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JOURNAL ARTICLES
Expression of baculovirus P35 prevents cell death in Drosophila
B.A. Hay, T. Wolff, G.M. Rubin
Development 1994 120: 2121-2129;

Summary

The baculovirus P35 protein functions to prevent apoptotic death of infected cells. We have expressed P35 in the developing embryo and eye of the fly Drosophila melanogaster. P35 eliminates most, if not all, normally occurring cell death in these tissues, as well as X-irradiation-induced death. Excess pupal eye cells that are normally eliminated by apoptosis develop into pigment cells when their death is prevented by P35 expression. Our results suggest that one mechanism by which viruses prevent the death of the host cell is to block a cell death pathway that mediates normally occurring cell death. Identification of molecules that interact biochemically or genetically with P35 in Drosophila should provide important insights into how cell death is regulated.

REFERENCES

    1. Abrams J. K.,
    2. White K.,
    3. Fessler L. I.,
    4. Steller H.
    (1993) Programmed cell death during Drosophila embryogenesis. Development 117, 29–43
    OpenUrlAbstract/FREE Full Text
    1. Avery L.,
    2. Horvitz H. R.
    (1987) A cell that dies during wild-type C. elegans development can function as a neuron in a ced-3 mutant. Cell 51, 1071–1078
    OpenUrlCrossRefPubMedWeb of Science
    1. Bissonette R. P.,
    2. Echeverri F.,
    3. Mahboubi A.,
    4. Green D. R.
    (1992) Apoptotic cell death induced by c-myc inhibited by bcl-2. Nature 359, 552–554
    OpenUrlCrossRefPubMed
    1. Bonini N. M.,
    2. Leiserson W. M.,
    3. Benzer S.
    (1993) The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72, 379–395
    OpenUrlCrossRefPubMedWeb of Science
    1. Brand A. H.,
    2. Perrimon N.
    (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
    OpenUrlAbstract
    1. Cagan R. L.,
    2. Ready D. F.
    (1989) The emergence of order in the Drosophila pupal retina. Dev. Biol 136, 346–362
    OpenUrlCrossRefPubMedWeb of Science
    1. Chou J.,
    2. Roizman B.
    (1992) The y134. 5 gene of herpes simplex virus 1 precludes neuroblastoma cells from triggering total shutoff of protein synthesis characteristic of programmed cell death in neuronal cells. Proc. Natl. Acad. Sci. USA 89, 3266–3270
    OpenUrlAbstract/FREE Full Text
    1. Clarke A. R.,
    2. Purdie C. A.,
    3. Harrison D. J.,
    4. Morris R. G.,
    5. Bird C. C.,
    6. Hooper M. L.,
    7. Wyllie A. H.
    (1993) Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature 362, 849–852
    OpenUrlCrossRefPubMedWeb of Science
    1. Clem R. J.,
    2. Fechheimer M.,
    3. Miller L. K.
    (1991) Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254, 1388–1390
    OpenUrlAbstract/FREE Full Text
    1. Clem R. J.,
    2. Miller L. K.
    (1993) Apoptosis reduces both the in vitro replication and the in vivo infectivity of a baculovirus. J. Virol 67, 3730–3738
    OpenUrlAbstract/FREE Full Text
    1. Clouston W. M.,
    2. Kerr J. F. R.
    (1985) Apoptosis, lymphocytotoxicity and the containment of viral infections. Med. Hypoth 18, 399–404
    OpenUrlCrossRefPubMedWeb of Science
    1. Crook N. E.,
    2. Clem R. J.,
    3. Miller L. K.
    (1993) An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol 67, 2168–2174
    OpenUrlAbstract/FREE Full Text
    1. Ellis R. E.,
    2. Yuan J.,
    3. Horvitz H. R.
    (1991) Mechanisms and functions of cell death. Annu. Rev. Cell Biol 7, 663–698
    OpenUrlCrossRefWeb of Science
    1. Ellis M. C.,
    2. O'Neill E. M.,
    3. Rubin G. M.
    (1993) Expression of Drosophila glass protein and evidence for negative regulation of its activity in non-neuronal cells by another DNA-binding protein. Development 119, 855–865
