Importance of the Ser-132 phosphorylation site in cell transformation and apoptosis induced by the adenovirus type 5 E1A protein

Journal of Virology

Volumn 70, Issue 8, 1996, Pages 5373-5383

  Whalen, Steve G ^a   Marcellus, Richard C ^a   Barbeau, Dominique ^a   Branton, Philip E ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN;

ADENOVIRUS 5; AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CELL TRANSFORMATION; ENZYME IMMUNOASSAY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS; VIRUS MUTANT; VIRUS MUTATION; VIRUS VIRULENCE;

EID: 0030013726     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.8.5373-5383.1996     Document Type: Article

References (83)

1. Barbeau, D., R. Charbonneau, S. G. Whalen, S. T. Bayley, and P. E. Branlon. 1994. Functional interactions within adenovirus E1A protein complexes. Oncogene 9:359-373.
2. Barbeau, D., R. C. Marcellus, S. Bacchetti, S. T. Bayley, and P. E. Branton. 1992. Quantitative analysis of regions of adenovirus E1A products involved in interactions with cellular proteins. Biochem. Cell Biol. 70:1123-1124.
3. Barbosa, M. S., C. Edmonds, C. Fisher, J. T. Schiller, D. R. Lowy, and K. H. Vousden. 1990. The region of the HPV E7 oncoprotein homologous to adenovirus E1a and SV40 large T antigen contains separate domains for Rb binding and casein kinase II phosphorylation. EMBO J. 9:153-160.
4. Berk, A. J., and P. A. Sharp. 1978. Structure of the adenovirus 2 early mRNAs. Cell 14:695-711.
5. Carroll, D., N. Santoro, and D. R. Marshak. 1988. Regulating cell growth: casein kinase-II-dependent phosphorylation of nuclear oncoproteins. Cold Spring Harbor Symp. Quant. Biol. 53:91-95.
6. Chow, L. T., T. R. Broker, and J. B. Lewis. 1979. Complex splicing patterns of RNAs from the early regions of adenovirus 2. J. Mol. Biol. 141:249-265.
7. Colby, W. W., and T. Shenk. 1981. Adenovirus type 5 virions can be assembled in vivo in the absence of detectable polypeptide IX. J. Virol. 39:977-980.
8. Corbeil, H. B., and P. E. Branton. 1994. Functional importance of complex formation between the retinoblastoma tumor suppressor family and adenovirus E1A proteins as determined by mutational analysis of E1A conserved region 2. J. Virol. 68:6697-6707.
9. Debbas, M., and E. White. 1993. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:546-554.
10. cdc2 protein kinase. Virology 189:111-120.
11. Dumont, D. J., R. C. Marcellus, S. T. Bayley, and P. E. Branton. 1993. Role of phosphorylation near the amino terminus of adenovirus type 5 early region 1A proteins. J. Gen. Virol. 74:583-595.
12. 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.
13. Dyson, N., R. Bernards, S. H. Friend, L. R. Gooding, J. A. Hassell, E. O. Major, J. M. Pipas, T. Vandyke, and E. Harlow. 1990. Large T antigens of many polyomaviruses are able to form complexes with the retinoblastoma protein. J. Virol. 64:1353-1356.
14. 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-kD protein (p300) reveals a protein with properties of a transcriptional adapter. Genes Dev. 8:869-884.
15. 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.
16. 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 1A of human adenovirus type 5. Mol. Cell. Biol. 8:3955-3959.
17. Egan, C., S.-P. Yee, B. Ferguson, M. Rosenberg, and P. E. Branton. 1987. Binding of cellular polypeptides to human adenovirus type 5 E1A proteins produced in Escherichia coli. Virology 169:292-296.
18. Ewen, M. E., Y. Xing, J. Bentley-Lawrence, and D. M. Livingston. 1991. Molecular cloning, chromosomal mapping, and expression of the cDNA for p107, a retinoblastoma gene product-related protein. Cell 66:1155-1164.
19. cdk2. J. Virol. 67:2456-2465.
20. Ferguson, B., N. Jones, J. Richter, and M. Rosenberg. 1984. Adenovirus E1A gene product expressed at high levels in Escherichia coli is functional. Science 224:1343-1346.
21. Firzlaff, J. M., D. A. Galloway, R. N. Eisenman, and B. Lüscher. 1989. The E7 protein of human papillomavirus type 16 is phosphorylated by casein kinase II. New Biol. 1:44-53.
22. Firzlaff, J. M., B. Lüscher, and R. N. Eisenman. 1991. Negative charge at the casein kinase II phosphorylation site is important for transformation but not for Rb protein binding by the E7 protein of human papillomavirus type 16. Proc. Natl. Acad. Sci. USA 88:5187-5191.
23. 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.
