Abstract
Transgenic flies in which ectopic expression of human p53 was targeted to the Drosophila eye imaginal disc were established. On sectioning of adult fly eyes which displayed a severe rough eye phenotype, most ommatidia were found to be fused and irregular shapes of rabdomeres were observed. In addition, many pigment cells were lost. In the developing eye imaginal disc, photoreceptor cell differentiation was initiated normally despite the ectopic expression of p53. However, expression of p53 inhibited cell cycle progression in eye imaginal disc cells and the S phase zone (the second mitotic wave) behind the morphogenetic furrow was almost completely abolished. Furthermore, expression of p53 induced extensive apoptosis of eye imaginal disc cells, and co-expression of baculovirus P35 in the eye imaginal disc suppressed the p53-induced rough eye phenotype. These results are consistent with the known functions of human p53 and indicate the existence of signaling systems with elements corresponding to human p53 in Drosophila eye imaginal disc cells. Genetic crosses of transgenic flies expressing p53 to a collection of Drosophila deficiency stocks allowed us to identify several genomic regions, deletions of which caused enhancement or suppression of the p53-induced rough eye phenotype. The transgenic flies established in this study should be useful to identify novel targets of p53 and its positive or negative regulators in Drosophila.
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References
Almong N and Rotter V. . 1997 Biochim. Biophys. Acta. 1333: F1–F27.
Bertin J, Mendrysa SM, LaCount DJ, Gauer S, Krebs JF, Armstrong RC, Tomaselli KJ and Friesen PD. . 1996 J. Virol. 70: 6251–6259.
Brand AH and Perrimon N. . 1993 Development 118: 401–415.
Bump NJ, Hackett M, Hugunin M, Seshagiri M, Brady K, Chen P, Ferenz C, Franklin S, Ghayur T, Li P, et al. 1995 Science 269: 1885–1888.
Butler SJ, Ray S and Hiromi Y. . 1997 Development 124: 781–792.
Chen P, Nordstrom W, Gish B and Abrams JM. . 1996a Genes Dev. 10: 1773–1782.
Chen X, Ko LJ, Jayaraman L and Prives C. . 1996b Genes Dev. 10: 2438–2451.
Crook NE, Clem RJ and Miller LK. . 1993 J. Virol. 67: 2168–2174.
de Nooij JC, Letendre MA and Hariharan IK. . 1996 Cell 87: 1237–1247.
Du W, Vidal M, Xie J-E and Dyson N. . 1996 Genes Dev. 10: 1206–1218.
Foley K and Cooley L. . 1998 Development 125: 1075–1082.
Gallant P, Shiio Y, Cheng PF, Parkhurst SM and Eisenman RN. . 1996 Science 274: 1523–1527.
Grether ME, Abrams JM, Agapite J, White K and Steller H. . 1995 Genes Dev. 9: 1694–1708.
Hay BA, Wolff T and Rubin GM. . 1994 Development 120: 2121–2129.
Hengartner MO. . 1995 Science 270: 931.
Kaghad M, Bonnet H, Yang A, Creancier L, Biscan J-C, Valent A, Minty A, Chalon P, Lelias J-M, Dumont X, Ferrara P, Mckeon F and Caput D. . 1997 Cell 90: 809–819.
Kastan MB, Onyekwere O, Sidransky D, Vogelstein B and Craig RW. . 1991 Cancer Res. 51: 6304–6311.
Kastan MB, Zhan Q, El-Deiry WS, Carrier F, Jacks T, Walsh WV, Plunket BS, Vogelstein B and Fornace AJ. . 1992 Cell 71: 587–597.
Kiyono T, Hiraiwa A, Ishii S, Takahashi T and Ishibashi M. . 1994 J. Virol. 68: 4656–4661.
Ko LJ and Prives C. . 1996 Genes and Development 10: 1054–1072.
Kuerbiyz SJ, Plunkett BS, Walsh WV and Kastan MB. . 1992 Proc. Natl. Acad. Sci. USA 89: 7491–7495.
