Subunit composition determines E2F DNA-binding site specificity

Molecular and Cellular Biology

Volumn 17, Issue 12, 1997, Pages 6994-7007

  Tao, Yunxia ^a   Kassatly, Robert F ^b   Cress, W Douglas ^b   Horowitz, Jonathan M ^a,c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BACULOVIRUS; BINDING SITE; CELL CYCLE; CELL PROLIFERATION; DNA BINDING; GENE EXPRESSION; IMMUNOPRECIPITATION; MONKEY; MULTIGENE FAMILY; NONHUMAN; OSTEOSARCOMA; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; RETINOBLASTOMA; SMALL CELL CARCINOMA;

ANIMALIA; MAMMALIA; PAPILLOMAVIRUS; UNIDENTIFIED BACULOVIRUS; VERTEBRATA;

EID: 0030688065     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.12.6994     Document Type: Article

References (85)

1. Adnane, J., Z. Shao, and P. D. Robbins. 1995. The retinoblastoma susceptibility gene product represses transcription when directly bound to the promoter. J. Biol. Chem. 270:8837-8843.
2. Bagchi, S., P. Raychaudhuri, and J. R. Nevins. 1990. Adenovirus E1A can dissociate heteromeric complexes involving the E2F transcription factor: A novel mechanism for E1A trans-activation. Cell 62:659-669.
3. Bandara, L. R., V. M. Buck. M. Zamanian, L. H. Johnston, and N. B. La Thangue. 1993. Functional synergy between DP-1 and E2F-1 in the cell cycle-regulating transcription factor DRTF1/E2F. EMBO J. 12:4317-4324.
4. 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.
5. Beijersbergen, R. L., R. M. Kerkhoven, L. Zhu, L. Carlee, P. M. Voorhoeve, and R. Bernards. 1994. E2F-4, a new member of the E2F gene family, has oncogenic activity and associates with p107 in vivo. Genes Dev. 8:2680-2690.
6. Bennett, J. D., P. G. Farlie, and R. J. Watson. 1996. E2F binding is required but not sufficient for repression of B-myb transcription in quiescent fibroblasts. Oncogene 13:1073-1082.
7. Blake, M. C., and J. C. Azizkhan. 1989. Transcription factor E2F is required for efficient expression of the hamster dihydrofolate reductase gene in vitro and in vivo. Mol. Cell. Biol. 9:4994-5002.
8. Buchkovich, K., L. A. Duffy, and E. Harlow. 1989. The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell 58:1097-1105.
9. Cao, 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.
10. Chellappan, S. P., 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.
11. Chen, P.-L., P. Scully, J.-Y. Shew;, J. Y. J. Wang, and W.-H. Lee. 1989. Phosphorylation of the retinoblastoma gene product is modified during the cell cycle and cellular differentiation. Cell 58:1193-1198.
12. Chittenden, T., D. M. Livingston, and W. G. J. Kaelin. 1991. The T/E1A-binding domain of the retinoblastoma product can interact selectively with a sequence-specific DNA-binding protein. Cell 65:1073-1082.
13. Claudio, P. P., C. M. Howard, A. Baldi, A. De Luca, Y. Fu, G. Condorelli, Y. Sun, N. Colburn, B. Calabretta, and A. Giordano. 1994. p130/pRb2 has growth suppressive properties similar to yet distinctive from those of retinoblastoma family members pRb and p107. Cancer Res. 54:5556-5560.
14. 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.
15. Cress, W. D., and J. R. Nevins. 1994. Interacting domains of E2F1, DP1, and the adenovirus E4 protein. J. Virol. 68:4213-4219.
16. Cress, W. D., and J. R. Nevins. 1996. A role for a bent DNA structure in E2F-medialcd transcription activation. Mol. Cell. Biol. 16:2119-2127.
17. 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 54:275-282.
18. 1/S-regulatory genes. Mol. Cell. Biol. 15:4215-4224.
19. 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.
20. Field, S. J., F.-Y. Tsai, F. Kuo, A. M. Zubiaga, W. G. Kaelin, Jr., D. M. Livingston, S. H. Orkin, and M. E. Greenberg. 1996. E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell 85:549-561.
21. Fry, C. J., J. E. Slansky, and P. J. Farnham. 1997. Position-dependent transcriptional regulation of the murine dihydrofolate reductase promoter by the E2F transactivation domain. Mol. Cell. Biol. 17:1966-1976.
