The human papillomavirus type 16 E7 protein complements adenovirus type 5 E1A amino-terminus-dependent transactivation of adenovirus type 5 early genes and increases ATF and Oct-1 DNA binding activity

Journal of Virology

Volumn 70, Issue 1, 1996, Pages 332-340

  Wong, Henry K ^a   Ziff, Edward B ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; MUTANT PROTEIN; VIRUS ANTIGEN; VIRUS PROTEIN;

ADENOVIRUS 5; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL CULTURE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC COMPLEMENTATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SIMIAN VIRUS 40; TRANSACTIVATION; VIRUS CELL TRANSFORMATION; VIRUS GENE; VIRUS TRANSCRIPTION; WART VIRUS;

3T3 CELLS; ADENOVIRUS E1A PROTEINS; ADENOVIRUSES, HUMAN; ANIMAL; BASE SEQUENCE; BLOOD PROTEINS; DNA, VIRAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, VIRAL; GENES, VIRAL; GENETIC COMPLEMENTATION TEST; HELA CELLS; HUMAN; MICE; MOLECULAR SEQUENCE DATA; ONCOGENE PROTEINS, VIRAL; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-JUN; RETINOBLASTOMA PROTEIN; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, NON-P.H.S.; SUPPORT, U.S. GOV'T, P.H.S.; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

EID: 0029656147     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.1.332-340.1996     Document Type: Article

References (95)

1. Abdel-Hafiz, H. A., C. Y. Chen, T. Marcell, D. J. Kroll, and J. P. Hoeffler. 1993. Structural determinants outside of the leucine zipper influence the interactions of CREB and ATF-2: interaction of CREB with ATF-2 blocks E1a-ATF-2 complex formation. Oncogene 8:1161-1174
2. Abraham, S. E., S. Lobo, P. Yaciuk, H. G. Wang, and E. Moran. 1993. p300, and p300-associated proteins, are components of TATA-binding protein (TBP) complexes Oncogene 8:1639-1647.
3. Angel, P., E. A. Allegretto, S. T. Oklno, K. Hattori, W. J. Boyle, T. Hunter, and M. Karin. 1988. Oncogene jun encodes a sequence-specific trans-activator similar to AP-1. Nature (London) 332:166-171.
4. Arany, Z., W. R. Sellers, D. M. Livingston, and R. Eekner. 1994. E1A-associated p300 and CREB-associated CBP belong to a conserved family of coacrivators. Cell 77:799-800 (Letter.)
5. Arroyo, M., and P. Raychaudhuri. 1992. Retinoblastoma-repression of E2F-dependent transcription depends on the ability of the retinoblastoma protein to interact with E2F and is abrogated by the adenovirus E1A oncoprotein. Nucleic Acids Res 20:5947-5954.
6. Ausubel, F. M., R. Brent, R, E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1994 Current protocols in molecular biology. John Wiley & Sons, New York.
7. 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.
8. Baker, C. C., W. C. Phelps, V. Lindgren, M. J. Braun, M. A. Gonda, and P. M. Howley. 1987. Structural and transcriptional analysis of human papillomavirus type 16 sequences in cervical carcinoma cell tines J. Virol. 61:962-971.
9. Barbeau, D., R. Charbonneau, S. G. Whalen, S. T. Bayley, and P. E. Branton, 1994. Functional interactions within adenovirus E1A protein complexes Oncogene 9:359-373.
10. Berk, A. J. 1986. Functions of adenovirus E1A Cancer Surv. 5:367-387
11. Berk, A. J., F. Lee, T. Harrison, J. Williams, and P. A. Sharp. 1979 Pre-early adenovirus 5 gene product regulates, synthesis of early viral messenger RNAs Cell 17:935-944.
12. Berk, A. J., and P. A. Sharp. 1978. Structure of the adenovirus 2 early mRNAs Cell 14:695-711
13. Braithwaite, A. W., C. C. Nelson, and A. J. Bellett. 1991 E1a revisited: the case for multiple cooperative trans-activation domains. New Biol 3:18-26.
