Adenovirus type 5 early region 4 is responsible for E1A-induced p53- independent apoptosis

Journal of Virology

Volumn 70, Issue 9, 1996, Pages 6207-6215

  Marcellus, Richard C ^a   Teodoro, Jose G ^a   Wu, Tim ^a   Brough, Douglas E ^b   Ketner, Gary ^c   Shore, Gordon C ^a   Branton, Philip E ^a  

^a MCGILL UNIVERSITY   (Canada)

^b GENVEC INC   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; VIRUS PROTEIN;

APOPTOSIS; ARTICLE; DNA DEGRADATION; ELECTROIMMUNOASSAY; EXPRESSION VECTOR; GENE EXPRESSION REGULATION; HUMAN; HUMAN ADENOVIRUS 5; HUMAN CELL; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; TRANSACTIVATION; VIRUS INFECTION;

EID: 0029793365     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.9.6207-6215.1996     Document Type: Article

References (95)

1. Akusjärvi, G. 1993. Proteins with transcription regulatory properties encoded by human adenoviruses. Trends Microbiol. 1:163-170.
2. Bacchetti, S., and F. L. Graham. 1993. Inhibition of cell proliferation by an adenovirus vector expressing the human wild type p53 protein. Int. J. Oncol. 3:781-788.
3. Barbeau, D., R. Charbonneau, S. G. Whalen, S. T. Bayley, and P. E. Branton. 1994. Functional interactions within adenovirus E1A protein complexes. Oncogene 9:359-373.
4. Barbeau, D., R. C. Marcellus, S. Bacchetti, S. T. Bayley, and P. E. Branton. 1993. Quantitative analysis of regions of adenovirus E1A products involved in interactions with cellular proteins. Biochem. Cell Biol. 70:1123-1124.
5. Barker, D., and A. J. Berk. 1987. Adenovirus proteins from both E1B reading frames are required for transformation of rodent cells by viral infection and DNA transfection. Virology 156:107-121.
6. Bayley, S. T., and J. S. Mymryk. 1994. Adenovirus E1A proteins and transformation: a review. Int. J. Oncol. 5:425-444.
7. Bernards, R., M. G. de Leeuw, A. Houweling, and A. J. van der Eb. 1986. Role of the adenovirus early region 1B tumor antigens in transformation and lytic infection. Virology 150:126-139.
8. Bett, A. J., and F. L. Graham. Unpublished results.
9. Bett, A. J., W. Haddara, L. Prevec, and F. L. Graham. 1994. An efficient and flexible system for construction of adenovirus vectors with insertions or deletions-in early regions 1 and 3. Proc. Natl. Acad. Sci. USA 91:8802-8806.
10. Bondesson, M., C. Svensson, S. Linder, and G. Akusjärvi. 1992. The carboxy-terminal exon of the adenovirus E1A protein is required for the E4F-dependent transcription activation. EMBO J. 11:3347-3354.
11. Boyd, J. M., S. Malstrom, T. Subramanian, L. K. Venkatesh, U. Schaeper, B. Elangovan, C. D'Sa-Eipper, and G. Chinnadurai. 1994. Adenovirus E1B 19 kDa and Bcl-2 proteins interact with a common set of cellular proteins. Cell 79:341-351.
12. Braithwaite, A. W., C. C. Nelson, and A. J. D. Bellett. 1991 E1A revisited: the case for multiple cooperative trans-activation domains. New Biol. 3:18-26.
13. Braithwaite, A., C. Nelson, A. Skulimowski, J. McGovern, D. Pigott, and J. Jenkins. 1990. Transactivation of the p53 oncogene by Ela gene products. Virology 177:595-605.
14. Branton, P. E., S. T. Bayley, and F. L. Graham. 1985. Transformation by human adenoviruses. Biochim. Biophys. Acta 780:67-94.
15. Bridge, E., and G. Ketner. 1989. Redundant control of adenovirus late gene expression by early region 4. J. Virol. 63:631-638.
16. Bridge, E., and G. Ketner. 1990. Interaction of adenoviral E4 and E1b products in late gene expression. Virology 174:345-353.
17. Bridge, E., S. Medghalchi, S. Ubol, M. Leesong, and G. Ketner. 1993. Adenovirus early region 4 and viral DNA synthesis. Virology 193:794-801.
