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

Volumn 254, Issue 1, 1999, Pages 11-23

  Liao, Daiqing ^a,c   Yu, Adong ^a   Weiner, Alan M ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN; PROTEIN P53;

ADENOVIRUS; AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATIN; CHROMOSOME FRAGILITY; DNA PROBE; GENE EXPRESSION; GENE LOCUS; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYPOTHESIS; METAPHASE; MULTIGENE FAMILY; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; RNA STRUCTURE; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

EID: 0033079820     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1998.9512     Document Type: Article

References (67)

1. Anderson, M. J., Casey, G., Fasching, C. L., and Stanbridge, E. J. (1994). Evidence that wild-type TP53, and not genes on either chromosome 1 or 11, controls the tumorigenic phenotype of the human fibrosarcoma HT1080. Genes Chromosomes Cancer. 9, 266-281.
2. Bailey, A. D., Li, Z., Pavelitz, T., and Weiner, A. M. (1995). Adenovirus 12-induced fragility of the human RNU2 locus requires U2 snRNA transcriptional regulatory elements. Mol. Cell. Biol. 15, 6246-6255.
3. Baker, J. S., Markowitz, S., Fearon, R. E., Willson, V. K. J., and Vogelstein, B. (1992). Suppression of human colorectal carcinoma cell growth by wild-type p53. Science 249, 912-915.
4. Bernstein, L. B., Manser, T., and Weiner, A. M. (1985). Human U1 small nuclear RNA genes: Evidence for extensive conservation of flanking sequences suggests cycles of gene amplification and transposition. Mol. Cell. Biol. 5, 2159-2171.
5. Bischoff, J. R., Kim, D. H., Williams, A., Heise, C., Horn, S., Muna, M., Ng, L., Nye, J. A., Sampson-Johannes, A., Fattaey, A., and McCormick, F. (1996). An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 274, 373-376.
6. Braithwaite, A. W., and Jenkins, J. R. (1989). Ability of p53 and the adenovirus E1b 58-kilodalton protein to form a complex is determined by p53. J. Virol. 63, 1792-1799.
7. Branton, P. E., Bayley, S. T., and Graham, F. L. (1985). Transformation by human adenoviruses. Biochim. Biophys. Acta 780, 67-94.
8. Chen, P. L., Chen, Y. M., Bookstein, R., and Lee, W. H. (1990). Genetic mechanisms of tumor suppression by the human p53 gene. Science 250, 1576-1580.
9. Dobbelstein, M., Roth, J., Kimberly, W. T., Levine, A. J., and Shenk, T. (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., Horikoshi, N., Rubenwolf, S., and Shenk, T. (1996). Blockage by adenovirus E4orf6 of transcriptional activation by the p53 tumor suppressor. Science 272, 1470-1473.
11. Durnam, D. M., Smith, P. P., Menninger, J. C., and McDougall, J. K. (1986). The E1 region of human adenovirus type 12 determines the sites of virally induced chromosomal damage. In "Cancer Cells 4, DNA Tumor Viruses" (M. Botchan, et al. Eds.), pp. 349-354. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
12. Dyson, N., and Harlow, E. (1992). Adenovirus E1A targets key regulators of cell proliferation. Cancer Surv. 12, 161-195.
13. Fischer, U., Huber, J., Boelens, W. C., Mattaj, I. W., and Lührmann, R. (1995). The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82, 475-483.
14. Fridell, R. A., Fischer U., Lührmann, R., Meyer, B. E., Meinkoth, J. L., Malim, M. H., and Cullen, B. R. (1996). Amphibian transcription factor IIIA proteins contain a sequence element functionally equivalent to the nuclear export signal of human immunodeficiency virus type 1 Rev. Proc. Natl. Acad. Sci. USA 93, 2936-2940.
15. Gargano, S., Wang, P., Rusanganwa, E., and Bacchetti, S. (1995). The transcriptionally competent U2 gene is necessary and sufficient for adenovirus type 12 induction of the fragile site at 17q21-22. Mol. Cell. Biol. 15, 6256-6261.
