1887

Abstract

Ectromelia virus (EV) virulence factor p28 (EVp28) is a member of a family of poxvirus proteins that are defined largely by the presence of a C-terminal RING finger motif and localization to virus factories within the cytoplasm of infected cells. Previously, overexpression of the Shope fibroma virus (SFV) homologue, N1R, in vaccinia virus (VV)-infected BGMK cells was found to inhibit virus-induced apoptosis. Here, we report that both EVp28 and overexpression of SFV N1R in poxvirus-infected HeLa cells protect specifically from UV light-induced apoptosis, but not from apoptosis induced by Fas or TNF. Further, we report that both VV and EV protect from apoptosis induced by UV, Fas and TNF. Immunoblot analysis indicates that EVp28 acts upstream of caspase-3, blocking activation of the protease in response to UV irradiation. Although no difference was found in replication of an EVp28 mutant virus, which expresses a truncated p28 protein lacking the RING motif, compared to EV wild-type in HeLa cells, UV irradiation of infected HeLa cells reduced the replication of the EV mutant compared with wild-type EV.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-4-1087
2000-04-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/4/0811087a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-4-1087&mimeType=html&fmt=ahah

References

  1. Afonso, C. L., Tulman, E. R., Lu, Z., Oma, E., Kutish, G. F. & Rock, D. L. (1999). The genome of Melanoplus sanguinipes entomopoxvirus.Journal of Virology 73, 533-552. [Google Scholar]
  2. Barry, M., Hnatiuk, S., Mossman, K., Lee, S. F., Boshkov, L. & McFadden, G. (1997). The myxoma virus M-T4 gene encodes a novel RDEL-containing protein that is retained within the endoplasmic reticulum and is important for the productive infection of lymphocytes.Virology 239, 360-377.[CrossRef] [Google Scholar]
  3. Berra, E., Municio, M. M., Sanz, L., Frutos, S., Diaz-Meco, M. T. & Moscat, J. (1997). Positioning atypical protein kinase C isoforms in the UV-induced apoptotic signaling cascade.Molecular and Cellular Biology 17, 4346-4354. [Google Scholar]
  4. Bertin, J., Armstrong, R. C., Ottilie, S., Martin, D. A., Wang, Y., Banks, S., Wang, G. H., Senkevich, T. G., Alnemri, E. S., Moss, B., Lenardo, M. J., Tomaselli, K. J. & Cohen, J. I. (1997). Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis.Proceedings of the National Academy of Sciences, USA 94, 1172-1176.[CrossRef] [Google Scholar]
  5. Boldin, M. P., Goncharov, T. M., Goltsev, Y. V. & Wallach, D. (1996). Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death.Cell 85, 803-815.[CrossRef] [Google Scholar]
  6. Borden, K. L. & Freemont, P. S. (1996). The RING finger domain: a recent example of a sequence–structure family.Current Opinion in Structural Biology 6, 395-401.[CrossRef] [Google Scholar]
  7. Brash, D. E., Ziegler, A., Jonason, A. S., Simon, J. A., Kunala, S. & Leffell, D. J. (1996). Sunlight and sunburn in human skin cancer: p53, apoptosis, and tumor promotion.Journal of Investigative Dermatology Symposium Proceedings 1, 136-142. [Google Scholar]
  8. Brick, D. J., Burke, R. D., Schiff, L. & Upton, C. (1998). Shope fibroma virus RING finger protein N1R binds DNA and inhibits apoptosis.Virology 249, 42-51.[CrossRef] [Google Scholar]
  9. Buckbinder, L., Talbott, R., Velasco-Miguel, S., Takenaka, I., Faha, B., Seizinger, B. R. & Kley, N. (1995). Induction of the growth inhibitor IGF-binding protein 3 by p53.Nature 377, 646-649.[CrossRef] [Google Scholar]