18. Brough, U. E., A. Lizonova, C. Hsu, V. A. Kulesa, and I. Kovesci. A gene transfer vector-cell line system for complete functional complementation of adenovirus early regions E1 and E4. Submitted for publication.
19. Challberg, M. D., and G. Ketner. 1981. Deletion mutants of adenovirus 2: isolation and initial characterization of virus carrying mutations near the right end of the viral genome. Virology 114:196-209.
20. Chen, G., P. E. Branton, and G. C. Shore. 1995. Induction of p53-independent apoptosis by hygromycin B: suppression by Bcl-2 and adenovirus E1B 19-kDa protein. Exp. Cell Res. 221:55-59.
21. Cutt, J. R., T. Shenk, and P. Hearing. 1987. Analysis of adenovirus early region 4-encoded polypeptides synthesized in productively infected cells. J. Virol. 61:543-552.
22. Debbas, M., and E. White. 1993. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:546-554.
23. Diller, L., J. Kassel, C. E. Nelson, M. A. Gryka, G. Litwak, M. Gebhardt, B. Bressac, M. Ozturk, S. J. Baker, B. Vogelstein, and S. H. Friend. 1990. p53 functions as a cell cycle protein in osteosarcomaa. Mol. Cell. Biol. 10:5772-5781.
24. Downey, J. F., D. T. Rowe, S. Bacchetti, F. L. Graham, and S. T. Bayley. 1983. Mapping of a 14,000-dalton antigen to early region 4 of the human adenovirus 5 genome. J. Virol. 45:514-523.
25. Dumont, D. J., M. L. Tremblay, and P. E. Branton. 1989. Phosphorylation at serine 89 induces a shift in gel mobility but has little effect on the function of adenovirus type 5 E1A proteins. J. Virol. 63:987-991.
26. Dyson, N., and E. Harlow. 1992. Adenovirus E1A targets key regulators of cell proliferation. Cancer Surv. 12:161-195.
27. Eckner, R., M. E. Ewen, D. Newsome, M. Gerdes, J. A. DeCaprio, J. B. Lawrence, and D. M. Livingston. 1994. Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kDa protein (p300) reveals a protein with properties of a transcriptional adapter. Genes Dev. 8:869-884.
28. Egan, C., S. T. Bayley, and P. E. Branton. 1989. Binding of the Rb1 protein to E1A products is required for adenovirus transformation. Oncogene 4:383-388.
29. Egan, C., T. N. Jelsma, J. A. Howe, S. T. Bayley, B. Ferguson, and P. E. Branton. 1988. Mapping of cellular protein-binding sites on the products of early-region LA of human adenovirus type 5. Mol. Cell. Biol. 8:3955-3959.
30. Ezoe, H., R. B. Lai Fatt, and S. Mak. 1981. Degradation of intraccllular DNA in KB cells infected with cyt mutants of human adenovirus type 12. J. Virol. 40:20-27.
31. Finlay, C. A., P. W. Hinds, and A. J. Levine. 1989. The p53 proto-oncogene can act as a suppressor of transformation. Cell 57:1083-1093.
32. Flint, J., and T. Shenk. 1989. Adenovirus E1A protein paradigm viral trans-activator. Annu. Rev. Genet. 23:141-161.
33. Fryer, G. A., Y. Katch, and R. J. Roberts. 1984. Characterization of the major mRNAs from adenovirus 2 early region 4 by cDNA cloning and sequencing. Nucleic Acids Res. 12:3503-3519.
34. Ginsberg, D., D. Michael-Michalovitz, and M. Oren. 1991. Induction of growth arrest by a temperature-sensitive p53 mutant is correlated with increased nuclear localization and decreased stability of the protein. Mol. Cell. Biol. 11:582-587.
35. Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1044-1051.
36. Graham, F. L., J. Smiley, W. C. Russell, and R. Nairn. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36:59-72.
37. Graham, F. L., and A. J. van der Eb. 1973. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52:456-467.
