E1B 55-kilodalton oncoproteins of adenovirus types 5 and 12 inactivate and relocalize p53, but not p51 or p73, and cooperate with e4orf6 proteins to destabilize p53

Journal of Virology

Volumn 74, Issue 1, 2000, Pages 193-202

  Wienzek, Sandra ^a   Roth, Judith ^a   Dobbelstein, Matthias ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN; PROTEIN P53; VIRUS PROTEIN;

ADENOVIRUS; ARTICLE; CELL CULTURE; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

EID: 0033989602     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.1.193-202.2000     Document Type: Article

References (61)

1. Bailey, A. D., Z. Li, T. Pavelitz, and A. M. Weiner. 1995. Adenovirus type 12-induced fragility of the human RNU2 locus requires U2 small nuclear RNA transcriptional regulatory elements. Mol. Cell. Biol. 15:6246-6255.
2. Baker, S. J., S. Markowitz, E. R. Fearon, J. K. Willson, and B. Voselstein. 1990. Suppression of human colorectal carcinoma cell growth by wild-type p53. Science 249:912-915.
3. Bernards, R., P. I. Schrier, J. L. Bos, and A. J. Van der Eb. 1983. Role of adenovirus types 5 and 12 early region 1b tumor antigens in oncogenic transformation. Virology 127:45-53.
4. Bian, J., and Y. Sun. 1997. p53CP, a putative p53 competing protein that specifically hinds to the consensus p53 DNA binding sites: a third member of the p53 family? Proc. Natl. Acad. Sci. USA 94:14753-14758.
5. Blair Zajdel, M. E., and G. E. Blair. 1988. The intracellular distribution of the transformation-associated protein p53 in adenovirus-transformed rodent cells. Oncogene 2:579-584.
6. De Laurenzi, V., A. Costanzo, D. Barcaroli, A. Terrinoni, M. Falco, M. Annicchiarico-Petruzzelli, M. Levrero, and G. Melino. 1998. Two new p73 splice variants, gamma and delta, with different transcriptional activity. J. Exp. Med. 188:1763-1768.
7. Dobbelstein, M., A. K. Arthur, S. Dehde, K. van Zee, A. Dickmanns, and E. Fanning. 1992. Intracistronic complementation reveals a new function of SV40 T antigen that co-operates with Rb and p53 binding to stimulate DNA synthesis in quiescent cells. Oncogene 7:837-847.
8. Dobbelstein, M., and J. Roth. 1998. The large T antigen of simian virus 40 hinds and inactivates p53 but not p73. J. Gen. Virol. 79:3079-3083.
9. Dobbelstein, M., J. Roth, W. T. Kimberly, A. J. Levine, and T. Shenk. 1997. Nuclear export of the E1B 55-kDa and E4 34-kDa adenoviral oncoproteins mediated by a rev-like signal sequence. EMBO J. 16:4276-4284.
10. 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.
11. Donehower, L. A., M. Harvey, B. L. Slagle, M. J. McArthur, C. A. Montgomery, Jr., J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221.
12. Freedman, D. A., C. B. Epstein, J. C. Roth, and A. J. Levine. 1997. A genetic approach to mapping the p53 binding site in the MDM2 protein. Mol. Med. 3:248-259.
13. Gallimore, P. H., P. S. Lecane, S. Roberts, S. M. Rookes, R. J. Grand, and J. Parkhill. 1997, Adenovirus type 12 early region 1B 54K protein significantly extends the life span nf normal mammalian cells in culture. J. Virol. 71:6629-6640.
14. Goodrum, F. D., T. Shenk, and D. A. Ornelles. 1996. Adenovirus early region 4 34-kilodalton protein directs the nuclear localization of the early region 1B 55-kilodalton protein in primate cells. J. Virol. 70:6323-6335.
15. Grand, R. J. A., M. L. Grant, and P. H. Gallimore. 1994. Enhanced expression of p53 in human cells infected with mutant adenoviruses. Virology 203:229-240.
16. Haupt, Y., R. Maya, A. Kazaz, and M. Oren. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387:296-299.
17. Higashino, F., J. M. Pipas, and T. Shenk. 1998. Adenovirus e4orf6 oncoprotein modulates the function of the p53-related protein, p73. Proc. Natl. Acad. Sci. USA 95:15683-15687.
18. Jost, C. A., M. C. Marin, and W. G. Kaelin, Jr. 1997. p73 is a human p53-related protein that can induce apoptosis. Nature 389:191-194.
19. Kaelin, W. G., Jr. 1999. The emerging p53 gene family. J. Natl. Cancer Inst. 91:594-598.