  10. Buller, R. M. L. & Palumbo, G. J. (1991). Poxvirus pathogenesis.Microbiological Reviews 55, 80-122. [Google Scholar]
  11. Caelles, C., Helmberg, A. & Karin, M. (1994). p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes.Nature 370, 220-223.[CrossRef] [Google Scholar]
  12. Cao, J. X., Gershon, P. D. & Black, D. N. (1995). Sequence analysis of HindIII Q2 fragment of capripoxvirus reveals a putative gene encoding a G-protein-coupled chemokine receptor homologue.Virology 209, 207-212.[CrossRef] [Google Scholar]
  13. Chinnaiyan, A. M., O’Rourke, K., Tewari, M. & Dixit, V. M. (1995). FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis.Cell 81, 505-512.[CrossRef] [Google Scholar]
  14. Chinnaiyan, A. M., Tepper, C. G., Seldin, M. F., O’Rourke, K., Kischkel, F. C., Hellbardt, S., Krammer, P. H., Peter, M. E. & Dixit, V. M. (1996). FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis.Journal of Biological Chemistry 271, 4961-4965.[CrossRef] [Google Scholar]
  15. Crook, N. E., Clem, R. J. & Miller, L. K. (1993). An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif.Journal of Virology 67, 2168-2174. [Google Scholar]
  16. Denning, M. F., Wang, Y., Nickoloff, B. J. & Wrone-Smith, T. (1998). Protein kinase Cδ is activated by caspase-dependent proteolysis during ultraviolet radiation-induced apoptosis of human keratinocytes.Journal of Biological Chemistry 273, 29995-30002.[CrossRef] [Google Scholar]
  17. Dobbelstein, M. & Shenk, T. (1996). Protection against apoptosis by the vaccinia virus SPI-2 (B13R) gene product.Journal of Virology 70, 6479-6485. [Google Scholar]
  18. Elder, D. E. (1989). Human melanocytic neoplasms and their etiologic relationship with sunlight.Journal of Investigative Dermatology 92, 297S-303S.[CrossRef] [Google Scholar]
  19. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A. & Nagata, S. (1998). A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD.Nature 391, 43-50.[CrossRef] [Google Scholar]
  20. Frasch, S. C., Nick, J. A., Fadok, V. A., Bratton, D. L., Worthen, G. S. & Henson, P. M. (1998). p38 mitogen-activated protein kinase-dependent and -independent intracellular signal transduction pathways leading to apoptosis in human neutrophils.Journal of Biological Chemistry 273, 8389-8397.[CrossRef] [Google Scholar]
  21. Freemont, P. S. (1993). The RING finger. A novel protein sequence motif related to the zinc finger.Annals of the New York Academy of Sciences 684, 174-192.[CrossRef] [Google Scholar]
  22. Frutos, S., Moscat, J. & Diaz-Meco, M. T. (1999). Cleavage of zetaPKC but not lambda/iotaPKC by caspase-3 during UV-induced apoptosis.Journal of Biological Chemistry 274, 10765-10770.[CrossRef] [Google Scholar]
  23. Graham, K. A., Lalani, A. S., Macen, J. L., Ness, T. L., Barry, M., Liu, L. Y., Lucas, A., Clark-Lewis, I., Moyer, R. W. & McFadden, G. (1997). The T1/35kDa family of poxvirus-secreted proteins bind chemokines and modulate leukocyte influx into virus-infected tissues.Virology 229, 12-24.[CrossRef] [Google Scholar]
  24. Green, D. R. (1998). Apoptotic pathways: the roads to ruin.Cell 94, 695-698.[CrossRef] [Google Scholar]
  25. Griffiths, H. R., Mistry, P., Herbert, K. E. & Lunec, J. (1998). Molecular and cellular effects of ultraviolet light-induced genotoxicity.Critical Reviews in Clinical Laboratory Sciences 35, 189-237.[CrossRef] [Google Scholar]
  26. Gujuluva, C. N., Baek, J. H., Shin, K. H., Cherrick, H. M. & Park, N. H. (1994). Effect of UV-irradiation on cell cycle, viability and the expression of p53, gadd153 and gadd45 genes in normal and HPV-immortalized human oral keratinocytes.Oncogene 9, 1819-1827. [Google Scholar]
