Adenovirus type 5 E4 open reading frame 4 protein induces apoptosis in transformed cells

Journal of Virology

Volumn 72, Issue 4, 1998, Pages 2975-2982

  Shtrichman, Ronit ^a   Kleinberger, Tamar ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS PROTEIN E4ORF4;

ADENOVIRUS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL TRANSFORMATION; MOUSE; NONHUMAN; ONCOGENE C FOS; ONCOGENE C JUN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INDUCTION;

EID: 0031949940     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.4.2975-2982.1998     Document Type: Article

References (63)

1. Aaronson, S. A., and S. R. Tronick. 1991. Constitutive activation of growth factor signalling pathways in cancer cells, p. 41-56. In S. Broder (ed.), Molecular foundations of oncology. The Williams & Wilkins Co., Baltimore, Md.
2. Anderson, N. G., J. L. Maller, N. K. Tonks, and T. W. Sturgill. 1990. Requirement for integration of signals from two distinct phosphorylation pathways for activation of MAP kinases. Nature 343:651-653.
3. Arends, M. J., R. G. Morris, and A. H. Wyllie. 1990. Apoptosis: the role of endonuclease. Am. J. Pathol. 136:593-608.
4. Bellamy, C. O. C., R. D. G. Malcomson, D. J. Harrison, and A. H. Wyllie. 1995. Cell death in health and disease: the biology and regulation of apoptosis. Semin. Cancer Biol. 6:3-16.
5. Bondesson, M., K. Ohman, M. Mannervik, S. Fan, and G. Akusjarvi. 1996. Adenovirus E4 open reading 4 protein autoregulates E4 transcription by inhibiting E1A transactivation of the E4 promoter. J. Virol. 70:3844-3851.
6. Bridge, E., and G. Ketner. 1989. Redundant control of adenovirus late gene expression by early region 4. J. Virol. 63:631-638.
7. Bridge, E., and G. Ketner. 1990. Interaction of adenoviral E4 and E1B products in late gene expression. Virology 174:345-353.
8. Chen, C. Y., and D. V. Faller. 1996. Phosphorylation of Bcl-2 protein and association with p21Ras in Ras-induced apoptosis. J. Biol. Chem. 271:2376-2379.
9. Darzynkiewicz, Z., S. Bruno, G. Delbino, W. Gorczyca, M. A. Hotz, P. Lassota, and F. Traganos. 1992. Features of apoptotic cells measured by flow cytometry. Cytometry 13:795-808.
10. Debbas, M., and E. White. 1993. Wild type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev 7:546-554.
11. Dobner T., N. Horikoshi, S. Rubenwolf, and T. Shenk. 1996. Blockage by adenovirus E4orf6 of transcriptional activation by the p53 tumor suppressor. Science 272:1470-1473.
12. Engel, D. A., S. Hardy, and T. Shenk. 1988. cAMP acts in synergy with E1A protein to activate transcription of the adenovirus early genes E4 and E1A. Genes Dev. 2:1517-1528.
13. Freyer, G. A., Y. Katoh, 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.
14. Graham, F. L., J. Smiley, W. C. Russel, and R. Nairn. 1977. Characteristics of a human cell line transformed by human adenovirus type 5. J. Gen. Virol. 36:59-72.
15. Graham, F. L., and A. J. van der Eb. 1973. A new technique for the assay of infectrvity of human adenovirus 5 DNA. Virology 52:456-457.
16. Halbert, D. N., J. R. Cutt, and T. Shenk. 1985. Adenovirus early region 4 encodes functions required for efficient DNA replication, late gene expression, and host cell shutoff. J. Virol. 56:250-257.
17. Haldar, S., N. Jena, and C. M. Croce. 1995. Inactivation of Bcl-2 by phosphorylation. Proc. Natl. Acad. Sci. USA 92:4507-4511.
18. Haupt, Y., S. Rowan, E. Shaulian, K. H. Vousden, and M. Oren. 1995. Induction of apoptosis in HeLa cells by trans-activation-deficient p53. Genes Dev. 9:2170-2183.
19. Hinds, P., C. A. Finlay, R. S. Quartin, S. J. Baker, E. R. Fearon, B. Vogelstein, and A. J. Levine. 1990. Mutant p53 DNA clones from human colon carcinomas cooperate with ras in transforming primary rat cells: a comparison of the "hot spot" mutant phenotypes. Cell Growth Differ. 1:571-580.
