The dual effect of adenovirus type 5 E1A 13S protein on NF-κB activation is antagonized by E1B 19K

Molecular and Cellular Biology

Volumn 16, Issue 8, 1996, Pages 4052-4063

  Schmitz, M Lienhard ^a   Indorf, Almut ^a   Limbourg, Florian P ^a   Städtler, Heike ^a   Traenckner, E Britta Mareen ^a   Baeuerle, Patrick A ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; REACTIVE OXYGEN METABOLITE; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; VIRUS PROTEIN;

ADENOVIRUS 5; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL STRAIN COS1; CONTROLLED STUDY; ETIOLOGY; GENETIC TRANSCRIPTION; HELA CELL; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; RNA SPLICING; TATA BOX; VIRUS GENE;

EID: 0029899056     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.8.4052     Document Type: Article

References (105)

1. Akusjärvi, G. 1993. Proteins with transcription regulatory properties encoded by human adenoviruses. Trends Microbiol. 163:163-170.
2. Arany, Z., D. Newsome, E. Oldread, D. M. Livingstone, and R. Eckner. 1995. A family of transcriptional adaptor proteins targeted by the E1A oncoprotein. Nature (London) 374:81-84.
3. Baeuerle, P. A., and D. Baltimore. 1988. IκB: a specific inhibitor of the NF-κB transcription factor. Science 242:540-546.
4. Bagchi, S., P. Raychaudhuri, and J. R. Nevins. 1989. Phosphorylation-dependent activation of the adenovirus-inducible E2F transcription factor in a cell-free system. Proc. Natl. Acad. Sci. USA 86:4352-4356.
5. Bagchi, S., P. Raychaudhuri, and J. R. Nevins. 1990. Adenovirus E1A proteins can dissociate heteromeric complexes involving the E2F transcription factor: a novel mechanism for E1A trans-activation. Cell 62:659-669.
6. Bandara, L. R., and N. B. La Thangue. 1991. Adenovirus E1A prevents the retinoblastoma gene product from complexing with a cellular transcription factor. Nature (London) 351:494-497.
7. Baniahmad, A., A. C. Kohne, and R. Renkawitz. 1992. A transferable silencing domain is present in the thyroid hormone receptor, in the v-erbA oncogene product and in the retinoic acid receptor. EMBO J. 11:1015-1023.
8. Beg, A. A., and A. S. Baldwin, Jr. 1993. The IκB proteins: multifunctional regulators of Rel/NF-κB transcription factors. Genes Dev. 7:2064-2070.
9. Beg, A. A., W. C. Sha, R. T. Bronson, S. Gosh, and D. Baltimore. 1995. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB. Nature (London) 376:167-170.
10. Bergmann, Y., and D. Shavit. 1988. Regulation of the Ig κ-chain enhancer by the adenovirus E1A gene products. J. Immunol. 140:2073-2080.
11. Berkenstam, A., M. del Mar Vivanco Ruiz, D. Barettino, M. Horikoshi, and H. G. Stunnenberg. 1992. Cooperativity in transactivation between retinoic acid receptor and TFIID requires an activity analogous to E1A. Cell 69: 401-412.
12. Bernards, R., P. I. Schrier, A. Houweling, J. L. Bos, and A. J. Van der Eb. 1983. Tumorigenicity of cells transformed by adenovirus type 12 by evasion of T-cell immunity. Nature (London) 305:776-779.
13. Borelli, E., R. Hen, and P. Chambon. 1984. Adenovirus-2 E1A products repress enhancer-induced stimulation of transcription. Nature (London) 312:608-612.
14. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
15. Brockman, J. A., D. C. Scherer, T. A. McKinsey, S. M. Hall, X. Qi, W. Y. Lee, and D. W. Ballard. 1995. Coupling of a signal response domain in IκBα to multiple pathways for NF-κB activation. Mol. Cell. Biol. 15:2809-2818.