  27. Han, Z., Malik, N., Carter, T., Reeves, W. H., Wyche, J. H. & Hendrickson, E. A. (1996). DNA-dependent protein kinase is a target for a CPP32-like apoptotic protease.Journal of Biological Chemistry 271, 25035-25040.[CrossRef] [Google Scholar]
  28. Haupt, Y., Rowan, S., Shaulian, E., Vousden, K. H. & Oren, M. (1995). Induction of apoptosis in HeLa cells by trans-activation-deficient p53.Genes & Development 9, 2170-2183.[CrossRef] [Google Scholar]
  29. Havre, P. A., Yuan, J., Hedrick, L., Cho, K. R. & Glazer, P. M. (1995). p53 inactivation by HPV16 E6 results in increased mutagenesis in human cells.Cancer Research 55, 4420-4424. [Google Scholar]
  30. Havre, P. A., Rice, M. C., Noe, M. & Kmiec, E. B. (1998). The human REC2/RAD51B gene acts as a DNA damage sensor by inducing G1 delay and hypersensitivity to ultraviolet irradiation.Cancer Research 58, 4733-4739. [Google Scholar]
  31. Israeli, D., Tessler, E., Haupt, Y., Elkeles, A., Wilder, S., Amson, R., Telerman, A. & Oren, M. (1997). A novel p53-inducible gene, PAG608, encodes a nuclear zinc finger protein whose overexpression promotes apoptosis.EMBO Journal 16, 4384-4392.[CrossRef] [Google Scholar]
  32. Janicke, R. U., Sprengart, M. L., Wati, M. R. & Porter, A. G. (1998). Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis.Journal of Biological Chemistry 273, 9357-9360.[CrossRef] [Google Scholar]
  33. Kettle, S., Alcamı́, A., Khanna, A., Ehret, R., Jassoy, C. & Smith, G. L. (1997). Vaccinia virus serpin B13R (SPI-2) inhibits interleukin-1β-converting enzyme and protects virus-infected cells from TNF- and Fas-mediated apoptosis, but does not prevent IL-1β-induced fever.Journal of General Virology 78, 677-685. [Google Scholar]
  34. Kibler, K. V., Shors, T., Perkins, K. B., Zeman, C. C., Banaszak, M. P., Biesterfeldt, J., Langland, J. O. & Jacobs, B. L. (1997). Double-stranded RNA is a trigger for apoptosis in vaccinia virus-infected cells.Journal of Virology 71, 1992-2003. [Google Scholar]
  35. Kimura, C., Zhao, Q. L., Kondo, T., Amatsu, M. & Fujiwara, Y. (1998). Mechanism of UV-induced apoptosis in human leukemia cells: roles of Ca2+/Mg2+-dependent endonuclease, caspase-3, and stress-activated protein kinases.Experimental Cell Research 239, 411-422.[CrossRef] [Google Scholar]
  36. Kluck, R. M., Bossy-Wetzel, E., Green, D. R. & Newmeyer, D. D. (1997). The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis.Science 275, 1132-1136.[CrossRef] [Google Scholar]
  37. Kuida, K., Zheng, T. S., Na, S., Kuan, C., Yang, D., Karasuyama, H., Rakic, P. & Flavell, R. A. (1996). Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice.Nature 384, 368-372.[CrossRef] [Google Scholar]
  38. Lane, D. P. (1992). Cancer. p53, guardian of the genome.Nature 358, 15-16.[CrossRef] [Google Scholar]
  39. Lee, S. B. & Esteban, M. (1994). The interferon-induced double-stranded RNA-activated protein kinase induces apoptosis.Virology 199, 491-496.[CrossRef] [Google Scholar]
  40. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S. & Wang, X. (1997). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade.Cell 91, 479-489.[CrossRef] [Google Scholar]
  41. Liu, M. & Pelling, J. C. (1995). UV-B/A irradiation of mouse keratinocytes results in p53-mediated WAF1/CIP1 expression.Oncogene 10, 1955-1960. [Google Scholar]
  42. Liu, X., Kim, C. N., Yang, J., Jemmerson, R. & Wang, X. (1996). Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c.Cell 86, 147-157.[CrossRef] [Google Scholar]
