Adenovirus E1A downregulates cJun- and JunB-mediated transcription by targeting their coactivator p300

Molecular and Cellular Biology

Volumn 16, Issue 8, 1996, Pages 4312-4326

  Lee, Jeng Shin ^a,b   See, Raymond H ^a   Deng, Tiliang ^c   Shi, Yang ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN; TRANSCRIPTION FACTOR; VIRUS PROTEIN;

ADENOVIRUS; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; ONCOGENE C JUN; PRIORITY JOURNAL; PROTEIN ISOLATION; REPRESSOR GENE; TRANSCRIPTION REGULATION; VIRUS MUTATION; VIRUS TRANSCRIPTION;

EID: 0029953720     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.8.4312     Document Type: Article

References (71)

1. Angel, P., K. Hattori, T. Smeal, and M. Karin. 1988. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell 55:875-885.
2. Angel, P., and M. Karin. 1991. The role of Jun, Fos and the AP-1 complex in cell proliferation and transformation. Biochim. Biophys. Acta 1072:129-157.
3. Arany, Z., D. Newsome, E. Oldread, D. M. Livingston, and R. Eckner. 1995. A family of transcriptional adaptor proteins targeted by the E1A oncoprotein. Nature (London) 374:81-84.
4. Arany, Z., W. R. Sellers, D. M. Livingston, and R. Eckner. 1994. E1A-associated p300 and CREB-associated CBP belong to a conserved family of coactivators. Cell 77:799-800.
5. Arias, J., A. S. Alberts, P. Brindle, F. X. Claret, T. Smeal, M. Karin, J. Feramisco, and M. Montminy. 1994. Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature (London) 370: 226-229.
6. 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.
7. Baichwal, V. R., A. Park, and R. Tjian. 1992. The cell-type-specific activator region of c-Jun juxtaposes constitutive and negatively regulated domains. Genes Dev. 6:1493-1502.
8. Baichwal, V. R., and R. Tjian. 1990. Control of c-Jun activity by interaction of a cell-specific inhibitor with regulatory domain δ: difference between v-and c-Jun. Cell 63:815-825.
9. 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.
10. Bannister, A. J., and T. Kouzarides. 1995. CBP-induced stimulation of c-Fos activity is abrogated by E1A. EMBO J. 14:4758-4762.
11. Bannister, A. J., T. Oehler, D. Wilhelm, P. Angel, and T. Kouzarides. 1995. Stimulation of c-Jun activity by CBP: c-Jun residues Ser 63/73 are required for CBP induced stimulation in vivo and CBP binding in vitro. Oncogene 11:2509-2514.
12. Bohmann, D., T. J. Bos, A. Admon, T. Nishimura, P. K. Vogt, and R. Tjian. 1987. Human proto-oncogene cjun encodes a DNA binding protein with structural and functional properties of transcription factor AP-1. Science 238:1386-1392.
13. Chatterjee, P. K., M. Bruner, S. J. Flint, and M. L. Harter. 1988. DNA-binding properties of an adenovirus 289R E1A protein. EMBO J. 7:835-841.
14. Chellappan, S., S. Hiebert, M. Mudryj, J. M. Horowitz, and J. R. Nevins. 1991. The E2F transcription factor is a cellular target for the RB protein. Cell 65:1053-1061.
15. Chrivia, J. C., R. P. S. Kwok, N. Lamb, M. Hagiwara, M. R. Montimy, and R. H. Goodman. 1993. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature (London) 265:855-859.
16. Cohen, D. R., P. C. P. Ferreira, R. Gentz, B. R. Franza, and T. Curran. 1989. The product of a fos related gene. fra-1, binds cooperatively to the AP-1 site with Jun: transcription factor AP-1 is comprised of multiple protein complexes. Genes Dev. 3:173-184.
17. Dai, P., H. Akimaru, Y. Tanaka, D.-X. Hou, T. Yasukawa, C. Kanei-Ishii, T. Takahashi, and S. Ishii. 1996. CBP as a transcriptional coactivator of c-Myb. Genes Dev. 10:528-540.
18. de Groot, R., N. Foulkes, M. Mulder, W. Kruijer, and P. Sassone-Corsi, 1991. Positive regulation of jun/AP-1 by E1A. Mol. Cell. Biol. 11:192-201.
19. Deng, T., and M. Karin. 1992. Construction and expression of a monomeric c-Jun protein that binds and activates transcription of AP-1-responsive genes. Proc. Natl. Acad. Sci. USA 89:8572-8576.
20. Dorsman, J. C., B. M. Hagmeyer, J. Veenstra, P. Elfferich, N. Nabben, A. Zantema, and A. J. van der Eb. 1995. The N-terminal region of the adenovirus type 5 E1A proteins can repress expression of cellular genes via two distinct but overlapping domains. J. Virol. 69:2962-2967.