20. Kaghad, M., H. Bonnet, A. Yang, L. Creancier, J. C. Biscan, A. Valent, A. Minty, P. Chalon, J. M. Lelias, X. Dumont, P. Ferrara, F. McKeon, and D. Caput. 1997. Monoallelically expressed gene related to p53 at 1p36, a region frequently deleted in neuroblastoma and other human cancers. Cell 90:809-819.
21. Kubbutat, M. H., S. N. Jones, and K. H. Vousden. 1997. Regulation of p53 stability by Mdm2. Nature 387:299-303.
22. Lane, D. P. 1992. p53, guardian of the genome. Nature 358:15-16.
23. Levine, A. J. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323-331.
24. Li, Z., A. Yu, and A. M. Weiner. 1998. Adenovirus type 12-induced fragility of the human RNU2 locus requires p53 function. J. Virol. 72:4183-4191.
25. Liao, D., A. Yu, and A. M. Weiner. 1999. Coexpression of the adenovirus 12 E1B 55 kDa oncoprotein and cellular tumor suppressor p53 is sufficient to induce metaphase fragility of the human RNU2 locus. Virology 254:11-23.
26. Lin, J., J. Chen, B. Elenbaas, and A. J. Levine. 1994. Several hydrophobic amino acids in the p53 amino-terminal domain are required for transcriptional activation, binding to mdm-2 and the adenovirus 5 E1B 55-kD protein. Genes Dev. 8:1235-1246.
27. Mai, M., A. Yokomizo, C. Qian, P. Yang, D. J. Tindall, D. I. Smith, and W. Liu. 1998. Activation of p73 silent allele in lung caneer. Cancer Res. 58: 2347-2349.
28. Marin, M. C., C. A. Jost, M. S. Irwin, J. A. DeCaprio, D. Caput, and W. G. Kaelin, Jr. 1998. Viral oncoproteins discriminate between p53 and the p53 homolog p73. Mol. Cell. Biol. 18:6316-6324.
29. Mills, A. A., B. Zheng, X. J. Wang, H. Vogel, D. R. Roop, and A. Bradley. 1999. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398:708-713.
30. Moore, M., N. Horikoshi, and T. Shenk. 1996. Oncogenic potential of the adenovirus E4orf6 procein. Proc. Natl. Acad. Sci. USA 93:11295-11301.
31. Nomoto, S., N. Haruki, M. Kondo, H. Konishi, and T. Takahashi. 1998. Search for mutations and examination of allelic expression imbalance of the p73 gene at 1p36.33 in human lung cancers. Cancer Res. 58:1380-1383.
32. Osada, M., M. Ohba, C. Kawahara, C. Ishioka, R. Kanamaru, I. Katoh, Y. Ikawa, Y. Nimura, A. Nakagawara, M. Obinata, and S. Ikawa. 1998. Cloning and functional analysis of human p51, which structurally and functionally resembles p53. Nat. Med. 4:839-843.
33. Prabhu, N. S., K. Somasundaram, K. Satyamoorthy, M. Herlyn, and W. S. El-Deiry. 1998. p73, unlike p53, suppresses growth and induces apoptosis of human papillomavirus E6-expressing cancer cells. Int. J. Oncol. 13:5-9.
34. Querido, E., R. C. Marcellus, A. Lai, R. Charbonneau, J. G. Teodoro, G. Ketner, and P. E. Branton. 1997. Regulation of p53 levels by the E1B 55-kilodalton protein and E4orf6 in adenovirus-infected cells. J. Virol. 71: 3788-3798.
35. Roth, J., D. Dittmer, D. Rea, J. Tartaglia, E. Paoletti, and A. J. Levine. 1996. p53 as a target for cancer vaccines: recombinant canarypox virus vectors expressing p53 protect mice against lethal tumor cell challenge. Proc. Natl. Acad. Sci. USA 93:4781-4786.
36. Roth, J., M. Dobbelstein, D. A. Freedman, T. Shenk, and A. J. Levine. 1998. Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein. EMBO J. 17:554-564.
37. Roth, J., C. König, S. Wienzek, S. Weigel, S. Ristea, and M. Dobbeistein. 1998. Inactivation of p53 but not p73 by adenovirus type 5 E1B 55-kilodalton and E4 34-kilodalton oncoproteins. J. Virol. 72:8510-8516.
38. Sarnow, P., P. Hearing, C. W. Anderson, D. N. Halbert, T. Shenk, and A. J. Levine. 1984. Adenovirus early region IB 58,000-dalton tumor antigen is physically associated with an early region 4 25,000-dalton protein in productively infected cells. J. Virol. 49:692-700.
39. 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 54 kd cellular protein in transformed cells. Cell 28:387-394.