14. Buchkovich, K., N. Dyson, P. Whyte, and E. Harlow. 1990. Cellular proteins that are targets for transformation by DNA tumour viruses. Ciba Found. Symp. 150:262-278.
15. Buchou, T., O. Kranenburg, H. van Dam, D. Roelen, A. Zantema, F. L. Hall, and A. van der Eb. 1993. Increased cyclin A and decreased cyclin D levels in adenovirus 5 E1A-transformed rodent cell lines. Oncogene 8:1765-1773.
16. Can, L., B. Faha, M. Dembski, L. H. Tsai, E. Harlow, and N. Dyson. 1992. Independent binding of the retinoblastoma protein and p107 to the transcription factor E2F. Nature (London) 355:176-179.
17. Carlotti, F., and L. Crawford. 1993. Trans-activation of the adenovirus E2 promoter by human papillomavirus type 16 E7 is mediated by retinobiastoma-dependent and -independent pathways J Gen Virul 74:2479-2486.
18. Challberg, M. D., and T. J. J. Kelly. 1979. Adenovirus replication in vitro. Proc. Natl Acad. Sci. USA 76:655-659.
19. Chatton, B., J. L. Bocco, M. Gaire, C. Hauss, B. Reimund, J. Goetz, and C. Kedinger. 1993. Transeriplional activation by the adenovirus larger E1a product is mediated by members of the cellular transcription factor ATF family which can directly associate with E1a. Mol. Cell Biol 13:561-570.
20. Chellappan, S. P., and J. R. Nevins. 1990 DNA octamer element can confer E1A trans-acttvation, and adenovirus infection results in a stimulation of the DNA-binding activity- of OTF-I/NFIII factor Proc. Nail. Acad. Sci. USA 87:5878-5882.
21. Chittenden, T., D. M. Livingston, and J. A. DcCaprio. 1993. Increased cyclin A and decreased cyclin D levels in adenovirus 5 E1A-tiansformed rodent cell lines. Mol. Cell. Biol. 13:3975-3983.
22. Ciccolini, F., G. Di Pasquale, F. Carlotti, L. Crawford, and M. Tommasino. 1994. Functional studies of E7 proteins from different HPV types. Oncogene 9:2633-2638
23. Cobrinik, D., P. Whyte, D. S. Peeper, T. Jacks, and R. A. Weinberg. 1993. Cell cycle-specific association of E2F with the p130 E1A-binding protein. Genes Dev. 7:2392-2404.
24. DeCaprio, J. A., J. W. Ludlow, J. Figge, J. Y. Shew, C. M. Huang, W. H. Lee, E. Marsilio, E. Paucha, and D. M. Livingston. 1988 SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell 54:275-283.
25. Dyson, N., K. Buchkovich, P. Whyte, and E. Harlow. 1989. The cellular 107K protein that binds to adenovirus E1A also associates with the large T antigens of SV40 and JC virus. Cell 58:249-255.
26. Dyson, N., P. Guida, K. Munger, and E. Harlow. 1992. Homologous sequences in adenovirus E1A and human papillomavirus E7 proteins mediate interaction with the same set of cellular proteins. J. Virol. 66:6893-6902.
27. Dyson, N., P. M. Howley, K. Munger, and E. Harlow. 1989. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934-937.
28. 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 adaptor. Genes Dev. 8:869-884.
29. 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.
30. Ewen, M. E., B. Faha, E. Harlow, and D. M. Livingston. 1992. Interaction of p 107 with cyclin A independent of complex formation with viral oncoproteins. Science 255:85-87.
31. Faha, B., M. E. Ewen, L. H. Tsai, D. M. Livingston, and E. Harlow. 1992. Interaction between human cyclin A and adenovirus E1A-associated p107 protein. Science 255:87-90
32. Fattaey, A. R., E. Harlow, and K. Helin. 1993. Independent regions of adenovirus E1A are required for binding to and dissociation of E2F-protein complexes Mol Cell. Biol. 13:7267-7277
33. Feinberg, A. P., and B. Vogelstein. 1983 A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity Anal Biochem. 132:6-13.