16. Goodrum, F. D., Shenk, T., and Ornelles, D. A. (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.
17. Grand, R. J. A., Grant, M. L., and Gallimore, P. H. (1994). Enhanced expression of p53 in human cells infected with mutant adenoviruses. Virology 203, 229-240.
18. Horikoshi, N., Usheva, A., Chen, J., Levine, A. J., Weinmann, R., and Shenk, T. (1995). Two domains of p53 interact with the TATA-binding protein, and the adenovirus 13S E1A protein disrupts the association, relieving p53-mediated transcriptional repression. Mol. Cell. Biol. 15, 227-234.
19. Kao, C. C., Yew, P. R., and Berk, A. J. (1990). Domains required for in vitro association between the cellular p53 and the adenovirus 2 E1B 55K proteins. Virology 179, 806-814.
20. Kern, E. S., Pietenpol, J. A., Thiagalingam, S., Seymour, A., Kinzler, W. K., and Vogelstein, B. (1992). Oncogenic forms of p53 inhibit p53 regulated gene expression. Science 256, 827-830.
21. Kleckner, N. (1983). Transposon Tn 10. In "Mobile Genetic Elements" (J. A. Shapiro, Ed.), pp. 261-298. Academic Press, New York.
22. Li, Y. P., Tomanin, R., Smiley, J. R., and Bacchetti, S. (1993). Generation of a new adenovirus type 12-inducible fragile site by insertion of an artificial U2 locus in the human genome. Mol. Cell. Biol. 13, 6064-6070.
23. Li, Z., Bailey, A. D., Buchowski, J., and Weiner, A. M. (1998a). A tandem array of minimal U1 snRNA genes is sufficient to generate a new Adenovirus 12-inducible chromosome fragile site. J. Virol. 72, 4205-4211.
24. Li, Z., Yu, A., and Weiner, A. M. (1998b). Adenovirus 12-induced fragility of the human RNU2 locus requires p53 function. J. Virol. 72, 4183-4191.
25. Liao, D., Pavelitz, T., Kidd, J. R., Kidd, K. K., and Weiner, A. M. (1997). Concerted evolution of the tandemly repeated genes encoding human U2 snRNA (the RNU2 locus) involves rapid intrachromosomal homogenization and rare interchromosomal gene conversion. EMBO J. 16, 588-598.
26. Liao, D., Pavelitz, T., and Weiner, A. M. (1998). Characterization of a novel class of interspersed LTR elements in primate genomes: Structure, genomic distribution, and evolution. J. Mol. Evol. 46, 649-660.
27. Liao, D., and Weiner, A. M. (1995). Concerted evolution of the tandemly repeated genes encoding primate U2 small nuclear RNA (the RNU2 locus) does not prevent rapid diversification of the (CT)n·(GA)n microsatellite embedded within the U2 repeat unit. Genomics 30, 583-593.
28. Lill, N. L., Grossman, S. R., Ginsberg, D., DeCaprio, J., and Livingston, D. M. (1997). Binding and modulation of p53 by p300/CBP coactivators. Nature 387, 823-827.
29. Lim, K., and Chae, C. B. (1989). A simple assay for DNA transfection by incubation of the cells in culture dishes with substrates for β-galactosidase. Biotechniques 7, 576-579.
30. Lindgren, V., Ares, M., Weiner, A. M., and Francke, U. (1985a). Human genes for U2 small nuclear RNA map to a major Adenovirus 12 modification site on chromosome 17. Nature 314, 115-116.
31. Lindgren, V. L., Bernstein, L. B., Weiner, A. M., and Francke, U. (1985b). Human U1 small nuclear RNA pseudogenes do not map to the site of the U1 genes in 1p36 but are clustered in 1q12-q22. Mol. Cell. Biol. 5, 2172-2180.
32. Linke, S. P., Clarkin, K. C., Di Leonardo, A., Tsou, A., and Wahl, G. M. (1996). A reversible, p53-dependent G0/G1 cell cycle arrest induced by ribonucleotide depletion in the absence of detectable DNA damage. Genes Dev. 10, 934-947.