22. Geng, Y., E. N. Eaton, M. Picon, J. M. Roberts. A. S. Lundberg, A. Gifford, C. Sardet, and R. A. Weinberg. 1996. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene 12:1173-1180.
23. Ginsberg, D., G. Vairo, T. Chittenden, Z.-X. Xiao, G. Xu, K. L. Wydner, J. A. DeCaprio, J. B. Lawrence, and D. M. Livingston. 1994. E2F-4, a new member of the E2F transcription factor family, interacts with p107. Genes Dev. 8:2665-2679.
24. Helin, K., J. A. Lees, M. Vidal, N. Dyson, E. Harlow, and A. Fattaey. 1992. A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell 70:337-350.
25. Helin, K., C.-L. Wu, A. R. Fattaey, J. A. Lees, B. D. Dynlacht, C. Ngwu, and E. Harlow. 1993. Heterodimerization of the transcription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev. 7:1850-1861.
26. Hijmans, E. M., P. M. Voorhoeve, R. L. Beijersbergen, L. J. van 't Veer, and R. Bernards. 1995. E2F-5, a new E2F family member that interacts with p130 in vivo. Mol. Cell. Biol. 15:3082-3089.
27. Horowitz, J. M., and A. J. Udvadia. 1995. Regulation of transcription by the retinoblastoma (Rb) protein. Mol. Cell. Differ. 3:275-314.
28. Horowitz, J. M., D. W. Yandell, S.-H. Park, S. Canning, P. Whyte, K. J. Buchkovich, E. Harlow, R. A. Weinberg, and T. P. Dryja. 1989. Point mutational inactivation of the retinoblastoma antioncogene. Science 243:937-940.
29. Hsiao, K.-M., S. L. McMahon, and P. J. Farnham. 1994. Multiple DNA elements are required for the growth regulation of the mouse E2F1 promoter. Genes Dev. 8:1526-1537.
30. Hu, Q., N. Dyson, and E. Harlow. 1990. The regions of the retinoblastoma protein needed for binding to adenovirus E1A or SV40 large T antigen are common sites for mutations. EMBO J. 9:1147-1155.
31. Huber, H. E., P. J. Goodhart, and P. S. Huang. 1994. Retinoblastoma protein reverses DNA bending by transcription factor E2F. J. Biol. Chem. 269:6999-7005.
32. Johnson, D. G., K. Ohtani, and J. R. Nevins. 1994. Autoregulatory control of E2F1 expression in response to positive and negative regulators of cell cycle progression. Genes Dev. 8:1514-1525.
33. Kaelin, W. G., Jr., W. Krek, W. R. Sellers, J. A. DeCaprio, F. Ajchenbaum, C. S. Fuchs, T. Chittenden, Y. Li, P. J. Farnham, M. A. Blanar, D. M. Livingston, and E. K. Flemington. 1992. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell 70:351-364.
34. Karlseder, J., H. Rotheneder, and E. Wintersberger. 1996. Interaction of Sp1 with the growth- and cell cycle-regulated transcription factor E2F. Mol. Cell. Biol. 16:1659-1667.
35. Kerppola, T. K., and T. Curran. 1991. DNA bending by Fos and Jun: the flexible hinge model. Science 254:1210-1214.
36. Kerppola, T. K., and T. Curran. 1991. Fos-Jun heterodimers and Jun homodimers bend DNA in opposite orientations: implications for transcription factor cooperativity. Cell 66:317-326.
37. Kim, J., C. Zwieb, C. Wu, and S. Adhya. 1989. Bending of DNA hy gene-regulatory proteins: construction and use of a DNA bending vector. Gene 85:15-23.
38. Kim, S.-J., U. S. Onwuta, Y. I. Lee, R. Li, M. R. Botchan, and P. D. Robbins. 1992. The retinoblastoma gene product regulates Sp1-mediated transcription. Mol. Cell. Biol. 12:2455-2463.
39. Knudson, A. G. J. 1993. Antioncogenes and human cancer. Proc. Natl. Acad. Sci. USA 90:10914-10921.
40. Koo, H., H. Wu, and D. M. Crothers. 1986. DNA bending at adenine-thymine tracts. Nature (London) 320:501-506.
41. Kovesdi, I., R. Reichel, and J. R. Nevins. 1986. Identification of a cellular transcription factor involved in E1A trans-activation. Cell 45:219-228.
42. Krek, W., D. M. Livingston, and S. Shirodkar. 1993. Binding to DNA and the retinoblastoma gene product promoted by complex formation of different E2F family members. Science 262:1557-1560.
43. Lam, E. W.-F., and N. B. La Thangue. 1995. DP and E2F proteins: coordinating transcription with cell cycle progression. Curr. Opin. Cell Biol. 6:859-866.
44. Lam, E. W.-F., and R. J. Watson. 1993. An E2F-binding site mediates cell-cycle regulated repression of mouse B-myb transcription. EMBO J. 12:2705-2713.