Lane DP. . 1992 Nature 358: 15–16.
Lee S, Elenbaas B, Levine A and Griffith J. . 1995 Cell 81: 1013–1020.
Levine A. . 1997 Cell 88: 323–331.
Livingston LR, White A, Sprouse J, Livanos E, Jacks T and Tlsty TD. . 1992 Cell 70: 923–935.
Maltzman W and Czyzyk L. . 1984 Mol. Cell. Biol. 4: 1689–1694.
McCall K and Steller H. . 1997 Trends Genet. 13: 222–226.
Moses K and Rubin G. . 1991 Genes Dev. 5: 583–593.
Norimura T, Nomoto S, Katsuki M, Gondo Y and Kondo S. . 1996 Nature Med. 2: 577–580.
Robertson HM, Preston CR, Philips RW, Johnson-Schlitz DM, Benz WK and Engels WR. . 1988 Genetics 118: 461–470.
Sakamuro D, Sabbatini P, White E and Prendergast GC. . 1997 Oncogene 15: 887–898.
Sanchez Y and Elledge JS. . 1995 BioAssays 17: 545–548.
Soussi T, de Fromentel CC and May P. . 1990 Oncogene 5: 945–952.
Spradling AC. . 1986 Drosophila: a practical approach. Roberts DB. (ed.).. IRL Press: Oxford pp.175–197.
Takahashi T, D'Amico D, Chiba I, Buchhagen DL and Minna JD. . 1990 J. Clin. Invest. 86: 363–369.
Takahashi T, Carbone D, Takahashi T, Nau MM, Hida T, Linnoila I, Ueda R and Minna JD. . 1992 Cancer Res. 52: 2340–2343.
Wang XW, Vermeulen W, Coursen JD, Gibson M, Lupold SE, Forrester K, Xu G, Elmore L, Yeh H, Hoeijmakers JH and Harris CC. . 1996 Genes Dev. 10: 1219–1232.
White K, Grether M, Abrams J, Young L, Farrell K and Steller H. . 1994 Science 264: 677–683.
Wilder EL and Perrimon N. . 1995 Development 121: 477–488.
Wolff T and Ready DF. . 1991 Development 113: 825–839.
Wolff T and Ready DF. . 1993 The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York pp.1277–1326.
Xue D and Horvitz R. . 1995 Nature 377: 248–251.
Yamaguchi M, Hayashi Y, Matsuoka S, Takahashi T and Matsukage A. . 1994 Eur. J. Biochem. 221: 227–237.
Zhou Q, Krebs JF, Snipas SJ, Price A, Alnemri ES, Tomaselli KJ and Salvesen GS. . 1998 Biochemistry 37: 10757–10765.
Zhou X, Wang XW, Xu L, Hagiwara K, Nagashima M, Wolkowicz R, Zurer I, Rotter V and Harris CC. . 1999 Cancer Res. 59: 843–848.
Zhu J, Jiang J, Zhou W, Zhu K and Chen X. . 1999 Oncogene 18: 2149–2155.
Acknowledgements
We are grateful to Drs S Hayashi, Y Nishida, G Rubin, B Hay, I Hariharan and Y Hiromi for fly stocks; N Perrimon for pUAST and pGaTB; T Takahashi for pcNXRS, pcH5FR and pcH6FR; T Kiyono for pCMVp53C234; Y Hiromi for anti-elav antibody; K Inada and T Kiyono for anti-human p53 antibodies and M Moore for critical reading of the manuscript. This work was supported in part by grants-in-aid from the Ministry of Education, Science, Sports and Culture of Japan.
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Yamaguchi, M., Hirose, F., Inoue, Y. et al. Ectopic expression of human p53 inhibits entry into S phase and induces apoptosis in the Drosophila eye imaginal disc. Oncogene 18, 6767–6775 (1999). https://doi.org/10.1038/sj.onc.1203113
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DOI: https://doi.org/10.1038/sj.onc.1203113
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