33. MacArthur H. L., Agarwal, M. L., and Bacchetti, S. (1997). Induction of fragility at the human RNU2 locus by cytosine arabinoside is dependent upon a transcriptionally competent U2 small nuclear RNA gene and the expression of p53. Somatic Cell Mol. Genet. 23, 379-389.
34. Mak, I., Lai Fatt, R. B., and Mak, S. (1986). Inhibition of protein synthesis enhances transformation of primary cells by viral DNA. Biochem. Cell Biol. 64, 256-263.
35. Nevels, M., Rubenwolf, S., Spruss, T., Wolf, H., and Dobner, T. (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.
36. Palmeri, D., and Malim, M. H. (1996). The human T-cell leukemia virus type 1 posttranscriptional trans-activator Rex contains a nuclear export signal. J. Virol. 70, 6442-6445.
37. Pavelitz, T., Rusché, L., Matera, A. G., Scharf, J. M., and Weiner, A. M. (1995). Concerted evolution of the tandem array encoding primate U2 snRNA occurs in situ, without changing the cytological context of the RNU2 locus. EMBO J. 14, 169-177.
38. Pellegata, N. S., Antoniono, R. J., Redpath, J. L., and Stanbridge, E. L. (1996). DNA damage and p53-mediated cell cycle arrest: A reevaluation. Proc. Natl. Acad. Sci. USA 93, 15209-15214.
39. Pereira, D. S., Rosenthal, K. L., and Graham, F. L. (1995). Identification of adenovirus E1A regions which affect MHC class I expression and susceptibility to cytotoxic T lymphocytes. Virology 211, 268-277.
40. Ridgway, P. J., Hall, A. R., Myers, C. J., Braithwaite, A. W. (1997). p53/ E1b58kDa complex regulates adenovirus replication. Virology 237, 404-413.
41. Sarnow, P., Ho, S., Williams, J., and Levine, A. J. (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.
42. Schouten, G. J., van der Eb, A. J., and Zantema, A. (1995). Downregulation of MHC class I expression due to interference with p105-NFkB1 processing by Ad12 E1A. EMBO J. 14, 1498-1507.
43. Schramayr, S., Caporossi, D., Mak, I., Jelinek, T., and Bacchetti, S. (1990). Chromosomal damage induced by human adenovirus type 12 requires expression of the E1B 55 kilodalton viral protein. J. Virol. 64, 2090-2095.
44. Selby, C. P., and Sancar, A. (1997). Cockayne syndrome group B protein enhances elongation by RNA polymerase II. Proc. Natl. Acad. Sci. USA 94, 11205-11209.
45. Sharma, S., Schwarte-Waldhoff, I., Oberhuber, H., and Schafer, R. (1993). Functional interaction of wild-type and mutant p53 transfected into human tumor cell lines carrying activated ras genes. Cell Growth Differ. 4, 861-869.
46. Shenk, T. (1996). Adenoviridae: The viruses and their replication. In "Virology" (B. N. Fields, Ed.), pp. 2111-2148. Lippincott-Raven, Philadelphia.
47. Sorensen, P. D., Lomholt, B., Frederiksen, S., and Tommerup, N. (1991). Fine mapping of human 5S rRNA genes to chromosome 1q42.11-q42.13. Cytogenet. Cell Genet. 57, 26-29.
48. Steegenga, W. T., Riteco, N., Jochemsen, A. G., Fallaux, F. J., Bos, J. L. (1998). The large E1B protein together with the E4orf6 protein target p53 for active degradation in adenovirus infected cells. Oncogene 16, 349-357.
49. Steegenga, W. T., Shvarts, A., van Laar, T., van der Eb, A. J., and Jochemsen, A. G. (1995a). Altered phosphorylation and oligomerization of p53 in adenovirus type 12-transformed cells. Oncogene 11, 49-57.
50. Steegenga, W. T., van Laar, T., Riteco, N., Mandarino, A., Shvarts, A., van der Eb, A. J., and Jochemsen, A. G. (1996). Adenovirus E1A proteins inhibit activation of transcription by p53. Mol. Cell. Biol. 16, 2101-2109.