38. Harlow, E., P. Whyte, B. R. Franza, Jr., and C. Schley. 1986. Association of adenovirus early-region 1A proteins with cellular polypeptides. Mol. Cell Biol. 6:1579-1589.
39. Harrison, T., F. L. Graham, and J. Williams. 1977. Host range mutants of adenovirus type 5 defective for growth in HeLa cells. Virology 77:319-329.
40. Harvey, D. M., and A. J. Levine. 1991. p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes Dev. 5:2375-2385.
41. Hérissé, J., M. Rigolet, S. DuPont de Dinechin, and F. Galibert. 1981. Nucleotide sequence of adenovirus 2 DNA fragment encoding the carboxylic region of the fiber protein and the entire E4 region. Nucleic Acids Res. 9:4023-4042.
42. Hirt, B. 1967. Selective extraction of polyoma DNA from infected mouse cultures. J. Mol. Biol. 26:365-369.
43. Horwitz, M. S. 1990. Adenoviridae and their replication, p. 1679-1721. In B. N. Fields and D. M. Knipe (ed.), Virology, 2nd ed. Raven Press, New York.
44. Huang, M. M., and P. Herring. 1989. The adenovirus early region 4 open reading frame 6/7 regulates the DNA binding activity of the cellular transcription factor, E2F, through a direct complex. Genes Dev, 3:1699-1710.
45. Javier, R., K. Raska, Jr., and T. Shenk. 1993. Requirement for the adenovirus type9 E4 region in production of mammary tumors. Science 257:1267-1271.
46. Jelsma, T. N., J. A. Howe, C. M. Evelegh, N. F. Cunniff, M. H. Skiadopoulos, M. R. Floroff, J. E. Denman, and S. T. Bayley. 1988. Use of deletion and point mutants spanning the coding region of the adenovirus 5 E1A gene to define a domain that is essential for transcriptional activation. Virology 163:494-502.
47. Jones, N., and T. Shenk. 1979. Isolation of adenovirus type 5 host-range deletion mutants defective for transformation of rat embryo cells. Cell 17: 683-689.
48. Kimelman, D. J., J. S. Miller, D. Porter, and B. E. Roberts. 1985. E1a regions of the human adenoviruses and of the highly oncogenic simian adenovirus 7 are closely related. J. Virol. 53:399-409.
49. Kleinberger, T., and T. Shenk. 1993. Adenovirus E4orf4 protein hinds to protein phosphatase 2A, and the complex down regulates E1A-enhanced junB transcription. J. Virol. 67:7556-7550.
50. Kovesdi, I., R. Reichel, and J. R. Nevins. 1987. Role of adenovirus E2 promoter binding factor in E1A-mediated coordinate gene control. Proc. Natl. Acad. Sci. USA 84:2180-2184.
51. Lowe, S. W., T. Jacks, D. E. Housman, and H. E. Ruley. 1994. Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells. Proc. Natl. Acad. Sci. USA 91:2026-2030.
52. Lowe, S. W., and H. E. Ruley. 1993. Stabilization of the p53 tumor suppressor is induced by adenovirus E1A in mouse thymocytes. Genes Dev. 7:535-545.
53. Marton, M. J., S. B. Bairn, D. A. Ornelles, and T. Shenk. 1990. The adenovirus E4 17-kilodalton protein complexes with the cellular transcription factor E2F, altering its DNA-binding properties and stimulating E1A-independent accumulation of E2 mRNA. J. Virol. 64:2345-2359.
54. McGrory, W. J., D. D. Bautista, and F. L. Graham. 1988. A simple technique for the rescue of early region 1 mutations into infectious human adenovirus type 5. Virology 163:614-617.
55. McLorie, W, C. J. McGlade, D. Takayesu, and P. E. Branton. 1991. Individual adenovirus E1B proteins induce transformation independently but by additive pathways. J. Gen. Virol. 72:1467-1471.
56. Moran, E., and M. B. Mathews. 1987. Multiple functional domains in the adenovirus E1A gene. Cell 48:177-178.
57. Müller, U., T. Kleinberger, and T. Shenk. 1992. Adenovirus E4orf4 protein reduces phosphorylation of c-Fos and E1a proteins while simultaneously reducing the level of AP-1. J. Virol. 66:5867-5878.