    OpenUrlAbstract/FREE Full Text
    1. Evan G. I.,
    2. Wyllie A. H.,
    3. Gilbert C. S.,
    4. Littlewood T. D.,
    5. Land H.,
    6. Brooks M.,
    7. Waters C. M.,
    8. Penn L. Z.,
    9. Hancock D. C.
    (1992) Induction of apoptosis in fibroblasts by c-myc protein. Cell 69, 119–128
    OpenUrlCrossRefPubMedWeb of Science
    1. Fairbairn L. J.,
    2. Cowling G. J.,
    3. Reipert B. M.,
    4. Dexter T. M.
    (1993) Suppression of apoptosis allows differentiation and development of a multipotent hemopoietic cell line in the absence of added growth factors. Cell 74, 823–832
    OpenUrlCrossRefPubMedWeb of Science
    1. Glucksmann A.
    (1950) Cell deaths in normal and vertebrate ontogeny. Biol. Rev. Cambridge Philos. Soc 26, 59–86
    OpenUrl
    1. Gooding L. R.,
    2. Elmore L. W.,
    3. Tollefson A. E.,
    4. Brady H. A.,
    5. Wold W. S. M.
    (1988) A 14,700 MW protein from the E3 region of adenovirus inhibits cytolysis by tumor necrosis factor. Cell 53, 341–346
    OpenUrlCrossRefPubMedWeb of Science
    1. Gooding L. R.,
    2. Ranheim T. S.,
    3. Tollefson A. E.,
    4. Aquino L.,
    5. Duerksen-Hughes P. J.,
    6. Horton T. M.,
    7. Wold W. S. M.
    (1991) The 10,400-and 14,500-dalton proteins encoded by region E3 of adenovirus function together to protect many but not all mouse cell lines against lysis by tumor necrosis factor. J. Virol 65, 4114–4123
    OpenUrlAbstract/FREE Full Text
    1. Gooding L. R.,
    2. Aquino L.,
    3. Duerlsen-Hughes P. J.,
    4. Day D.,
    5. Horton T. M.,
    6. Yei S.,
    7. Wold W. S. M.
    (1991) The E1B-19K protein of group C adenoviruses prevents cytolysis by tumor necrosis factor of human cells but not mouse cells. J. Virol 65, 3083–3094
    OpenUrlAbstract/FREE Full Text
    1. Gregory C. D.,
    2. Dive C.,
    3. Henderson S.,
    4. Smith C. A.,
    5. Williams G. T.,
    6. Gordon J.,
    7. Rickson A. B.
    (1991) Activation of Epstein-Barr virus latent genes protects human B cells from death by apoptosis. Nature 349, 612–614
    OpenUrlCrossRefPubMedWeb of Science
    1. Hashimoto S.,
    2. Ishii A.,
    3. Yonehara S.
    (1991) The E1B oncogene of adenovirus confers cellular resistance to cytotoxicity of tumor necrosis factor and monoclonal anti-Fas antibody. Int. Immunol 3, 343–351
    OpenUrlAbstract/FREE Full Text
    1. Hay B. A.,
    2. Ackerman L.,
    3. Barbel S.,
    4. Han L.,
    5. Jan Y. N.
    (1988) Identification of a component of Drosophila polar granules. Development 103, 625–640
    OpenUrlAbstract/FREE Full Text
    1. Henderson S.,
    2. Rowe M.,
    3. Gregory C.,
    4. Croom-Carter D.,
    5. Wang F.,
    6. Longnecker R.,
    7. Kieff E.,
    8. Rickinson A.
    (1991) Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 65, 1107–1115
    OpenUrlCrossRefPubMedWeb of Science
    1. Henderson S.,
    2. Huen D.,
    3. Rowe M.,
    4. Dawson C.,
    5. Johnson G.,
    6. Rickson A.
    (1993) Epstein-Barr virus-coded BHRF1 protein, a viral homologue of Bcl-2, protects human B cells from programmed cell death. Proc. Natl. Acad. Sci. USA 90, 8479–8483