21. Dyson, N., and E. Harlow. 1992. Adenovirus E1A targets key regulators for cell proliferation. Cancer Surv. 12:161-195.
22. 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.
23. 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.
24. 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.
25. Ferguson, B., B. Krippl, O. Andrisani, N. Jones, H. Westphal, and M. Rosenberg. 1985. E1A 13S and 12S mRNA products made in Escherichia coli both function as nucleus-localized transcription activators but do not directly bind DNA. Mol. Cell. Biol. 5:2653-2661.
26. Franza, B. R., Jr., F. J. Rauscher III, S. F. Josephs, and T. Curran. 1988. The fos complex and fos-related antigens recognize sequence elements that contain AP-1 binding sites. Science 239:1150-1153.
27. Frisch, S. M., R. Reich, I. E. Collier, L. T. Genrich, G. Martin, and G. I. Goldberg. 1990. Adenovirus E1A represses protease gene expression and inhibits metastasis of human tumor cells. Oncogene 5:75-83.
28. Hagmeyer, R. M., H. Konig, 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.
29. Hai, T., and T. Curran. 1991. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc. Natl. Acad. Sci. USA 88:3720-3724.
30. Hai, T., F. Liu, E. A. Allegretto, M. Karin, and M. R. Green. 1988. A family of immunologically related transcription factors that includes multiple forms of ATF and AP-1. Genes Dev. 2:1216-1226.
31. Hamel, P. A., R. M. Gill, R. A. Phillips, and B. L. Gallie. 1992. Transcriptional repression of the E2-containing promoters EIIaE, c-myc, and KB1 by the product of the RB1 gene. Mol. Cell. Biol. 12:3431-3438.
32. 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.
33. Hiebert, S. W., S. P. Chellappan, J. M. Horowitz, and J. R. Nevins. 1992. The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev. 6:177-185.
34. Hofmann, M., W. Rudy, U. Gunthert, S. G. Zimmer, V. Zawadzki, M. Zoller, R. B. Lichtner, P. Herrlich, and H. Ponta. 1993. A link between ras and metastatic behavior of tumor cells: ras induces CD44 promoter activity and leads to low-level expression of metastatic-specific variants of CD44 in CREF cells. Cancer Res. 53:1516-1521.
35. Horikoshi, N., K. Maguire, A. Krelli, E. Maldanado, D. Reinberg, and R. Weinmann. 1991. Direct interaction between adenovirus E1A protein and the TATA box binding transcription factor IID. Proc. Natl. Acad. Sci. USA 88:5124-5128.
36. Houweling, A., P. J. van der Elsen, and A. J. van der Eb. 1980. Partial transformation of primary rat cells by the leftmost 4.5% fragment of adenovirus 5 DNA. Virology 105:537-550.
37. Howe, J. A., J. S. Mymryk, C. Egan, P. E. Branton, and S. T. Bayley. 1990. Retinoblastoma growth suppressor and a 300-kDa protein appear to regulate cellular DNA synthesis. Proc. Natl. Acad. Sci. USA 87:5883-5887.
38. Hsin-Fang, Y.-Y., R. Chiu, and M. Karin. 1990. Elevation of AP1 activity during F9 cell differentiation is due to increased c-jun transcription. New Biol. 2:351-361.
39. Jelsma, T. N., J. A. Howe, J. S. Mymryk, C. M. Evelegh, N. F. Cunnif, and S. T. Bayley. 1989. Sequences in E1A 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.
40. Kitabayashi, I., R. Chiu, G. Gachelin, and K. Yokoyama. 1991. E1A dependent up-regulation of cJun/AP-1 activity. Nucleic Acids Res. 12:479-487.
41. Kwok, R. P. S., J. R. Lundblad, J. C. Chrivia, J. P. Richards, H. P. Bachinger, R. G. Brennan, S. G. E. Roberts, M. R. Green, and R. H. Goodman. 1994. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature (London) 370:223-226.
42. Lee, J.-S., X. Zhang, and Y. Shi. Differential interactions of the CREB/ ATF family of transcription factors with p300 and adenovirus E1A. J. Biol. Chem., in press.
43. Lee, J.-S., K. M. Galvin, R. H. See, R. Eckner, D. Livingston, E. Moran, and Y. Shi. 1995. Relief of YY1 transcriptional repression by adenovirus E1A is mediated by E1A-associated protein p300. Genes Dev. 9:1188-1198.
44. Lee, J.-S., K. M. Galvin, and Y. Shi. 1993. Evidence for physical interaction between the zinc finger transcription factors YY1 and Sp1. Proc. Natl. Acad. Sci. USA 90:6145-6149.