  43. Lowe, S. W., Schmitt, E. M., Smith, S. W., Osborne, B. A. & Jacks, T. (1993). p53 is required for radiation-induced apoptosis in mouse thymocytes.Nature 362, 847-849.[CrossRef] [Google Scholar]
  44. Lu, A. & Miller, L. K. (1995). The roles of eighteen baculovirus late expression factor genes in transcription and DNA replication.Journal of Virology 69, 975-982. [Google Scholar]
  45. Macen, J. L., Graham, K. A., Lee, S. F., Schreiber, M., Boshkov, L. K. & McFadden, G. (1996). Expression of the myxoma virus tumor necrosis factor receptor homologue and M11L genes is required to prevent virus-induced apoptosis in infected rabbit T lymphocytes.Virology 218, 232-237.[CrossRef] [Google Scholar]
  46. McFadden, G. & Barry, M. (1998). How poxviruses oppose apoptosis.Seminars in Virology 8, 429-442.[CrossRef] [Google Scholar]
  47. Maltzman, W. & Czyzyk, L. (1984). UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells.Molecular and Cellular Biology 4, 1689-1694. [Google Scholar]
  48. Martin, S. J. & Cotter, T. G. (1991). Ultraviolet B irradiation of human leukaemia HL-60 cells in vitro induces apoptosis.International Journal of Radiation Biology 59, 1001-1016.[CrossRef] [Google Scholar]
  49. Martin, S. J., Newmeyer, D. D., Mathias, S., Farschon, D. M., Wang, H. G., Reed, J. C., Kolesnick, R. N. & Green, D. R. (1995). Cell-free reconstitution of Fas-, UV radiation- and ceramide-induced apoptosis.EMBO Journal 14, 5191-5200. [Google Scholar]
  50. Medema, J. P., Scaffidi, C., Kischkel, F. C., Shevchenko, A., Mann, M., Krammer, P. H. & Peter, M. E. (1997). FLICE is activated by association with the CD95 death-inducing signaling complex (DISC).EMBO Journal 16, 2794-2804.[CrossRef] [Google Scholar]
  51. Messud-Petit, F., Gelfi, J., Delverdier, M., Amardeilh, M. F., Py, R., Sutter, G. & Bertagnoli, S. (1998). Serp2, an inhibitor of the interleukin-1β-converting enzyme, is critical in the pathobiology of myxoma virus.Journal of Virology 72, 7830-7839. [Google Scholar]
  52. Miller, M. L., Andringa, A., Elliott, J., Conwell, K.II, Dixon, K. & Carty, M. P. (1998). The morphological and spectral phenotype of apoptosis in HeLa cells varies following exposure to UV-C and the addition of inhibitors of ICE and CPP32.Cell Proliferation 31, 17-33.[CrossRef] [Google Scholar]
  53. Miyashita, T., Krajewski, S., Krajewska, M., Wang, H. G., Lin, H. K., Liebermann, D. A., Hoffman, B. & Reed, J. C. (1994). Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo.Oncogene 9, 1799-1805. [Google Scholar]
  54. Moore, M., Horikoshi, N. & Shenk, T. (1996). Oncogenic potential of the adenovirus E4orf6 protein.Proceedings of the National Academy of Sciences, USA 93, 11295-11301.[CrossRef] [Google Scholar]
  55. Mossman, K., Lee, S. F., Barry, M., Boshkov, L. & McFadden, G. (1996). Disruption of M-T5, a novel myxoma virus gene member of poxvirus host range superfamily, results in dramatic attenuation of myxomatosis in infected European rabbits.Journal of Virology 70, 4394-4410. [Google Scholar]
  56. Muzio, M., Chinnaiyan, A. M., Kischkel, F. C., O’Rourke, K., Shevchenko, A., Ni, J., Scaffidi, C., Bretz, J. D., Zhang, M., Gentz, R., Mann, M., Krammer, P. H., Peter, M. E. & Dixit, V. M. (1996). FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex.Cell 85, 817-827.[CrossRef] [Google Scholar]
  57. Natuk, R. J. & Holowczak, J. A. (1985). Vaccinia virus proteins on the plasma membrane of infected cells. III. Infection of peritoneal macrophages.Virology 147, 354-372.[CrossRef] [Google Scholar]