16. Brown, K., S. Gerstberger, L. Carlson, G. Franzoso, and U. Siebenlist. 1995. Control of IκB-α proteolysis by site-specific, signal-induced phosphorylation. Science 267:1485-1488.
17. Chen, Z., J. Hagler, V. J. Palombella, F. Melandri, D. Scherer, D. Ballard, and T. Maniatis. 1995. Signal-induced site-specific phosphorylation targets IκB-α to the ubiquitin-proteasome pathway. Genes Dev. 9:1586-1597.
18. Das, G., C. S. Hinkley, and W. Herr. 1995. Basal promoter elements as a selective determinant of transcriptional activator function. Nature (London) 374:657-660.
19. Debbas, M., and E. White. 1993. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:546-554.
20. Deryckere, F., C. Ebenau-Jehle, W. S. M. Wold, and H.-G. Burgert. 1995. Tumor necrosis factor α increases expression of adenovirus E3 proteins. Immunobiology 193:186-192.
21. De Wet, J. R., K. V. Wood, M. deLuca, D. R. Helinski, and S. Subramani. 1987. Firefly luciferase gene: structure and expression in mammalian cells. Mol. Cell. Biol. 7:725-737.
22. Du, W., D. Thanos, and T. Maniatis. 1993. Mechanisms of transcriptional synergism between distinct virus-inducible enhancer elements. Cell 74:887-898.
23. Eckner, R., M. E. Ewen, D. Newsome, M. Gerdes, J. A. DeCaprio, J. Bentley Lawrence, and D. M. Livingstone. 1994. Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor. Genes Dev. 8:869-884.
24. 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 160:292-296.
25. Emani, K. H., W. W. Navarre, and S. T. Smale. 1995. Core promoter specificities of the SP1 and VP16 transcriptional activation domains. Mol. Cell. Biol. 15:5906-5916.
26. Evans, A. S. 1958. Latent adenovirus infections of the human respiratory tract. Am. J. Hyg. 67:256-629.
27. Folkers, G. E., and P. T. van der Saag. 1995. Adenovirus E1A functions as a cofactor for retinoic acid receptor β (RARβ) through direct interaction with RARβ. Mol. Cell. Biol. 15:5868-5878.
28. Fox, J. P., C. E. Hall, and M. K. Cooney. 1977. The Seattle virus watch. VII. Observations of adenovirus infections. Am. J. Epidemiol. 105:362-396.
29. Graham, F. L., A. J. Van der Eb, and H. L. Heineker. 1974. Size and location of the transforming region in human adenovirus type 5. Nature (London) 251:687-691.
30. Grilli, M., J. J. Chiu, and M. J. Lenardo. 1993. NF-κB and rel - participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 143:1-62.
31. Grimm, S., M. K. A. Bauer, P. A. Baeuerle, and K. Schulze-Osthoff. 1996. Bcl-2 downregulates the activity of transcription factor NF-κB which is induced upon apoptosis. J. Cell Biol. 134:1-12.
32. Hagmeyer, B. M., H. König, I. Herr, R. Offringa, A. Zantema, A. J. Van der Eb, P. Herrlich, and P. Angel. 1993. Adenovirus E1A negatively and positively modulates transcription of AP-1 dependent genes by dimer-specific regulation of the DNA binding and transactivation activities of Jun. EMBO J. 12:3559-3572.
33. Hannon, G. J., D. Demetrich, and D. Beach. 1993. Isolation of the Rb-related p130 through its interaction with cdk2 and cyclins. Genes Dev. 7:2378-2391.
34. Hashimoto, S., A. Ishii, and S. Yonehara. 1991. The E1B oncogene of adenovirus confers cellular resistance to cytotoxicity of tumor necrosis factor and monoclonal anti-Fas antibody. Int. Immunol. 3:343-351.
