I. Rebay, R Fehon, S. Artavanis-Tsakonas, ibid 74, 319 (1993).
37. T. Lieber, S. Kidd, E. Alcamo, V Corbin, M. W. Young, Genes Dev. 7, 1949 (1993).
38. D Lyman and M W. Young, Proc. Natl. Acad. Sci U.S.A. 90, 10395 (1993).
39. R. J. Diederich, K Matsuno, H. Hing, S. Artavanis-Tsakonas, Development 120, 473 (1994).
40. K Matsuno, R J Diedrich, M J. Go, C. M Blaumueller, S Artavanis-Tsakonas, ibid. 121, 2633 (1995)
41. M. E. Fortini and S. Artavanis-Tsakonas, Cell 79, 273 (1994).
42. K. Tamura et al., Curr. Biol 5, 1416 (1995).
43. S. Jamault et al., Nature 377, 355 (1995).
44. E. J Rulrfson and S. S. Blair, Development 121, 2813 (1995)
45. J Kim, K. D. Irvine, S. B Carroll, Cell 82, 795 (1995).
46. J P Couso, E. Knust, A Martinez Arias, Curr Biol 5, 1437 (1995).
47. D2 mutation is associated with dominant female sterility and has no effect on development of somatic tissues. The timing of clone induction was determined by collecting white prepupae at timed intervals after heat shock.
48. ΔBem/Rv (27) and Hs:ICN2 (N amino acids 2109 to 2703) was done simultaneously with Hs: dsh in a 1.5-hour pulse during the last 12 hours of third instar to assess their effects on the ectopic bristle response.
49. ΔBem/Rv (27) and Hs:ICN2 (N amino acids 2109 to 2703) was done simultaneously with Hs: dsh in a 1.5-hour pulse during the last 12 hours of third instar to assess their effects on the ectopic bristle response.
50. ΔBem/Rv (27) and Hs:ICN2 (N amino acids 2109 to 2703) was done simultaneously with Hs: dsh in a 1.5-hour pulse during the last 12 hours of third instar to assess their effects on the ectopic bristle response.
51. ΔBem/Rv (27) and Hs:ICN2 (N amino acids 2109 to 2703) was done simultaneously with Hs: dsh in a 1.5-hour pulse during the last 12 hours of third instar to assess their effects on the ectopic bristle response.
52. ΔBem/Rv (27) and Hs:ICN2 (N amino acids 2109 to 2703) was done simultaneously with Hs: dsh in a 1.5-hour pulse during the last 12 hours of third instar to assess their effects on the ectopic bristle response.
53. ΔBem/Rv (27) and Hs:ICN2 (N amino acids 2109 to 2703) was done simultaneously with Hs: dsh in a 1.5-hour pulse during the last 12 hours of third instar to assess their effects on the ectopic bristle response.
54. ΔBem/Rv (27) and Hs:ICN2 (N amino acids 2109 to 2703) was done simultaneously with Hs: dsh in a 1.5-hour pulse during the last 12 hours of third instar to assess their effects on the ectopic bristle response.
55. J. D. Axelrod, unpublished observations.
56. 4 (pH 7.O)], fixed for 20 min in 2% formaldehyde in insect PBS. and stained in X-Gal according to standard methods. Discs were mounted in 80% glycerol and photographed by use of Nomarski optics. To examine SMCs in wild-type discs, y w females were crossed to A101/TM3, Sb males. To assess the effects of Hs.dsh, Hs:dsh females were crossed to A101/TM3, Sb males, and the progeny were heat shocked as described above. In each case, half the discs showed the A707 staining pattern.
57. 4 (pH 7.O)], fixed for 20 min in 2% formaldehyde in insect PBS. and stained in X-Gal according to standard methods. Discs were mounted in 80% glycerol and photographed by use of Nomarski optics. To examine SMCs in wild-type discs, y w females were crossed to A101/TM3, Sb males. To assess the effects of Hs.dsh, Hs:dsh females were crossed to A101/TM3, Sb males, and the progeny were heat shocked as described above. In each case, half the discs showed the A707 staining pattern.