  58. Nemoto, S., Xiang, J., Huang, S. & Lin, A. (1998). Induction of apoptosis by SB202190 through inhibition of p38β mitogen-activated protein kinase.Journal of Biological Chemistry 273, 16415-16420.[CrossRef] [Google Scholar]
  59. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A. and others (1995). Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376, 37–43.[CrossRef] [Google Scholar]
  60. Nicoletti, I., Migliorati, G., Pagliacci, M. C., Grignani, F. & Riccardi, C. (1991). A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry.Journal of Immunological Methods 139, 271-279.[CrossRef] [Google Scholar]
  61. Okan, I., Wang, Y., Chen, F., Hu, L. F., Imreh, S., Klein, G. & Wiman, K. G. (1995). The EBV-encoded LMP1 protein inhibits p53-triggered apoptosis but not growth arrest.Oncogene 11, 1027-1031. [Google Scholar]
  62. Papadimitriou, J. M. & van Bruggen, I. (1993). Quantitative investigations of apoptosis of murine mononuclear phagocytes during mild hyperthermia.Experimental and Molecular Pathology 59, 1-12.[CrossRef] [Google Scholar]
  63. Papadimitriou, J. M., Murch, A. R. & van Bruggen, I. (1980). A cytogenetic and cytophotometric analysis of resident and exudate murine macrophages.Journal of Pathology 131, 175-182.[CrossRef] [Google Scholar]
  64. Porter, A. G. & Janicke, R. U. (1999). Emerging roles of caspase-3 in apoptosis.Cell Death and Differentiation 6, 99-104.[CrossRef] [Google Scholar]
  65. Quan, L. T., Caputo, A., Bleackley, R. C., Pickup, D. J. & Salvesen, G. S. (1995). Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A.Journal of Biological Chemistry 270, 10377-10379.[CrossRef] [Google Scholar]
  66. Rivas, C., Gil, J., Melkova, Z., Esteban, M. & Diaz-Guerra, M. (1998). Vaccinia virus E3L protein is an inhibitor of the interferon (i.f.n.)-induced 2-5A synthetase enzyme.Virology 243, 406-414.[CrossRef] [Google Scholar]
  67. Roberts, J. A. (1964a). Enhancement of the virulence of attenuated ectromelia virus in mice maintained in a cold environment.Australian Journal of Experimental Biology and Medical Science 42, 657-666.[CrossRef] [Google Scholar]
  68. Roberts, J. A. (1964b). Growth of virulent and attenuated ectromelia virus in cultured macrophages from normal and ectromelia immune mice.Journal of Immunology 92, 837-842. [Google Scholar]
  69. Rundel, R. D. & Nachtwey, D. S. (1978). Skin cancer and ultraviolet radiation.Photochemistry and Photobiology 28, 345-356.[CrossRef] [Google Scholar]
  70. Sakahira, H., Enari, M. & Nagata, S. (1998). Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis.Nature 391, 96-99.[CrossRef] [Google Scholar]
  71. Salgame, P., Varadhachary, A. S., Primiano, L. L., Fincke, J. E., Muller, S. & Monestier, M. (1997). An ELISA for detection of apoptosis.Nucleic Acids Research 25, 680-681.[CrossRef] [Google Scholar]
  72. Saurin, A. J., Borden, K. L., Boddy, M. N. & Freemont, P. S. (1996). Does this have a familiar RING?Trends in Biochemical Sciences 21, 208-214.[CrossRef] [Google Scholar]
  73. Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K. J., Debatin, K. M., Krammer, P. H. & Peter, M. E. (1998). Two CD95 (APO-1/Fas) signaling pathways.EMBO Journal 17, 1675-1687.[CrossRef] [Google Scholar]
  74. Scheffner, M., Werness, B. A., Huibregtse, J. M., Levine, A. J. & Howley, P. M. (1990). The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53.Cell 63, 1129-1136.[CrossRef] [Google Scholar]