34. Gedrich, R. W., S. T. Bayley, and D. A. Engel. 1992. Induction of AP-1 DNA-binding activity and c-fos mRNA by the adenovirus 243R E1A protein and cyclic AMP requires domains necessary for transformation. J. Virol 66:5849-5859.
35. Geisberg, J. V., W. S. Lee, A. J. Berk, and R. P. Ricciardi. 1994. The zinc finger region of the adenovirus E1A transactivating domain complexes with the TATA box binding protein. Proc. Natl. Acad. Sci USA 91:2488-2492.
36. Giordano, A., P. Whyte, E. Harlow, B. R. Franza, Jr., D. Beach, and G. Draetta. 1989 A 60 kd cdc2-associated polypeptide complexes with the E1A proteins in adenovirus-infected cells. Cell 58:981-990.
37. Guilfoyle, R. A., W. P. Osheroff, and M. Rossini. 1985 Two functions encoded by adenovirus early region 1A are responsible for the activation and repression of the DNA-binding protein gene. EMBO J. 4:707-713
38. Hagmeyer, B. M., H. Konig, I. Herr, R. Offringa, A. Zantema, A. 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.
39. Hannon, G. J., D. Demetrick, and D. Beach. 1993 Isolation of the Rb-related p130 through its interaction with CDK2 and cyclins Genes Dev 7:2378-2391.
40. Harlow, E., R. Franza, 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
41. Harlow, E., P. Whyte, B. R. Franza, Jr., and C. Schlev 1986. Association of adenovirus early-region 1A proteins with cellular polypeptides. Mol. Cell. Biol. 6:1579-1589.
42. Horikoshi, N., K. Maguire, A. Kralli. E. Maldonado, D. Reinberg, and R. Weinmann. 1991. Direct interaction between adenovirus E1A protein and the TATA box binding transcription factor HD. Proc. Natl. Acad. Sci. USA 88:5124-5128.
43. Huang, S., E. Shin, K. A. Sheppard, Chok, Y. W. Qian, E. Y. Lee. and A. S. Yee. 1992. The retinoblastoma protein region required for interaction with the E2F transcription factor includes the T/E1A binding and carboxy-terminal sequences. DNA Cell Biol. 11:539-548.
44. Johnson, D. G., J. K. Schwarz, W. D. Cress, and J. R. Nevins. 1993. Expression of transcription factor E2F1 induces quiescent cells to enter S phase Nature (London) 365:349-352.
45. Jones, N., and T. Shenk. 1979. An adenovirus type 5 early gene function regulates expression of other eaily viral genes. Proc. Natl. Acad. Sci. USA 76:3665-3669.
46. Jones, N. C., P. W. Rigby, and E. B. Ziff. 1988. Trans-acting protein factors and the regulation of eukaryotic transcription: lessons from studies on DNA tumor viruses. Genes Dev. 2:267-281.
47. Kitabayashi, I., R. Chiu, G. Gachelin, and K. Yokoyama. 1991. E1A dependent up-regulation of c-jun/AP-1 activity Nucleic Acids Res. 19:649-655
48. Kraus, V. B., E. Moran, and J. R. Nevins. 1992. Promoter-specific trans-activation by the adenovirus E1A 12S product involves separate E1A domains. Mol. Cell. Biol. 12:4391-4399.
49. Lee, K. A., and M. R. Green. 1987. A cellular transcription factor E4F1 interacts with an E1a-inducible enhancer and mediates constitutive enhancer function in vitro. EMBO J. 6:1345-1353.
50. Lee, K. A., T. Y. Hai, L. SivaRaman, B. Thimmappaya, H. C. Hurst, N. C. Jones, and M. R, Green. 1987. A cellular protein, activating transcription factor, activates transcription of multiple E1A-inducible adenovirus early promoters. Proc. Natl. Acad. Sci. USA 84:8355-8359.
51. Li, Y., C. Graham, L. S., A. M. 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 cyclins A and E. Genes Dev. 7:2366-2377.