58. Mymryk, J. S., and S. T. Bayley. 1993. Induction of gene expression by exon 2 of the major E1A proteins of adenovirus type 5. J. Virol. 67:6922-6928.
59. Neill, S. D., C. Hemstrom, A. Virtanen, and J. R. Nevins. 1990. An adenovirus E4 gene product trans-activates E2 transcription and stimulates stable E2F binding through a direct association with E2F. Proc. Natl. Acad. Sci. USA 87:2008-2012.
60. Nevins, J. R. 1991. Transcriptional activation by viral regulatory proteins. Trends Biochem. Sci. 16:435-439.
61. Nguyen, M., P. E. Branton, P. A. Walton, S. J. Korsmeyer, and G. C. Shore. 1994. Role of the membrane anchor domain of Bcl-2 in suppression of apoptosis caused by E1B-defective adenovirus. J. Biol. Chem. 269:16521-16524.
62. Obert, S., R. J. O'Connor, S. Schmid, and P. Hearing. 1994. The adenovirus E4-6/7 protein transactivates the E2 promoter by inducing dimerization of a heterodimeric E2F complex. Mol. Cell, Biol. 14:1333-1346.
63. Pilder, S., J. Logan, and T. Shenk. 1984. Deletion of the gene encoding the adenovirus 5 early region 1b 21,000-molecular-weight polypeptide leads to degradation of viral and host cell DNA. J. Virol. 52:664-671.
64. Pilder, S., M. Moore, J. Logan, and T. Shenk 1986. The adenovirus E1B-55K transforming polypeptide modulates transport or cytoplasmic stabilization of viral and host cell mRNAs. Mol. Cell. Biol. 6:470-476.
65. Popperl, H., and M. S. Featherstone. 1992. An autoregulatory element of the murine Hov-4.4 gene. EMBO J. 11:3673-3680.
66. Querido, E., J. G. Teodoro, and P. E. Branton. Unpublished data.
67. Rao, L., M. Debbas, P. Sabbatini, D. Hockenbery, S. Korsmeyer, and E. White. 1992. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and bcl-2 proteins. Proc. Natl. Acad. Sci. USA 89:7742-7746.
68. Raychaudhuri, P., S. Bagchi, S. D. Neill, and J. R. Nevins. 1990. Activation of E2F transcription factor in adenovirus infected cells involves E1A-dependent stimulation of DNA binding activity and induction of cooperative binding mediated by an E4 gene product. J. Virol. 64:2702-2710.
69. Sandier, A. B., and G. Ketiner. 1989. Adenovirus early region 4 is essential for normal stability of late nuclear RNAs. J. Virol. 63:624-630.
70. Sarnow, P., P. Hearing, C. W. Anderson, D. N. Halbert, T. Shenk, and A. J. Levine. 1984. Adenovirus early region 1b 58,000-dalton tumor antigen is physically associated with an early region 4 25,000-dallon protein in productively infected cells. J. Virol. 49:692-700.
71. Sarnow, P., Y. S. Ho, J. Williams, and A. J. Levine. 1982. Adenovirus E1b-58Kd tumor antigen and SV40 large tumor antigen are physically associated with the same 54Kd cellular protein in transformed cells. Cell 28:387-394.
72. Shenk, T. and J. Flint. 1991. Transcriptional and transforming activities of the adenovirus E1A proteins. Adv. Cancer Res. 57:7-85.
73. Shepherd, S. E., J. A. Howe, J. S. Mymryk, and S. T. Bayley. 1993. Induction of the cell cycle in baby rat kidney cells by adenovirus type 5 E1A in the absence of E1B and a possible influence of p53. J. Virol. 67:2944-2949.
74. Subramanian, T., M. Kuppuswamy, J. Gysbers, S. Mak, and G. Chinnadurai. 1984. 19-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.
75. Subramanian, T., B. Tarodi, and G. Chinnadurai. 1995. p53-independent apoptotic and necrotic cell deaths induced by adenovirus infection: suppression by E1B 19K and Bcl-2 proteins. Cell Growth Differ. 6:131-137.
76. Teodoro, J. G., and P. E. Branton. Unpublished data.