  75. Schlegel, J., Peters, I., Orrenius, S., Miller, D. K., Thornberry, N. A., Yamin, T. T. & Nicholson, D. W. (1996). CPP32/apopain is a key interleukin 1 beta converting enzyme-like protease involved in Fas-mediated apoptosis.Journal of Biological Chemistry 271, 1841-1844.[CrossRef] [Google Scholar]
  76. Schreiber, M., Sedger, L. & McFadden, G. (1997). Distinct domains of M-T2, the myxoma virus tumor necrosis factor (TNF) receptor homolog, mediate extracellular TNF binding and intracellular apoptosis inhibition.Journal of Virology 71, 2171-2181. [Google Scholar]
  77. Sedger, L. & McFadden, G. (1996). M-T2: a poxvirus TNF receptor homologue with dual activities.Immunology and Cell Biology 74, 538-545.[CrossRef] [Google Scholar]
  78. Senkevich, T. G., Koonin, E. V. & Buller, R. M. L. (1994). A poxvirus protein with a RING zinc finger motif is of crucial importance for virulence.Virology 198, 118-128.[CrossRef] [Google Scholar]
  79. Senkevich, T. G., Wolffe, E. J. & Buller, R. M. L. (1995). Ectromelia virus RING finger protein is localized in virus factories and is required for virus replication in macrophages.Journal of Virology 69, 4103-4111. [Google Scholar]
  80. Shisler, J. L., Senkevich, T. G., Berry, M. J. & Moss, B. (1998). Ultraviolet-induced cell death blocked by a selenoprotein from a human dermatotropic poxvirus.Science 279, 102-105.[CrossRef] [Google Scholar]
  81. Slee, E. A., Harte, M. T., Kluck, R. M., Wolf, B. B., Casiano, C. A., Newmeyer, D. D., Wang, H. G., Reed, J. C., Nicholson, D. W., Alnemri, E. S., Green, D. R. & Martin, S. J. (1999). Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner.Journal of Cell Biology 144, 281-292.[CrossRef] [Google Scholar]
  82. Spriggs, M. K., Hruby, D. E., Maliszewski, C. R., Pickup, D. J., Sims, J. E., Buller, R. M. L. & VanSlyke, J. (1992). Vaccinia and cowpox viruses encode a novel secreted interleukin-1-binding protein.Cell 71, 145-152.[CrossRef] [Google Scholar]
  83. Steegenga, W. T., van Laar, T., Riteco, N., Mandarino, A., Shvarts, A., van der Eb, A. J. & Jochemsen, A. G. (1996). Adenovirus E1A proteins inhibit activation of transcription by p53.Molecular and Cellular Biology 16, 2101-2109. [Google Scholar]
  84. Sugiyama, A., Noguchi, K., Kitanaka, C., Katou, N., Tashiro, F., Ono, T., Yoshida, M. C. & Kuchino, Y. (1999). Molecular cloning and chromosomal mapping of mouse intronless myc gene acting as a potent apoptosis inducer.Gene 226, 273-283.[CrossRef] [Google Scholar]
  85. Szekely, L., Selivanova, G., Magnusson, K. P., Klein, G. & Wiman, K. G. (1993). EBNA-5, an Epstein–Barr virus-encoded nuclear antigen, binds to the retinoblastoma and p53 proteins.Proceedings of the National Academy of Sciences, USA 90, 5455-5459.[CrossRef] [Google Scholar]
  86. Teodoro, J. G. & Branton, P. E. (1997). Regulation of apoptosis by viral gene products.Journal of Virology 71, 1739-1746. [Google Scholar]
  87. Tewari, M., Quan, L. T., O’Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D. R., Poirier, G. G., Salvesen, G. S. & Dixit, V. M. (1995a). Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase.Cell 81, 801-809.[CrossRef] [Google Scholar]
  88. Tewari, M., Telford, W. G., Miller, R. A. & Dixit, V. M. (1995b). CrmA, a poxvirus-encoded serpin, inhibits cytotoxic T-lymphocyte-mediated apoptosis.Journal of Biological Chemistry 270, 22705-22708.[CrossRef] [Google Scholar]
  89. Thompson, C. B. (1995). Apoptosis in the pathogenesis and treatment of disease.Science 267, 1456-1462.[CrossRef] [Google Scholar]