52. Lillie, J. W., and M. R. Green. 1989. Transcription activation by the adenovirus E1a protein. Nature (London) 338:39-44.
53. Lin, Y. S., and M. R. Green. 1988. Interaction of a common cellular transcription factor, ATF, with regulatory elements in both E1a- and cyclic AMP-inducible promoters. Proc. Natl. Acad. Sci. USA 85:3396-3400.
54. 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.
55. Maguire, K., X. P. Shi, N. Horikoshi, J. Rappaport, M. Rosenberg, and R. Weinmann. 1991. Interactions between adenovirus E1A and members of the AP-1 family of cellular transcription factors. Onuogene 6:1417-1422.
56. Mayol, X., X. Grana, A. Baldi, N. Sang, Q. Hu, and A. Giordano. 1993 Cloning of a new member of the retmoblastoma gerte family (pRb2) which binds to the E1A transforming domain Oncogene 8:2561-2566.
57. Moran, E., and M. B. Mathews. 1987. Multiple functional domains in the adenovirus E1A gene. Cell 48:177-178.
58. Moran, E., B. Zerler, T. M. Harrison, and M. B. Mathews. 1986. Identification of separate domains in the adenovirus E1A gene for immortalization activity and the activation of virus early genes Mol. Cell. Biol. 6:3470-3480.
59. Muller, 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.
60. Monger, K., W. C. Phelps, V. Bubb, P. M. Howley, and R. Schlegel. 1989. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary1 human keratinocytes. J Virol. 63:4417-1421.
61. Monger. 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.
62. Mymryk, J. S., and S. T. Bayley. 1993. Multiple pathways for gene activation in rodent cells by the smaller adenovirus 5 E1A protein and their relevance to growth and transformation. J Gen. Virol. 74:2131-2141.
63. Mymryk, J. S., and S. T. Bayley. 1994. Multiple pathways for activation of E2A expression in human KB cells by the 243R E1A protein of adenovirus type 5. Virus Res. 33:89-97.
64. Nakshatri, H., M. M. Pater, and A. Pater. 1990. Ubiquitous and cell-type-specific protein interactions with human papillomavirus type 16 and type 18 enhancers. Virology 178:92-103.
65. Nevins, J. R. 1981. Mechanism of activation of early viral transcription by the adenovirus E1A gene product. Cell 26:213-220.
66. Nevins, J. R. 1982. Induction of the synthesis of a 70.000 dalton mammalian heat shock protein by the adenovirus E1A gene product. Cell 29:913-919.
67. Nevins, J. R. 1992. E2F: a link between the Rb tumor suppressor protein and viral oncoprotems. Science 258:424-429.
68. Offord, E. A., and P. Beard. 1990. A member of the activator protein 1 family found in keratinocytes but not in fibroblasts required for transcription from a human papillomavirus type 18 promoter. J. Virol. 64:4792-4798.
69. O'Neill, E. A., C. Fletcher, C. R. Burrow, N. Heintz, R. G. Roeder, and T. J. Kelly. 1988. Transcription factor OTF-1 is functionally identical to the DNA replication factor NF-III. Science 241:1210-1213.
70. Phelps, W., B. Srilata, J. Barnes, P. Raychudhuri, V. Kraus, K. Munger, P. Howley, and J. R. Nevins. 1991. Analysis of trans activation by human papillomavirus type 16 E7 and adenovirus 12S E1A suggests a common mechanism J. Virol. 65:6922-6930.
71. Phelps, W. C., C. L. Yee, K. Munger, and P. M. Howley. 1988. The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A. Cell 53:539-547.
72. Phelps, W. C., C. L. Yee, K. Munger, and P. M. Howley. 1989. Function 1 and sequence similarities between HPV16 E7 and adenovirus E1A. Curr Top. Microbiol. Immunol 144:153-166.
73. Reid, T. W., D. M. Albert, A. D. Rabson, P. Russell, J. Craft, E. W. Chu, T. S. Tralka, and J. L. Wilcox. 1974. Characterization of an established cell line of retinobiastoma. J. Natl. Cancer Inst. 53:347-360
74. Rikitake, Y., and E. Moran. 1992. DNA-binding properlies of the E1A-associated 300-kilodalton prolein. Mol. Cell. Biol. 12:2826-2836.