    OpenUrlAbstract/FREE Full Text
    1. Hiromi Y.,
    2. Gehring W. J.
    (1987) Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell 50, 963–974
    OpenUrlCrossRefPubMedWeb of Science
    1. Levine B.,
    2. Huang Q.,
    3. Isaacs J. T.,
    4. Reed J. C.,
    5. Griffin D. E.,
    6. Hardwick J. M.
    (1993) Conversion of lytic to persistent alpha-virus infection by the bcl-2 cellular oncogene. Nature 361, 739–742
    OpenUrlCrossRefPubMed
    1. Lowe S. W.,
    2. Schmitt E. M.,
    3. Smith S. W.,
    4. Osborne B. A.,
    5. Jacks T.
    (1993) p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362, 847–849
    OpenUrlCrossRefPubMedWeb of Science
    1. Martz E.,
    2. Howell D. M.
    (1989) CTL: virus control cells first and cytolytic cells second?. Immunol. Today 10, 79–86
    OpenUrlCrossRefPubMedWeb of Science
    1. Meyaard L.,
    2. Otto S. A.,
    3. Jonker R. R.,
    4. Mijnster M. J.,
    5. Keet P. M.,
    6. Miedema F.
    (1992) Programmed death of T cells in HIV-1 infection. Science 257, 217–219
    OpenUrlAbstract/FREE Full Text
    1. Moses K.,
    2. Ellis M. C.,
    3. Rubin G. M.
    (1991) glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes and Devel 5, 583–593
    OpenUrlAbstract/FREE Full Text
    1. Murphy K. M.,
    2. Heimberger A. B.,
    3. Loh D. Y.
    (1990) Induction by antigen of intrathymic apoptosis of CD4+ CD8+ TCRldegthymocytes in vivo. Science 250, 1720–1723
    OpenUrlAbstract/FREE Full Text
    1. Pilder S.,
    2. Logan J.,
    3. Shenk T.
    (1984) Deletion of the gene encoding theadenovirus 5 early region 1B- 21,000-molecular weight polypeptide leads to degradation of viral and cellular DNA. J. Virol 52, 664–671
    OpenUrlAbstract/FREE Full Text
    1. Rabizadeh S.,
    2. LaCount D. J.,
    3. Friesen P. D.,
    4. Bredesen D. E.
    (1993) Expression of the baculovirus p35 gene inhibits mammalian cell death. J. Neurochem 61, 2318–2321
    OpenUrlCrossRefPubMedWeb of Science
    1. Raff M. C.
    (1992) Social control on cell survival and cell death. Nature 356, 397–400
    OpenUrlCrossRefPubMed
    1. Rubin G. M.,
    2. Spradling A. C.
    (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218, 348–353
    OpenUrlAbstract/FREE Full Text
    1. Subramanian T.,
    2. Kuppuswamy M.,
    3. Gysbers J.,
    4. Mak S.,
    5. Chinnadurai G.
    (1984) kDa tumor antigen coded by early region E1b of adenovirus 2 is required for efficient synthesis and for protection of viral DNA. J. Biol. Chem 259, 11777–11783
    OpenUrlAbstract/FREE Full Text
    1. White E.,
    2. Stillman B.
    (1987) Expression of the adenovirus E1B mutant phenotypes is dependent on the host cell and on the synthesis of E1A proteins. J. Virol 61, 426–435
    OpenUrlAbstract/FREE Full Text
    1. White E.,
    2. Sabbatini P.,
    3. Debbas M.,
    4. Wold W. S. M.,
    5. Kusher D. I.,
    6. Gooding L. R.
    (1992) The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor alpha. Mol. Cell. Biol 12, 2570–2580
    OpenUrlAbstract/FREE Full Text
    1. Winberg M. L.,
    2. Perez S. E.,
    3. Steller H.
    (1992) Generation and early differentiation of glial cells in the first optic ganglion of Drosophila melanogaster. Development 115, 903–911
    OpenUrlAbstract
    1. Wolff T.,
    2. Ready D. F.
    (1991) Cell death in normal and rough eye mutants of Drosophila. Development 113, 825–839
    OpenUrlAbstract
    1. Wyllie A. H.,
    2. Kerr J. F. R.,
    3. Currie A.
    (1980) Cell death: the significance of apoptosis. Int. Rev. Cytol 68, 251–306
    OpenUrlCrossRefPubMed
    1. Yonish-Rouach E.,
    2. Resnitzky D.,
    3. Lotem J.,
    4. Sachs L.,
    5. Kimchi A.,
    6. Oren M.
    (1991) Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature 352, 345–347
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Expression of baculovirus P35 prevents cell death in Drosophila
B.A. Hay, T. Wolff, G.M. Rubin
Development 1994 120: 2121-2129;
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