24. Graham, F. L., H. L. Heijneker, and A. J. van der Eb. 1974. Size and location of the transforming region in human adenovirus DNA. Nature (London) 251:687-691.
25. 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.
26. 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.
27. Haley, K. P., J. Overhauser, L. E. Babiss, H. S. Ginsberg, and N. C. Jones. 1984. Transformation properties of type 5 adenovirus mutants that differentially express the E1A gene products. Proc. Natl. Acad. Sci. USA 81:5734-5738.
28. Harlow, E., B. R. Franza, Jr., and C. Schley. 1985. Monoclonal antibodies specific for adenovirus early region 1A proteins: extensive heterogeneity in early region 1A products. J. Virol. 55:533-546.
29. 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.
30. Harter, M. L., and J. B. Lewis. 1978. Adenovirus type 2 early proteins synthesized in vivo and in vitro: identification in infected cells of the 38,000-to 50,000-molecular-weight protein coded by the left end of the adenovirus type 2 genome. J. Virol. 26:736-749.
31. 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.
32. Hateboer, G., H. T. M. Timmers, A. K. Rustgi, M. Biaaud, L. J. van'T Veer, and R. Bernards. 1993. TATA-binding protein and the retinoblastoma gene product bind to overlapping epitopes on c-Myc and adenovirus E1A protein. Proc. Natl. Acad. Sci. USA 90:8489-8493.
33. Heck, D. V., C. L. Yee, P. M. Howley, and K. Münger. 1992. Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses. Proc. Natl. Acad. Sci. USA 89:4442-4446.
34. 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.
35. Jelsma, T. N., J. A. Howe, J. S. Mymryk, C. M. Evelegh, N. F. A. Cuniff, and S. T. Bayley. 1989. Sequences in EIA proteins of human adenovirus 5 required for cell transformation, repression of a transcriptional enhancer, and induction of proliferating cell nuclear antigen. Virology 171:120-130.
36. 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.
37. Kitchingman, G. R., and H. Westphal. 1980. The structure of adenovirus 2 early nuclear and cytoplasmic RNAs. J. Mol. Biol. 137:23-48.
38. Kuppuswamy, M. N., and G. Chinnadurai. 1987. Relationship between the transforming and transcriptional regulatory functions of adenovirus 2 E1a oncogene. Virology 159:31-38.
39. Land, H., L. F. Parada, and R. A. Weinberg. 1983. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature (London) 304:596-602.
40. Larose, A., N. Dyson, M. Sullivan, E. Harlow, and M. Bastin. 1991. Polyomavirus large T mutants affected in retinoblastoma protein binding are defective in immortalization. J. Virol. 65:2308-2313.
41. 14C in polyacrylamide gels by fluorography. Eur. J. Biochem. 56:335-341.
42. Lee, W. S., C. Kao, G. O. Bryant, X. Liu, and A. J. Berk. 1991. Adenovirus E1A activation domain binds the basic repeat in the TATA box transcription factor. Cell 67:365-376.
43. Lillie, J. W., M. Green, and M. R. Green. 1986. An adenovirus E1A protein region required for transformation and transcriptional repression. Cell 46: 1043-1051.
44. Lillie, J. W., P. M. Loewenstein, M. R. Green, and M. Green. 1987. Functional domains of adenovirus type 5 E1a proteins. Cell 50:1091-1100.
45. Liu, F., and M. Green. 1994. Promoter targeting by adenovirus E1a through interaction with different cellular DNA-binding domains. Nature (London) 368:520-525.
46. 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.
47. Marcellus, R. C., J. G. Teodoro, T. Wu, D. E. Brough, G. Keiner, G. S. Shore, and P. E. Branton. Adenovirus 5 early region 4 is responsible for E1A-induced p53-independent apoptosis. Submitted for publication.
48. 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.
49. McKinnon, R. D., S. Bacchetti, and F. L. Graham. 1982. Tn5 mutagenesis of the transforming genes of human adenovirus type 5. Gene 19:33-42.
50. McLorie, W., C. J. McGlade, D. Takayesu, and P. E. Branton. 1991. Individual adenovirus E1A proteins induce transformation independently but by additive pathways. J. Gen Virol. 72:1467-1471.
51. Montell, C., G. Courtois, C. Eng, and A. J. Berk. 1984. Complete transformation by adenovirus 2 requires both E1A proteins. Cell 36:951-961.
52. Montell, C., E. F. Fisher, M. H. Caruthers, and A. J. Berk. 1982. Resolving the functions of overlapping genes by site-specific mutagenesis at a mRNA splice site. Nature (London) 295:380-384.
53. Moran, E. Unpublished data.