45. Lees, J. A., K. J. Buchkovich, D. R. Marshals, C. W. Anderson, and E. Harlow. 1991. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. EMBO J. 10:4279-4290.
46. Lin, S.-Y., A. Rhys Black, D. Kostic, S. Pajovic, C. N. Hoover, and J. C. Azizkhan. 1996. Cell cycle-regulated association of E2F1 and Sp1 is related to their functional interaction. Mol. Cell. Biol. 16:1668-1675.
47. Ludlow, J. W., J. Shon, J. M. Pipas, D. M. Livingston, and J. A. DeCaprio. 1990. The retinoblastoma susceptibility gene product undergoes cell cycle-dependent dephosphorylation and binding to and release from SV40 large T. Cell 60:387-396.
48. Magae, J., C.-L. Wu, S. Illenye, E. Harlow, and N. H. Heintz. 1996. Nuclear localization of DP and E2F transcription factors by heterodimeric partners and retinoblastoma protein family members. J. Cell. Sci. 109:1717-1726.
49. Mihara, K., X.-R. Cao, A. Yen, S. Chandler, B. Driscoli, A. L. Murphree, A. T'Ang, and Y.-K. T. Fung. 1989. Cell cycle-dependent regulation of phosphorylation of the human retinoblastoma gene product. Science 246:1300-1303.
50. Moberg, K., M. A. Starz, and J. A. Lees. 1996. E2F-4 switches from p130 to p107 and pRB in response to cell cycle reentry. Mol. Cell. Biol. 16:1436-1449.
51. Nevins, J. R. 1992. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science 258:424-429.
52. Ohtani, K., J. DeGregori, G. Leone, D. R. Herendeen, T. J. Kelly, and J. R. Nevins. 1996. Expression of the HsOrc1 gene, a human ORC1 homolog, is regulated by cell proliferation via the E2F transcription factor. Mol. Cell. Biol. 16:6977-6984.
53. Ohtani, K., J. DeGregori, and J. R. Nevins. 1995. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. USA 92:12146-12150.
54. Ormondroyd, E., S. de la Luna, and N. B. La Thangue. 1995. A new member of the DP family, DP-3, with distinct protein products suggests a regulatory role for alternative splicing in the cell cycle transcription factor DRTF1/E2F. Oncogene 11:1437-1446.
55. Ouellette, M. M., J. Chen, W. E. Wright, and J. W. Shay. 1992. Complexes containing the retinoblastoma gene product recognize different DNA motifs related to the E2F binding site. Oncogene 7:1075-1081.
56. Reichel, R., I. Kovesdi, and J. R. Nevins. 1988. Activation of a preexisting cellular factor as a basis for adenovirus E1A-mediated transcription control. Proc. Natl. Acad. Sci. USA 85:387-390.
57. Rogers, K. T., P. D. R. Higgins, M. M. Milla, R. S. Phillips, and J. M. Horowitz. 1995. DP-2, a heterodimeric partner of E2F: identification and characterization of DP-2 proteins expressed in vivo. Proc. Natl. Acad. Sci. USA 93:7594-7599.
58. Schulze, A., K. Zerfass, D. Spitkovsky, S. Middendorp, J. Berges, K. Helin, P. Jansen-Durr, and B. Henglein. 1995. Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site. Proc. Natl. Acad. Sci. USA 92:11264-11268.
59. Schwarz, J. K., S. H. Devoto, E. J. Smith, S. P. Chellappan, L. Jakoi, and J. R. Nevins. 1993. Interactions of the p107 and Rb proteins with E2F during the cell proliferation response. EMBO J. 12:1013-1020.
60. Sellers, W. R., J. W. Rodgers, and W. G. J. Kaelin. 1995. A potent transrepression domain in the retinoblasloma protein induces a cell cycle arrest when bound to E2F sites. Proc. Natl. Acad. Sci. USA 92:11544-11548.
61. Shan, B., X. Zhu, P. Chen, T. Durfee, Y. Yang, D. Sharp, and W. Lee. 1992. Molecular cloning of cellular genes encoding retinoblastoma-associated proteins: identification of a gene with properties of the transcription factor E2F. Mol. Cell. Biol. 12:5620-5631.
62. Shirodkar, S., M. Ewen, J. A. DeCaprio, J. Morgan, D. M. Livingston, and T. Chittenden. 1992. The transcription factor E2F interacts with the retinoblastoma product and p107-cyclin A complex in a cell cycle-regulated manner. Cell 68:157-166.