75. Rooney, R. J., P. Raychaudnuri, and J. R. Nevins. 1990. E4F and ATF, two transcription factors that recognize the same site, can be distinguished both physically and functionally: a role for E4F in E1A trans activation Mol Cell. Biol. 10:5138-5149.
76. 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
77. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
78. Schneider-Gadicke, A., and E. Schwarz. 1986. Different human cerncal carcinoma cell lines show similar transcription patterns of human papillomavirus type 18 early genes. EMBO J. 5:2285-2292.
79. Smith, D. H., and E. B. Ziff. 1988. The amino-terminal region of the adenovirus serotype 5 E1a protein performs two separate functions when expressed in primary baby rat kidney cells. Mol. Cell. Biol. 8:3882-3890
80. Smotkin, D., and F. O. Wettstein. 1986. Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein. Proc. Natl. Acad. Sci. USA 83:4680-4684.
81. Stein, R., and E. B. Ziff. 1984. HeLa cell β-tubuhn gene transcription is stimulated by adenovirus 5 in parallel with viral early genes by an E1a-dependent mechanism. Mol. Cell. Biol. 4:2792-2801.
82. van Dam, H., M. Duyndam, R. Rottier, A. Bosch, L. de Vries-Smits, P. Herrlich, A. Zantema, P. Angel, and A. J. van der Eb. 1993. Heterodimer formation of cJun and ATF-2 is responsible for induction of c-jun by the 243 amino acid adenovirus E1A protein. EMBO J. 12:479-487.
83. van Dam, H., R. Offringa, I. Meijer, B. Stein, A. M. Smits, P. Herrlich, J. L. Bos, and A. J. van der Eb. 1990. Differential effects of the adenovirui E1A oncogene on members of the AP-1 transcription factor family. Mol Cell. Biol. 10:5857-5864.
84. Velcich, A., and E. B. Ziff. 1985. Adenovirus E1A proteins repress transcription from the SV40 early promoter. Cell 40:705-716.
85. Vousden, K. H., and P. S. Jat 1989. Functional similarity between HPV16E7. SV40 large T and adenovirus E1a proteins. Oncogene 4:153-158.
86. Wang, H. G., Y. Rikitake, M. C. Carter, P. Yaciuk, S. E. Abraham, B. Zerler, and E. Moran. 1993. Identification of specific adenovirus E1A N-termmal residues critical to the binding of cellular proteins and to the control of cell growth. J. Virol. 67:476-488.
87. Weinberg, R. A. 1989. The molecular basis of retmoblastomas. Ciba Found. Symp. 142:99-111.
88. Weinberg, R, A. 1995. The retinobiastoma protein and cell cycle control Cell 81:323-330.
89. 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 retinobiastoma gene product. Nature (London) 334:124-129.
90. Whyte, P., H. E. Ruley, and E. Harlow. 1988. Two regions of the adenovrus early region 1A proteins are required for transformation. J. Virol. 62:251-265.
91. Whyte, P., N. M. Williamson, and E. Harlow. 1989. Cellular targets for transformation by the adenovirus E1A proteins. Cell 56:67-75.
92. Wong, H. K., and E. B. Ziff. 1994 Complementary functions of E1a conserved region 1 cooperate with conserved region 3 to activate adenovnus serotype 5 early promoters J Virol. 68:4910-4920
93. Yaciuk, P., and E. Moran. 1991. Analysis with specific polyclonal antiserum indicates that the E1A-associated 300-kilodalton product is a stable nuclear phosphoprotein that undergoes cell cycle phase-specific modification. Mol Cell. Biol. 11:5389-5397.
94. Ziff, E. B. 1990. Transcription factors: a new family gathers at the cAMP response site. Trends Genet. 6:69-72.
95. zur Hausen, H. 1991. Viruses in human cancer. Science 254:1167-1173