54. Moran, E., T. Grodzicker, R. J. Roberts, M. B. Mathews, and B. Zerler. 1986. Lytic and transforming functions of individual products of the adenovirus E1A gene. J. Virol. 57:765-775.
55. Münger, K., B. A. Werness, N. Dyson, W. C. Phelps, E. Harlow, and P. M. Howley. 1989. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J. 8:4099-4105.
56. 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.
57. Pearson, R. B., and B. E. Kemp. 1991. Protein kinase phosphorylation site sequences and consensus specificity motifs. Methods Enzymol. 200:62-81.
58. Perricaudet, M., G. Aküsjarvi, A. Virtanen, and U. Pettersson. 1979. Structure of two spliced mRNAs from the transforming region of human subgroup C adenoviruses. Nature (London) 281:694-696.
59. Phelps, W. C., K. Münger, C. L. Yee, J. A. Barnes, and P. M. Howley. 1992. Structure-function analysis of the human papillomavirus type 16 E7 oncoprotein. J. Virol. 66:2418-2427.
60. Popperl, H., and M. S. Featherstone. 1992. An autoregulatory element of the murine Hox-4.2 gene. EMBO J. 11:3673-3680.
61. Querido, E., J. G. Teodoro, and P. E. Branton. Unpublished data.
62. 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.
63. Ricciardi, R. P., R. L. Jones, C. L. Cepko, P. A. Sharp, and B. E. Roberts. 1981. Expression of early adenovirus genes requires a viral encoded acidic polypeptide. Proc. Natl. Acad. Sci. USA 78:1621-1625.
64. Rowe, D. T., F. L. Graham, and P. E. Branton. 1983. Intracellular localization of adenovirus type 5 tumor antigens in productively infected cells. Virology 129:456-468.
65. Ruley, H. E. 1983. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature (London) 304:602-606.
66. Schneider, J. F., F. Fisher, C. Gooding, and N. C. Jones. 1987. Mutational analysis of the adenovirus E1A gene: the role of transcriptional regulation in transformation. EMBO J. 6:2053-2060.
67. 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.
68. Subramanian, T., B. Tarodi, and C. Chinnadurai. 1995. p53-independent apoptotic and necrotic cell deaths induced by adenovirus infection: suppression by E1B 19K and Bcl-2 proteins. Cell Growth Differ. 652:131-137.
69. Svensson, C., M. Bondesson, E. Nyberg, S. Linder, N. Jones, and G. Akusjärvi. 1991. Independent transformation activity by adenovirus-5 Ela-conserved regions 1 or 2 mutants. Virology 182:553-561.
70. 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.
71. Tremblay, M. L., D. J. Dumont, and P. E. Branton. 1989. Analysis of phosphorylation sites in the exon 1 region of E1A proteins of human adenovirus type 5. Virology 169:397-407.
72. Tremblay, M. L., C. J. McGlade, G. E. Gerber, and P. E. Branton. 1988. Identification of the phosphorylation sites in the early region 1A proteins of adenovirus type 5 by analysis of proteolytic peptides and amino acid sequencing. J. Biol. Chem. 263:6375-6383.
73. Tsukamoto, A. S., A. Ponticelli, A. J. Berk, and R. B. Gaynor. 1986. Genetic mapping of a major site of phosphorylation in adenovirus type 2 E1A proteins. J. Virol. 59:14-22.
74. Wang, H.-G. H., Y. Rikitake, M. C. Carter, P. Yaciuk, S. E. Abraham, B. Zerler, and E. Moran. 1993. Identification of specific adenovirus E1A N-terminal residues critical to the binding of cellular proteins and to the control of cell growth. J. Virol. 67:476-488.
75. Webster, L. C., and R. P. Ricciardi. 1991. trans-dominant mutants of E1A provide genetic evidence that the zinc finger of the trans-activating domain binds a transcription factor. Mol. Cell. Biol. 11:4287-4296.
76. Weeks, D. L., and N. C. Jones. 1983. E1A control of gene expression is mediated by sequences 5′ to the transcriptional starts of the early viral genes. Mol. Cell. Biol. 3:1222-1234.
77. Whalen, S. G., R. C. Marcellus, D. Barbeau, and P. E. Branton. Unpublished data.
78. 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.
79. 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.
80. 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.
81. Whyte, P., N. M. Williamson, and E. Harlow. 1989. Cellular targets for transformation by the adenovirus E1A proteins. Cell 56:67-75.
82. 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.
83. Yee, S.-P., D. T. Rowe, M. L. Tremblay, M. McDermott, and P. E. Branton. 1983. Identification of human adenovirus early region 1 products using antisera against synthetic peptides corresponding to the predicted carboxy terminus. Virology 46:1003-1013.