51. Steegenga, W. T., van Laar, T., Shvarts, A., Terleth, C., van der Eb, A. J., and Jochemsen, A. G. (1995b). Distinct modulation of p53 activity in transcription and cell-cycle regulation by the large (54 kDa) and small (21 kDa) adenovirus E1B proteins. Virology 212, 543-554.
52. Takebe, Y., Seiki, M., Fujisawa, J., Hoy, P., Yokota, K., Arai, K., Yoshida, M., and Arai, N. (1988). SRα promoter: An efficient and versatile mammalian cDNA expression system composed of the simian virus 40 early promoter and the R-U5 segment of human T-cell leukemia virus type 1 long terminal repeat. Mol. Cell. Biol. 8, 466-472.
53. Teodoro, J. G., and Branton, P. E. (1997). Regulation of apoptosis by viral gene products. J. Virol. 71, 1739-1746.
54. Tiley, L. S., Malim, M. H., and Cullen, B. R. (1991). Conserved functional organization of the human immunodeficiency virus type 1 and visna virus Rev proteins. J. Virol. 65, 3877-3881.
55. Uzvolgyi, E., Classon, M., Henriksson, M., Huang, M., Szekely, L., Lee, W. H., Klein, G., Sumegi, J. (1991). Reintroduction of a normal retinoblastoma gene into retinoblastoma and osteosarcoma cells inhibits the replication associated function of SV40 large T antigen. Cell Growth Differ. 2, 297-303.
56. van Arsdell, S. W., and Weiner, A. M. (1984a). Human genes for U2 small nuclear RNA are tandemly repeated. Mol. Cell. Biol. 4, 492-499.
57. van Arsdell, S. W., and Weiner, A. M. (1984b). Pseudogenes for human U2 do not have a fixed site of 3′ truncation. Nucleic Acids Res. 12, 1463-1471.
58. van der Heuvel, S. J. L., van Laar, The, T. I., and van der Eb, A. J. (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.
59. Wang, X. W., Yeh, H., Schaeffer, L., Roy, R., Moncollin, V., Egly, J. M., Wang, Z., Friedberg, E. C., Evans, M. K., Taffe, B. G., et al. (1995). p53 modulation of TFIIH-associated nucleotide excision repair activity. Nat. Genet. 10, 188-195.
60. Waterman, M. J. F., Stavridi, E. S., Waterman, J. L. F., and Halazonetis, T. D. (1998). ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nat. Genet. 19, 175-178.
61. Wen, W., Meinkoth, J. L., Tsien, R. Y., and Taylor, S. S. (1995). Identification of a signal for rapid export of proteins from the nucleus. Cell 82, 463-473.
62. Yaciuk, P., and Moran, E. (1991). Analysis with specific polyclonal antiserum indicates that the E1A-associated 300 Kda product is a stable nuclear phosphoprotein that undergoes cell cycle phase-specific modification. Mol. Cell. Biol. 11, 5389-5397.
63. Yew, P. R., and Berk, A. J. (1992). Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein Nature 357, 82-85.
64. Yew, P. R., Liu, X., and Berk, A. J. (1994). Adenovirus E1B oncoprotein tethers a transcriptional repression domain to p53. Genes Dev. 8, 190-202.
65. Yu, A., Bailey, A. D., and Weiner, A. M. (1998). Metaphase fragility of the human RNU1 and RNU2 loci is induced by actinomycin D through a p53-dependent pathway. Hum. Mol. Genet. 7, 609-617.
66. Zantema, A., Schrier, P. I., Davis-Olivier, A., van Laar, T., Vaessen, R. T. M. J., and van der Eb, A. J. (1985). Adenovirus serotype determines association and localization of the large E1B tumor antigene with cellular antigen p53 in transformed cells. Mol. Cell. Biol. 5, 3084-3091.
67. zur Hausen, H. (1967). Induction of specific chromosomal aberrations by adenovirus type 12 in human embryonic kidney cells. J. Virol. 1, 1174-1185.