35. Hateboer, G., A. Gennissen, Y. F. M. Ramos, R. M. Kerkhoven, V. Sonntag-Buck, H. G. Stunnenberg, and R. Bernards. 1995. BS69, a novel adenovirus E1A-associatcd protein that inhibits E1A transactivation. EMBO J. 14: 3159-3169.
36. Hirai, H., T. Suzuki, J. Fujisawa, J. Inoue, and M. Yoshida. 1994. Tax protein of human T-cell leukemia virus type I binds to the ankyrin motifs of inhibitory κB and induces nuclear translocation of transcription factor NF-κB proteins for transcriptional activation. Proc. Natl. Acad. Sci. USA 91:3584-3588.
37. Hoeffler, W. K., R. Kovelman, and R. G. Roeder. 1988. Activation of transcription factor 3C by the adenovirus E1A protein. Cell 53:907-920.
38. Houweling, A., P. J. Van den Elsen, and A. J. Van der Eb. 1980. Partial transformation of primary rat cells by leftmost 4.5% fragment of adenovirus 5 DNA. Virology 105:537-550.
39. Howe, J. A., and S. T. Bayley. 1992. Effects of Ad 5 E1A mutant viruses on the cell cycle in relation to the binding of cellular proteins including the retinoblastoma protein and cyclin A. Virology 186:15-24.
40. Israël, A. 1995. A role for phosphorylation and degradation in the control of NF-κB activity. Trends Genet. 11:203-205.
41. Israël, N., M. A. Gougertot-Pocidalo, F. Aillet, and J. L. Virelizier. 1992. Redox status of cells influences constitutive or induced NF-κB translocation and HIV long terminal repeat activity in human T and monocytic cell lines. J. Immunol. 149:3386-3393.
42. Kaltschmidt, B., P. A. Baeuerle, and C. Kaltschmidt. 1993. Potential role of transcription factor NF-κB in neurological disorder. Mol. Aspects Med. 14:171-190.
43. Kanno, T., G. Franzoso, and U. Siebenlist. 1994. Human T-cell leukemia virus type I Tax protein-mediated activation of NF-κB from p100 (NF-κB2)-inhibited cytoplasmic reservoirs. Proc. Natl. Acad. Sci. USA 91:12634-12638.
44. Kaszubska, W., R. H. van Huisduijnen, P. Ghersa, A.-M. DeRaemy-Schenk, B. P. C. Chen, T. Hai, J. F. DeLamarter, and J. Whelan. 1993. Cyclic AMP-independent ATF family members interact with NF-κB and function in the activation of the E-selectin promoter in response to cytokines. Mol. Cell. Biol. 13:7180-7190.
45. Kimelman, D., J. S. Miller, U. Porter, and B. E. Roberts. 1985. E1A regions of the human adenoviruses and the highly oncogenic simian adenovirus 7 are closely related. J. Virol. 53:399-409.
46. Röntgen, F., R. J. Grumont, A. Strasser, D. Metcalf, R. Li, D. Tarlinton, and S. Gerondakis. 1995. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 9:1965-1977.
47. Lee, W. S., C. Cheng Kao, G. O. Bryant, X. Liu, and A. J. Berk. 1991. Adenovirus E1A activation domain binds the basic repeat in the TATA binding transcription factor. Cell 67:365-376.
48. Lernbecher, T., U. Müller, and T. Wirth. 1993. Distinct NF-κB/Rel transcription factors are responsible for tissue-specific and inducible gene activation. Nature (London) 356:767-770.
49. Levine, B., Q. Huang, J. T. Isaacs, J. C. Reed, D. E. Griffin, and J. M. Hardwick. 1993. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature (London) 361:739-742.
50. Li, Y., C. Graham, C. Lacy, A. M. V. Duncan, and P. Whyte. 1993. The adenovirus E1A-associated 130 kD protein is encoded by a member of the retinoblastoma gene family and physically interacts with cyclin A and E. Genes Dev. 7:2366-2377.
51. 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.