20. Hirt, B. 1967. Selective extraction of polyoma DNA from infected mouse cultures. J. Mol. Biol. 26:365-369.
21. Huang, M. M., and P. Hearing. 1989. Adenovirus early region 4 encodes two gene products with redundant effects in lytic infection. J. Virol. 63:2605-2615.
22. Huang, P., and M. M. Hearing. 1989. The adenovirus early region 4 open reading frame 6/7 protein regulates the DNA binding activity of the cellular transcription factor E2F through a direct complex. Genes Dev. 3:1699-1710.
23. Hunter, T. 1991. Cooperation between oncogenes. Cell 64:249-270.
24. Javier, R. T. 1994. Adenovirus type 9 E4 open reading frame 1 encodes a transforming protein required for the production of mammary tumors in rats. J. Virol. 68:3917-3924.
25. Karin, M., and T. Smeal. 1992. Control of transcription factors by signal transduction pathways: the beginning of the end. Trends Biochem. Sci. 17:418-422.
26. Kleinberger, T., and T. Shenk. 1993. Adenovirus E4orf4 protein binds to protein phosphatase 2A, and the complex down regulates E1A-enhanced junB transcription. J. Virol. 67:7556-7560.
27. Lee, S. S., R. S. Weiss, and R. T. Javier. 1997. Binding of human virus oncoproteins to hD1g/SAP97, a mammalian homolog of the drosophila discs large tumor suppressor protein. Proc. Natl. Acad. Sci. USA 94:6670-6675.
28. Leppard, K. N., and T. Shenk. 1989. The adenovirus E1B 55 kd protein influences mRNA transport via an intranuclear effect on RNA metabolism. EMBO J. 8:2329-2336.
29. Lowe, S., and H. E. Ruley. 1993. Stabilization of the p53 tumor suppressor is induced by adenovirus-5 E1A and accompanies apoptosis. Genes Dev. 7:535-545.
30. Marcellus, R. C., J. G. Teodoro, T. Wu, D. E. Brough, G. Ketner, G. Shore, and P. E. Branton. 1996. Adenovirus type 5 early region 4 is responsible for E1A-induced p53-independent apoptosis. J. Virol. 70:6207-6215.
31. Marton, M. J., S. B. Baim, 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.
32. May, W. S., P. G. Tyler, T. Ito, D. K. Armstrong, K. A. Qatsha, and N. E. Davidson. 1994. Interleukin-3 and bryostatin-1 mediate hyperphosphorylation of BCL2α in association with suppression of apoptosis. J. Biol. Chem. 269:26865-26870.
33. McCormick, F. 1989. ras oncogenes, p. 125-145. In R. A. Weinberg (ed.), Oncogenes and the molecular origins of cancer. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
34. Mitsudomi, T., S. M. Steinberg, M. M. Nau, D. Carbone, D. D'Amico, S. Bodner, H. K. Oie, R. I. Linnoila, J. L. Mulshine, J. D. Minna and A. F. Gazdar. 1992. p53 gene mutations in non-small-cell lung cancer cell lines and their correlation with the presence of ras mutations and clinical features. Oncogene 7:171-180.
35. Miyashita, T., S. Krajevski, M. Krajevska, H. G. Wang, H. K. Lin, D. A. Liebermann, B. Hoffman, and J. C. Reed. 1994. Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9:1799-1805.
36. Moore, M., N. Horikoshi, and T. Shenk. 1996. Oncogenic potential of the adenovirus E4orf6 protein. Proc. Natl. Acad. Sci. USA 93:11295-11301.
37. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-2596.
38. 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.
39. Müller, U., M. P. Roberts, D. A. Engel, W. Doerfler, and T. Shenk. 1989. Induction of transcription factor AP-1 by adenovirus E1A protein and cAMP. Genes Dev. 3:1991-2002.
40. Mymryk, J. S., K. Shire, and S. T. Bayley. 1994. Induction of apoptosis by adenovirus type 5 E1A in rat cells requires a proliferation block. Oncogene 9:1187-1193.
41. 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.
42. Nevels, M., S. Rubenwolf, T. Spruss, H. Wolf, and T. Dobner. 1997. The adenovirus E4orf6 protein can promote E1A/E1B-induced focus formation by interfering with p53 tumor suppressor function. Proc. Natl. Acad. Sci. USA 94:1206-1211.