  90. Upton, C., Macen, J. L., Schreiber, M. & McFadden, G. (1991). Myxoma virus expresses a secreted protein with homology to the tumor necrosis factor receptor gene family that contributes to viral virulence.Virology 184, 370-382.[CrossRef] [Google Scholar]
  91. Upton, C., Mossman, K. & McFadden, G. (1992). Encoding of a homolog of the IFN-gamma receptor by myxoma virus.Science 258, 1369-1372.[CrossRef] [Google Scholar]
  92. Verhaegen, S., McGowan, A. J., Brophy, A. R., Fernandes, R. S. & Cotter, T. G. (1995). Inhibition of apoptosis by antioxidants in the human HL-60 leukemia cell line.Biochemical Pharmacology 50, 1021-1029.[CrossRef] [Google Scholar]
  93. Wang, X. W., Gibson, M. K., Vermeulen, W., Yeh, H., Forrester, K., Sturzbecher, H. W., Hoeijmakers, J. H. & Harris, C. C. (1995). Abrogation of p53-induced apoptosis by the hepatitis B virus X gene.Cancer Research 55, 6012-6016. [Google Scholar]
  94. Werness, B. A., Levine, A. J. & Howley, P. M. (1990). Association of human papillomavirus types 16 and 18 E6 proteins with p53.Science 248, 76-79.[CrossRef] [Google Scholar]
  95. White, E. (1996). Life, death, and the pursuit of apoptosis.Genes & Development 10, 1-15.[CrossRef] [Google Scholar]
  96. Woo, M., Hakem, R., Soengas, M. S., Duncan, G. S., Shahinian, A., Kagi, D., Hakem, A., McCurrach, M., Khoo, W., Kaufman, S. A., Senaldi, G., Howard, T., Lowe, S. W. & Mak, T. W. (1998). Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes.Genes & Development 12, 806-819.[CrossRef] [Google Scholar]
  97. Wyllie, A. H., Kerr, J. F. & Currie, A. R. (1980). Cell death: the significance of apoptosis.International Review of Cytology 68, 251-306. [Google Scholar]
  98. Yonish-Rouach, E., Resnitzky, D., Lotem, J., Sachs, L., Kimchi, A. & Oren, M. (1991). Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6.Nature 352, 345-347.[CrossRef] [Google Scholar]
  99. Zanke, B. W., Boudreau, K., Rubie, E., Winnett, E., Tibbles, L. A., Zon, L., Kyriakis, J., Liu, F. F. & Woodgett, J. R. (1996). The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat.Current Biology 6, 606-613.[CrossRef] [Google Scholar]
  100. Zhan, Q., Carrier, F. & Fornace, A. J.Jr (1993). Induction of cellular p53 activity by DNA-damaging agents and growth arrest.Molecular and Cellular Biology 13, 4242-4250. [Google Scholar]
  101. Zhan, Q., Fan, S., Bae, I., Guillouf, C., Liebermann, D. A., O’Connor, P. M. & Fornace, A. J.Jr (1994). Induction of bax by genotoxic stress in human cells correlates with normal p53 status and apoptosis.Oncogene 9, 3743-3751. [Google Scholar]
  102. Zhou, Q., Snipas, S., Orth, K., Muzio, M., Dixit, V. M. & Salvesen, G. S. (1997). Target protease specificity of the viral serpin CrmA. Analysis of five caspases.Journal of Biological Chemistry 272, 7797-7800.[CrossRef] [Google Scholar]
  103. Ziegler, A., Jonason, A. S., Leffell, D. J., Simon, J. A., Sharma, H. W., Kimmelman, J., Remington, L., Jacks, T. & Brash, D. E. (1994). Sunburn and p53 in the onset of skin cancer.Nature 372, 773-776.[CrossRef] [Google Scholar]
  104. Zou, H., Henzel, W. J., Liu, X., Lutschg, A. & Wang, X. (1997). Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3.Cell 90, 405-413.[CrossRef] [Google Scholar]
  105. Zou, H., Li, Y., Liu, X. & Wang, X. (1999). An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9.Journal of Biological Chemistry 274, 11549-11556.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-4-1087
Loading
/content/journal/jgv/10.1099/0022-1317-81-4-1087
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error