52. Lillie, J. W., and M. R. Green. 1989. Transcription activation by the adenovirus E1A protein. Nature (London) 338:39-44.
53. Limbourg, F. P., P. A. Baeuerle, and M. L. Schmitz. Unpublished data.
54. Lin, K.-I., S.-H. Lee, R. Narayanan, J. M. Baraban, J. M. Hardwick, and R. R. Ratan. 1995. Thiol agents and Bcl-2 identify an alphavirus-induced apoptotic pathway that requires activation of the transcription factor NF-κB. J. Cell Biol. 131:1149-1161.
55. Liu, F., and M. R. Green. 1990. A specific member of the ATF transcription factor family can mediate transcription activation by the adenovirus E1A protein. Cell 61:1217-1224.
56. Liu, F., and M. R. Green. 1994. Promoter targeting by adenovirus E1A through interaction with different cellular DNA-binding domains. Nature (London) 368:520-525.
57. Lopata, M. A., D. W. Cleveland, and B. Sollner-Webb. 1984. High level transient expression of a chloramphenicol acetyl transferase gene by DEAE-dextran mediated DNA transfection coupled with a dimethylsulfoxide or glycerol shock treatment. Nucleic Acids Res. 12:5707-5717.
58. Lundblad, J. R., R. P. S. Kwok, M. E. Laurance, M. L. Harter, and R. H. Goodman. 1995. Adenoviral E1A associated protein p300 as a functional homologue of the transcriptional co-activator CBP. Nature (London) 374: 85-88.
59. Meijer, I., A. J. M. Boot, G. Mahibir, A. Zantema, and A. J. Van der Eb. 1992. Reduced binding activity of transcription factor NFκB accounts for MHC class 1 repression in adenovirus type 12 E1-transformed cells. Cell. Immunol. 145:56-65.
60. Metz, R., A. J. Bannister, J. A. Sutherland, C. Hagemeier, E. C. O'Rourke, A. Cook, R. Bravo, and T. Kouzarides. 1994. c-Fos-induced activation of a TATA-box-containing promoter involves direct contact with TATA-box-binding protein. Mol. Cell. Biol. 14:6021-6029.
61. Miyamoto, S., P. J. Chiao, and I. M. Verma. 1994. Enhanced IκBα degradation is responsible for constitutive NF-κB activity in mature murine B-cell lines. Mol. Cell. Biol. 14:3276-3282.
62. Moran, M., and M. B. Mathews. 1987. Multiple functional domains in the adenovirus E1A gene. Cell 48:177-178.
63. Munoz, E., and A. Israël. 1995. Activation of NF-κB by the Tax protein of HTLV-1. Immunobiology 193:128-136.
64. Nielsch, U., S. G. Zimmer, and L. E. Babiss. 1991. Changes in NF-κB and ISGF3 DNA binding activities are responsible for differences in MHC and β-IFN gene expression in Ad5- versus Ad12-transformed cells. EMBO J. 10:4169-4175.
65. Paal, K., P. A. Baeuerle, and M. L. Schmitz. Unpublished data.
66. Pahl, H. L., and P. A. Baeuerle. 1994. Oxygen and the control of gene expression. Bioessays 16:497-502.
67. Pahl, H. L., and P. A. Baeuerle. 1995. Expression of influenza virus hemagglutinin activates transcription factor NF-κB. J. Virol. 69:1480-1484.
68. Palombella, V. J., O. J. Rande, A. L. Goldberg, and T. Maniatis. 1994. The ubiquitin-proteasome pathway is required for processing the NF-κB1 precursor protein and the activation of NF-κB. Cell 78:773-785.
69. Pierce, J. W., M. Lenardo, and D. Baltimore. 1988. An oligonucleotide that binds nuclear factor NF-κB acts as a lymphoid-specific and inducible enhancer element. Proc. Natl. Acad. Sci. USA 85:1482-1486.
70. Pines, J., and T. Hunter. 1990. Human cyclin A is the E1A-associated protein p60 and behaves differently from cyclin B. Nature (London) 346: 760-763.