43. Nordqvist, K., K. Ohman, and G. Akusjarvi. 1994. Human adenovirus encodes two proteins which have opposite effects on accumulation of alternatively spliced mRNAs. Mol. Cell. Biol. 14:437-445.
44. Ohman, K., K. Nordqvist, and G. Akusjarvi. 1993. Two adenovirus proteins with redundant activities in virus growth facilitate tripartite leader mRNA accumulation. Virology 194:50-58.
45. Pallas, D. C., W. Weller, S. Jaspers, T. B. Miller, W. S. Lane, and T. M. Roberts. 1992. The third subunit of protein phosphatase 2A (PP2A), a 55-kilodalton protein which is apparently substituted for by T antigens in complexes with the 36- and 63-kilodalton PP2A subunits, bears little resemblance to T antigens. J. Virol. 66:886-893.
46. Rao, L. M., M. Debbas, P. Sabbatini, D. Hockenberry, S. Korsmeyer, and E. White. 1992. The adenovirus E1A proteins induce apoptosis which is inhibited by the E1B-19k and Bcl-2 proteins. Proc. Natl. Acad. Sci. USA 89:7742-7746.
47. Sambrook, J. E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, p. 16.59-16.67. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
48. Selvakumaran, M., H.-K. Lin, T. Miyashita, H. G. Wang, S. Krajewski, J. C. Reed, B. Hoffman, and D. Liebermann. 1994. Immediate early up-regulation of bax expression by p53 but not TGFβ1: a paradigm for distinct apoptotic pathways. Oncogene 9:1791-1798.
49. Shen, Y., and T. Shenk. 1994. Relief of p53-mediated transcriptional repression by the adenovirus E1B 19k protein or the cellular bcl-2 protein. Proc. Natl. Acad. Sci. USA 91:8940-8944.
50. Shen, Y., and T. Shenk. 1995. Viruses and apoptosis. Curr. Opin. Genet. Dev. 5:105-111.
51. Shenk. T. 1995. Adenoviridae, the viruses and their replication, p. 2111-2148. In B. Fields, P. Howley, and D. Knipe (ed.), Virology. Raven Press, New York, N.Y.
52. Sontag, E., S. Fedorov, C. Kaminayashi, D. Robbins, M. Cobb, and M. Mumby. 1993. The interaction of SV40 small tumor antigen with protein phosphatase 2A stimulates the Map kinase pathway and induces cell proliferation. Cell 75:887-897.
53. Teodoro, J. G., and P. E. Branton. 1997. Regulation of apoptosis by viral gene products. J. Virol. 71:1739-1746.
54. 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.
55. Tollefson, A. E., A. Scaria, T. W. Hermiston, J. S. Ryerse, L. J. Wold, and W. S. M. Wold. 1996. The adenovirus death protein (E3-11.6K) is required at very late stages in infection for efficient cell lysis and release of adenovirus from infected cells. J. Virol. 70:2296-2306.
56. Virtanen, A., P. Gilardi, A. Naslund, J. M. LeMoullec, U. Petterson, and M. Perricaudet. 1984. mRNAs from human adenovirus 2 early region 4. J. Virol. 51:822-831.
57. Weinberg, D. H., and G. Ketner. 1986. Adenoviral early region 4 is required for efficient viral DNA replication and for late gene expression. J. Virol. 57:833-838.
58. Weiss, R. S. S. S. Lee, B. V. B. Prasad, and R. T. Javier. 1997. Human adenovirus early region 4 open reading frame 1 genes encode growth-transforming proteins that may be distantly related to dUTP pyrophosphatase enzymes. J. Virol. 71:1857-1870.
59. Whalen, S. G. R. C. Marcellus, A. Whalen, N. G. Ahn, R. P. Ricciardi, and P. E. Branton. 1997. Phosphorylation within the transactivation domain of adenovirus E1A protein by mitogen-activated protein kinase regulates expression of early region 4. J. Virol. 71:3545-3553.
60. White, E. 1996. Life, death and the pursuit of apoptosis. Genes Dev. 10: 1-15.
61. Wu, X., and A. J. Levine. 1994. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA 91:3602-3606.
62. Xia, Z., M. Dickens, J. Raingeaud, R. J. Davis, and M. E. Greenberg. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
63. Zha, J., H. Harada, E. Yang, J. Jockel, and S. J. Korsmeyer. 1996. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-XL. Cell 87:619-628.