40. Sarnow, P., C. A. Sullivan, and A. J. Levine. 1982. A monoclonal antibody detecting the adenovirus type 5-E1b-58Kd tumor antigen: characterization of the E1b-SKKd tumor antigen in adenovirus-infected and -transformed cells. Virology 120:510-517.
41. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
42. Schmale, H., and C. Bamberger. 1997. A novel protein with strong homology to the tumor suppressor p53. Oncogene 15:1363-1367.
43. Senoo, M., N. Seki, M. Ohira, S. Sugano, M. Watanabe, M. Tachibana, T. Tanaka, Y. Shinkai, and H. Kato. 1998. A second p53-related protein, p73L, with high homology to p73. Biochem. Biophys. Res. Commun. 248:603-607.
44. Shenk, T. 1996. Adenoviridae: the viruses and their replication, p. 2111-2148. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Virology, 3rd ed., vol. 2. Lippincott-Raven, Philadelphia, Pa.
45. Steegenga, W. T., N. Riteco, A. G. Jochemsen, F. J. Fallaux, and J. L. Bos. 1998. The large E1B protein together with the E4orf6 protein target p53 for active degradation in adenovirus infected cells. Oncogene 16:349-357.
46. Steegenga, W. T., A. Shvarts, N. Riteco, J. L. Bos, and A. G. Jochemsen. 1999. Distinct regulation of p53 and p73 activity by adenovirus E1A, E1B, and e4orf6 proteins. Mol. Cell. Biol. 19:3885-3894.
47. Sunahara, M., S. Ichimiya, Y. Nimura, N. Takada, S. Sakiyama, Y. Sato, S. Todo, W. Adachi, J. Amano, and A. Nakagawara. 1998. Mutational analysis of the p73 gene localized at chromosome 1p36.3 in colorectal carcinomas. Int. J. Oncol. 13:319-323.
48. Takahashi, H., S. Ichimiya, Y. Nimura, M. Watanabe, M. Furusato, S. Wakui, R. Yatani, S. Aizawa, and A. Nakagawara. 1998. Mutation, allelotyping, and transcription analyses of the p73 gene in prostatic carcinoma. Cancer Res. 58:2076-2077.
49. Tanaka, M., and W. Herr. 1990. Differential transcriptional activation by Oct-1 and Oct-2: interdependent activation domains induce Oct-2 phosphorylation. Cell 60:375-386.
50. Trink, B., K. Okami, L. Wu, V. Sriuranpong, J. Jen, and D. Sidransky. 1998. A new human p53 homologue. Nat. Med. 4:747-748.
51. van den Heuvel, S. J., T. van Laar, I. The, and A. J. van der Eb. 1993. Large E1B proteins of adenovirus types 5 and 12 have different effects on p53 and distinct roles in cell transformation. J. Virol. 67:5226-5234.
52. Werness, B. A., A. J. Levine, and P. M. Howley. 1990. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248:76-79.
53. Yang, A., M. Kaghad, Y. Wang, E. Gillet, M. D. Fleming, V. Dotsch, N. C. Andrews, D. Caput, and F. McKeon. 1998. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol. Cell 2:305-316.
54. Yang, A., R. Schweitzer, D. Sun, M. Kaghad, N. Walker, R. T. Bronson, C. Tabin, A. Sharpe, D. Caput, C. Crum, and F. McKeon. 1999. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398:714-718.
55. Yew, P. R., and A. J. Berk. 1992. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature 357:82-85.
56. Yew, P. R., X. Liu, and A. J. Berk. 1994. Adenovirus E1B oncoprotein tethers a transcriptional repression domain to p53. Genes Dev. 8:190-202.
57. Zantema, A., J. A. Fransen, A. Davis-Olivier, F. C. Ramaekers, G. P. Vooijs, B. DeLeys, and A. J. Van der Eb. 1985. Localization of the E1B proteins of adenovirus 5 in transformed cells, as revealed by interaction with monoclonal antibodies. Virology 142:44-58.
58. Zantema, A., P. I. Schrier, A. Davis-Olivier, T. van Laar, R. T. Vaessen, and A. van der Eb. 1985. Adenovirus serotype determines association and localization of the large E1B tumor antigen with cellular tumor antigen p53 in transformed cells. Mol. Cell. Biol. 5:3084-3091.
59. Zeng, X., A. J. Levine, and H. Lu. 1998. Non-p53 p53RE binding protein, a human transcription factor functionally analogous to P53. Proc. Natl. Acad. Sci. USA 95:6681-6686.
60. Zhu, H., Y. Shen, and T. Shenk. 1995. Human cytomegalovirus 1E1 and 1E2 proteins block apoptosis. J. Virol. 69:7960-7970.
61. Zhu, J., J. Jiang, W. Zhou, and X. Chen. 1998. The potential tumor suppressor p73 differentially regulates cellular p53 target genes. Cancer Res. 58:5061-5065.