71. Rao, L., P. 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.
72. Raychaudhuri, P., S. Bagchi, and J. R. Nevins. 1989. DNA-binding activity of the adenovirus-induced E4F transcription factor is regulated by phosphorylation. Genes Dev. 3:620-627.
73. Sabbatini, P., S.-K. Chiou, L. Rao, and E. White. 1995. Modulation of p53-mediated transcriptional repression and apoptosis by the adenovirus E1B 19K protein. Mol. Cell. Biol. 15:1060-1070.
74. Schmidt, K. N., P. Amstad, P. Cerutti, and P. A. Baeuerle. 1995. The roles of hydrogen peroxide and superoxide as messengers in the activation of transcription factor NF-κB. Chem. Biol. 2:13-22.
75. Schmitz, M. L., and P. A. Baeuerle. 1991. The p65 subunit is responsible for the strong transcription activating potential of NF-κB, EMBO J. 10:3805-3817.
76. Schmitz, M. L., M. A. dos Santos Silva, H. Altmann, M. Czisch, T. A. Holak, and P. A. Baeuerle. 1994. Stuctural and functional analysis of the NF-κB p65 C-terminus: an acidic and modular transactivation domain with the potential to adopt an α-helical conformation. J. Biol. Chem. 269:25613-25620.
77. 1 and phorbol ester-stimulated activity and phosphorylation in intact cells. J. Biol. Chem. 270:15576-15584.
78. Schmitz, M. L., G. Stelzer, H. Altmann, M. Meisterernst, and P. A. Baeuerle. 1995. Interaction of the COOH-terminal transactivation domain of p65 NF-κB with TATA-binding protein, transcription factor IIB, and co-activators. J. Biol. Chem. 270:7219-7226.
79. Schöler, H. R., T. Ciesiolka, and P. Gruss. 1991. A nexus between Oct-4 and E1A: implications for gene regulation in embryonic stem cells. Cell 66:291-304.
80. Schouten, G. J., A. J. Van der Eb, and A. Zantema. 1995. Downregulation of MHC class 1 expression due to interference with p 105-NFκB1 processing by Ad12E1A. EMBO J. 14:1498-1507.
81. Schreck, R., R. Grassmann, B. Fleckenstein, and P. A. Baeuerle. 1992. Antioxidants selectively suppress activation of NF-κB by human T-cell leukemia virus type I Tax protein. J. Virol. 66:6288-6293.
82. Schreiber, E., P. Matthias, M. M. Müller-Immerglück, and W. Schaffner. 1989. Rapid detection of octamer binding proteins with mini-extracts, prepared from a small number of cells. Nucleic Acids Res. 17:6419.
83. Schulze-Osthoff, K., R. Beyaert, V. Van Dervoorde, G. Haegemann, and W. Fiers. 1993. Depletion of the mitochondrial electron transport abrogates the cytotoxic and gene induction effects of TNF. EMBO J. 12:3095-3104.
84. Sha, W. C., H.-C. Liou, E. I. Tuomanen, and D. Baltimore. 1995. Targeted disruption of the p50 subunit of NF-κB leads to multifocal defects in immune responses. Cell 80:321-330.
85. Siebenlist, U., G. Franzoso, and K. Brown. 1994. Structure, regulation and function of NF-κB. Annu. Rev. Cell Biol. 10:405-455.
86. Slater, A. F. G., M. Kimland, S. A. Jiang, and S. Orrenius. 1995. Constitutive nuclear NF-κB/rel DNA-binding activity of rat thymocytes is increased by stimuli that promote apoptosis, but not inhibited by pyrrolidine dithiocarbamate. Biochem. J. 312:833-838.
87. Tarodi, B., T. Subramanian, and G. Chinnadurai. 1993. Functional similarity between adenovirus E1B 19K gene and Bcl2 oncogene: mutant complementation and suppression of cell death induced by DNA damaging agents. Int. J. Oncol. 3:467-472.