77. Teodoro, J. G., T. Halliday, S. G. Whalen, D. Takayesu, F. L. Graham, and P. E. Branton. 1994. Phosphorylation at the carboxy terminus of the 55-kilodalton adenovirus type 5 E1B protein regulates transforming activity. J. Virol. 68:775-786.
78. Teodoro, J. G., G. C. Shore, and P. E. Branton. 1995. Adenovirus E1A proteins induce apoptosis by both p53-dependent and p53-independent mechanisms. Oncogene 11:467-474.
79. Tremblay, M. L., S. P. Yee, R. H. Persson, S. Bacchetti, J. R. Smiley, and P. E. Branton. 1985. Activation and inhibition of expression of the 72,000-Da early protein of adenovirus type 5 in mouse cells constitutively expressing an immediate early protein of herpes simplex virus type 1. Virology 144:35-45.
80. Virtanen, A., P. Gilardi, A. Naslund, J. M. LeMoullec, U. Pettersson, and M. Perricaudet. 1984. mRNAs from human adenovirus 2 early region 4. J. Virol. 51:822-831.
81. Webster, L. C., and R. P. Ricciardi. 1991. trans-dominant mutants of EIA provide genetic evidence that the zinc finger of the trans-activating domain binds a transcription factor. Mol. Cell. Biol. 11:4287-4296.
82. Weeks, D. L., and N. C. Jones. 1983. E1A control of gene expression is mediated by sequences 5́ to the transcriptional starts of the early viral genes. Mol. Cell. Biol. 3:1222-1234.
83. White, E. Personal communication.
84. White, E., and R. Cipriani. 1989. Specific disruption of intermediate filaments and the nuclear lamina by the 19-kilodalton product of the adenovirus E1B oncogene. Proc. Natl. Acad. Sci. USA 86:9886-9890.
85. White, E., R. Cipriani, P. Sabbatini, and A. Denton. 1991. Adenovirus E1B 19-kilodalton protein overcomes the cytotoxicity of E1A proteins. J. Virol. 65:2968-2978.
86. White, E., P. Sabbatini, M. Debbas, W. S. M. Wold, D. I. Kusher, and L. R. Gooding. 1992. The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor α. Mol. Cell. Biol. 12:2570-2580.
87. Whyte, P., K. J. Buchkovich, J. M. Horowitz, S. H. Friend, M. Raybuck, R. A. Weinberg, and E. Harlow. 1988. Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product. Nature (London) 334:124-129.
88. Whyte, P., H. E. Ruley, and E. Harlow. 1988. Two regions of the adenovirus early region 1A proteins are required for transformation. J. Virol. 62:257-265.
89. Whyte, P., N. M. Williamson, and E. Harlow. 1989. Cellular targets for transformation by the adenovirus E1A proteins. Cell 56:67-75.
90. Yee, S.-P., and P. E. Branton. 1985. Detection of cellular proteins associated with human adenovirus type 5 early region 1A polypeptides. Virology 147: 142-153.
91. Yew, P. R., and A. J. Berk. 1992. Inhibition of p53 transactivation required for transformation by adenovirus early region 1B protein. Nature (London) 357:82-85.
92. Yew, P. R., C. C. Kao, and A. J. Berk. 1990. Dissection of functional domains in the adenovirus 2 early 1B 55K polypeptide by suppressor-linker insertional mutagenesis. Virology 179:795-805.
93. Yew, P. R., X. Liu, and A. J. Berk. 1994. Adenovirus E1A oncogene tethers a transcriptional repression domain to p53. Genes Dev. 8:190-202.
94. Yonish-Rouach, E., D. Resnitzky, J. Lotem, L. Sachs, A. Kimchi, and M. Oren. 1991. Wild-type p53 induces apoptosis of myeloid leukaemias cells that is inhibited by interleukin-6. Nature (London) 352:345-347.
95. Zhang, S., S. Mak, and P. E. Branton. 1992. Overexpression of the E1B 55-kilodalton (482R) protein of human adenovirus type 12 appears to permit efficient transformation of primary baby rat kidney cells in the absence of the E1B 19-kilodalton protein. J. Virol. 66:2303-2309.