45. Lee, J.-S., R. H. See, K. M. Galvin, J. Wang, and Y. Shi. 1995. Functional interactions between YY1 and adenovirus E1A. Nucleic Acids Res. 23:925-931.
46. Lee, W. S., C. 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.
47. 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.
48. 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.
49. 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.
50. Nakabeppu, Y., K. Ryder, and D. Nathans. 1988. DNA binding activities of three murine jun proteins: stimulation by fos. Cell 55:907-915.
51. Nevins, J. R. 1992. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science 258:424-429.
52. Offringa, R., S. Gebel, H. van Dam, M. Timmers, A. Smits, R. Zwart, B. Stein, J. L. Bos, A. van der Eb, and P. Herrlich. 1990. A novel function of the transforming domain of E1A: repression of AP-1 activity. Cell 62:527-538.
53. Offringa, R., A. M. M. Smits, A. Houweling, J. L. Bos, and A. J. van der Eb. 1988. Similar effects of adenovirus E1A and glucocorticoid hormones on the expression of the metalloprotease stromelysin. Nucleic Acids Res. 16:10973-10984.
54. Pugh, B. F., and R. Tjian. 1990. Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell 61:1187-1197.
55. Rauscher, F. J., III, L. C. Sambucetti, T. Curran, R. J. Distel, and B. Spiegelman. 1988. A common DNA binding site for fos protein complexes and transcription factor AP-1. Cell 52:471-480.
56. Rauscher, F. J., III, P. J. Voulalas, B. R. Franza, and T. Curran. 1988. Fos and jun bind cooperatively to the AP-1 site: reconstitution in vitro. Genes Dev. 2:1687-1699.
57. 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.
58. Schutte, J., J. Viakket, M. Nau, S. Segal, J. Fedorko, and J. Minna. 1989. jun-B inhibits and c-fos stimulates the transforming and trans-activating activities of c-jun. Cell 59:987-997.
59. Shi, Y., E. Seto, L. S. Chang, and T. Shenk. 1991. Transcriptional repression by YY1, a human GLI-Kruppel related protein, and relief of repression by adenovirus E1A protein. Cell 67:377-388.
60. 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 adenovirus E1A oncogene on members of the AP-1 transcription factor family. Mol. Cell. Biol. 10:5857-5864.
61. van Dam, H., R. Offringa, A. M. Smits, J. L. Bos, N. C. Jones, and A. van der Eb. 1989. The expression of the growth factor-inducible genes JE, c-myc and stromelysin by adenovirus E1A is mediated by conserved region 1. Oncogene 4:1207-1212.
62. van der Eb, A. J., H. van Ormondt, and P. I. Schrier. 1979. Structure and function of the transforming genes of human adenoviruses and SV40. Cold Spring Harbor Symp. Quant. Biol. 44:383-399.
63. van der Elsen, P., S. de Parter, A. Houweling, J. van der Veer, and A. J. van der Eb. 1982. The relationship between regions E1a and E1b of human adenoviruses in cell transformation. Gene 18:175-185.
64. van der Elsen, P. J., A. Houweling, and A. J. van der Eb. 1983. Morphological transformation of human adenoviruses is determined to a large extent by gene products of region E1a. Virology 131:242-246.
65. Vogt, P. K., and T. J. Bos. 1990. Jun: oncogene and transcription factor. Adv. Cancer Res. 55:1-35.
66. 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.
67. Weintraub, S. J., C. A. Prater, and D. C. Dean. 1992. Retinoblastoma protein switches the E2F site from positive to negative element. Nature (London) 358:259-261.
68. Whyte, P., N. M. Williamson, and E. Harlow. 1989. Cellular targets for transformation by the adenovirus E1A proteins. Cell 56:67-75.
69. 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.
70. Zamanian, M., and N. B. LaThangue. 1992. Adenovirus E1a prevents the retinoblastoma gene product from repressing the activity of a cellular transcription factor. EMBO J. 11:2603-2610.
71. Zerial, M., L. Toschi, R. P. Ryseck, M. Schuermann, R. Mueller, and R. Bravo. 1989. The product of a novel growth factor activated gene, fosB, interacts with JUN proteins enhancing their DNA binding activity. EMBO J. 8:805-813.