58. A. Brand and N. Perrimon, Development 118, 401 (1993).
59. G Struhl, K. Fitzgerald, I. Greenwald, Cell 74, 331 (1993).
60. S. Yanagawa, F van Leeuwen, A. Wodarz, J Klingensmith, R. Nusse, Genes Dev. 9, 1087 (1995).
61. A yeast interaction trap system was used as described [J Gyuris, E. Golemis, H. Chertkov, R. Brent, Cell 75, 791 (1993)]. Quantitative lac-Z assays were performed [J. H. Miller, Experiments in Molecular Genetics (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1972)]. The bait plasmids expressed either the entire dsh coding region, including amino acids 1 to 638 (Yd4), 1 to 393 (YD4dX), or 286 to 638 (Yd4BN). The "prey" plasmids expressed portions of the cytoplasmic domain of N, including amino acids 1027 to 2258 (ICN1, includes cdc10/ankyrin repeats) and amino acids 2109 to 2703 (ICN2). The assay was performed four independent times on independent isolates. Average values are expressed as a percentage of the positive control (an activation domain covalently linked to the DNA-binding domain). The ICN2 fragment has substantial ability to activate transcription (33, 39) and therefore may amplify the apparent strength of the interaction This activity also precludes the use of ICN2 as a bait.
62. A yeast interaction trap system was used as described [J Gyuris, E. Golemis, H. Chertkov, R. Brent, Cell 75, 791 (1993)]. Quantitative lac-Z assays were performed [J. H. Miller, Experiments in Molecular Genetics (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1972)]. The bait plasmids expressed either the entire dsh coding region, including amino acids 1 to 638 (Yd4), 1 to 393 (YD4dX), or 286 to 638 (Yd4BN). The "prey" plasmids expressed portions of the cytoplasmic domain of N, including amino acids 1027 to 2258 (ICN1, includes cdc10/ankyrin repeats) and amino acids 2109 to 2703 (ICN2). The assay was performed four independent times on independent isolates. Average values are expressed as a percentage of the positive control (an activation domain covalently linked to the DNA-binding domain). The ICN2 fragment has substantial ability to activate transcription (33, 39) and therefore may amplify the apparent strength of the interaction This activity also precludes the use of ICN2 as a bait.
63. Colocalization of Dsh and N was assayed by cotransfection of expression plasmids into Schneider cells (29). Expression constructs placed N and dsh under the inducible control of the Drosophila metallothionein and hsp70 promoters, respectively Capping of N was induced by coculture of the transfected cells with cells expressing Delta To facilitate visualization of Dsh, we inserted two tandem copies of a Myc epitope tag (sequence: EQKLISEEDL) (54) between amino acids 393 and 394. The resulting protein is functional in vivo, because, under control of the dsh promoter, it can rescue a null mutant (39). Dsh was visualized by use of a mouse antibody specific for the Myc epitope, and N was visualized by use of a rat polyclonal antibody. The N expression constructs pTM and pMTECN were as described (29).
64. R. G. Fehon et al , Cell 61, 523 (1990)
65. A. Ghysen, C. Dambly-Chaudière, L. Y. Jan, Y -N. Jan, Genes Dev. 7, 723 (1993).
66. M. E. Fortini, I Rebay, L A. Caron, S. Artavanis-Tsakonas, Nature 365, 555 (1993).
67. C. R. Coffman, P. Skoglund, W A. Harns, C. R Kintner, Cell 73, 659 (1993).
68. S. S. Blair, Dev. Biol. 152, 263 (1992)
69. J. F de Cells and A. Garcia-Bellido, Mech. Dev. 46, 109 (1994)
70. D F. Woods and P. J. Bryant, J. Cell Sci. Suppl. 17, 171 (1993)
71. T. B. Chou and N. Perrimon, Genetics 131, 643 (1992)
72. Abbreviations for the amino acid residues are as follows D, Asp; E, Glu; I, lie; K, Lys; L, Leu; Q, Gln; and S, Ser.
73. We thank J. Klingensmith for construction of the Hs:dsh plasmid; J Noordermeer, M. Young, and G. Struhl for fly stocks; R. Finley and R Brent for plasmids and yeast; and H Chen, M Melnick, and B. Noll for technical help We also thank to A. Manoukian for stimulating discussion and members of the Pernmnon lab for critically reviewing the manuscript We are grateful to A. Manoukian, J. P. Couso, A. Martinez Arias, S. Blair, S. Carroll, and S. Sokol for communicating results before publication. Supported by grants from the National Institutes of Health (J D.A. and N.P.) N P. and S. A.-T. are Investigators of the Howard Hughes Medical Institute