88. Thanos, D., and T. Maniatis. 1995. NF-κB: a lesson in family values. Cell 80:529-532.
89. Traenckner, E. B.-M., H. L. Pahl, T. Henkel, K. N. Schmidt, S. Wilk, and P. A. Baeuerle. 1995. Phosphorylation of human IκB-α on serines 32 and 36 controls IκB-α proteolysis and NF-κB activation in response to diverse stimuli. EMBO J. 14:2876-2883.
90. Traenckner, E. B.-M., S. Wilk, and P. A. Baeuerle. 1994. A proteasome inhibitor prevents activation of NF-κB and stabilizes a newly phosphorylated form of IκB-α that is still bound to NF-κB. EMBO J. 13:5433-5441.
91. Van den Elsen, P., A. Houweling, and A. J. Van der Eb. 1983. Morphological transformation of human adenoviruses is determined to a large extent by the products of region E1A. Virology 131:242-246.
92. Velcich, A., and E. Ziff. 1985. Adenovirus E1A proteins repress transcription from the SV40 early promotor. Cell 40:705-716.
93. Verma, I. M., J. K. Stevenson, E. M. Schwarz, D. Van Antwerp, and S. Miyamoto. 1995. Rel/NF-κB/IκB family: intimate tales of association and dissociation. Genes Dev. 9:2723-2735.
94. Wang, H.-G. H., C. Draetta, and E. Moran. 1991. E1A induces phosphorylation of the retinoblastoma protein independently of direct physical association between E1A and retinoblastoma products. Mol. Cell. Biol. 11: 4253-4265.
95. Watanabe, M., M. Muramatsu, H. Hirai, T. Suzuki, J. Fujisawa, Y. Mitsuaki, K. Arai, and N. Arai. 1993. HTLV-1 encoded Tax in association with NF-κB precursor p105 enhances nuclear localisation of NF-κB p50 and p65 in transfected cells. Oncogene 8:2949-2958.
96. Weigel, R. J., S. H. Devoto, and J. R. Nevins. 1990. Adenovirus 12S E1A gene represses differentiation of F9 teratocarcinoma cells. Proc. Natl. Acad. Sci. USA 87:9878-9882.
97. Weih, F., D. Carrasco, S. K. Durham, D. S. Barton, C. A. Rizzo, R.-P. Ryseck, S. A. Lira, and R. Bravo. 1995. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of RelB, a member of the NF-κB/Rel family. Cell 80:331-340.
98. Westendorp, M. O., V. A. Shatrov, K. Schulze-Osthoff, R. Frank, M. Kraft, M. Los, P. H. Krammer, W. Dröge, and V. Lehmann. 1995. HIV-1 Tat potentiates TNF-induced NF-κB activation and cytotoxicity by altering the cellular redox state. EMBO J. 14:546-554.
99. White, E., and R. Cipriani. 1990. Role of adenovirus E1B proteins in transformation: altered organization of intermediate filaments in transformed cells that express the 19-kilodalton protein. Mol. Cell. Biol. 10:120-130.
100. White, E., R. Cipriani, P. Sabbatini, and A. Denton. 1991. The adenovirus E1B 19-kilodalton protein overcomes the cytotoxicity of E1A proteins. J. Virol. 65:2968-2978.
101. White, E., P. Sabattini, M. Debbas, W. S. M. Wold, D. I. Kusher, and L. 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.
102. White, E., and B. Stillman. 1987. Expression of the adenovirus E1B mutant phenotypes is dependent on the host cell and on synthesis of E1A proteins. J. Virol. 61:426-435.
103. Whyte, P., K. J. Buchkovich, J. M. Horowitz, S. F. 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.
104. Whyte, P., N. M. Williamson, and E. Harlow. 1989. Cellular targets for transformation by the adenovirus E1A proteins. Cell 56:67-75.
105. 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.