63. Slansky, J. E., and P. J. Farnham. 1996. Introduction to the E2F family: protein structure and gene regulation, p. 1-30. In P. J. Farnham (ed.), Transcriptional control of cell growth: the E2F gene family. Springer-Verlag, New York, N.Y.
64. Sterner, J. M., Y. Murata, H. G. Kim, S. B. Kennet, D. J. Templeton, and J. M. Horowitz. 1995. Characterization of cellular proteins that form complexes with the amino-terminus of the retinoblastoma (Rb) protein: a novel cell-cycle regulated kinase associates with Rb in G2/M phases. J. Biol. Chem. 270:9281-9288.
65. Strauss, J. K., and L. J. I. Maher. 1994. DNA bending by asymmetric phosphate neutralization. Nature (London) 266:1829-1834.
66. Tao, Y., and J. M. Horowitz. Unpublished observations.
67. Taya, Y., H. Yasuda, M. Kamijo, K. Nakaya, Y. Nakamura, Y. Ohba, and S. Nishimura. 1989. In vitro phosphorylation of the tumor suppressor gene RB protein by mitosis-specific histone H1 kinase. Biochem. Biophys. Res. Commun. 164:580-586.
68. Thompson, J. F., and A. Landy. 1988. Empirical estimation of protein-induced DNA bending angles: application to lambda site-specific recombination complexes. Nucleic Acids Res. 16:9687-9705.
69. Tommasi, S., and G. P. Pfeifer. 1995. In vivo structure of the human cdc2 promoter: release of p130-E2F-4 complex from sequences immediately upstream of the transcription initiation site coincides with induction of cdc2 expression. Mol. Cell. Biol. 15:6901-6913.
70. Udvadia, A. J., K. T. Rogers, P. D. R. Higgins, Y. Murata, K. H. Martin, P. A. Humphrey, and J. M. Horowitz. 1993. Sp-1 binds promoter elements regu-lated by the Rb protein and Sp-1-mediatcd transcription is stimulated by Rb co-expression. Proc. Natl. Acad. Sci. USA 90:3265-3269.
71. Vairo, G., D. M. Livingston, and D. Ginsberg. 1995. Functional interaction between E2F-4 and p130: evidence for distinct mechanisms underlying growth suppression by different retinoblastoma protein family members. Genes Dev. 9:869-881.
72. Wade, M., M. C. Blake, R. C. Jambou, K. Helin, E. Harlow, and J. C. Azizkhan. 1995. An inverted repeat motif stabilizes binding of E2F and enhances transcription of the dihydrofolate reductase gene. J. Biol. Chem. 270:9783-9791.
73. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
74. Weinberg, R. A. 1996. E2F and cell proliferation: a world turned upside down. Cell 85:457-459.
75. Weintraub, S. J., K. N. B. Chow, R. X. Luo, S. H. Zhang, S. He, and D. C. Dean. 1995. Mechanism of active transcriptional repression by the retinoblastoma protein. Nature (London) 375:812-815.
76. 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.
77. Wells, J., P. Held, S. Illenye, and N. H. Heintz. 1996. Protein-DNA interactions at the major and minor promoters of the divergently transcribed dhfr and rep3 genes during the Chinese hamster ovary cell cycle. Mol. Cell. Biol. 16:634-647.
78. Wells, J., S. Illenye, C.-L. Wu, and N. H. Heintz. 1997. Accumulation of E2F-4/DP-1 DNA binding complexes correlates with induction of dhfr gene expression during G1 to S phase transition. J. Biol. Chem. 272:4483-4492.
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 susceptibility gene product. Nature (London) 334:124-129.
80. Yamasaki, L., T. Jacks, R. Bronson, E. Goillot. E. Harlow, and N. J. Dyson. 1996. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell 85: 537-548.
81. Yee, A. S., P. Raychaudhuri, L. Jakoi, and J. R. Nevins. 1989. The adenovirus-inducible factor E2F stimulates transcription after specific DNA binding. Mol. Cell. Biol. 9:578-585.
82. Zamanian, M., and N. B. La Thangue. 1993. Transcriptional repression by the Rb-relaled protein p107. Mol. Biol. Cell 4:389-396.
83. Zhu, L., S. van den Heuvel, K. Helin, A. Fattaey, M. Ewen, D. M. Livingston, N. Dyson, and E. Harlow. 1993. Inhibition of cell proliferation by p107, a relative of the retinoblastoma protein. Genes Dev. 7:1111-1125.
84. Zhu, L., E. Xie, and L.-S. Chang. 1995. Differential roles of two tandem E2F sites in repression of the human p107 promoter by retinoblastoma and p107 proteins. Mol. Cell. Biol. 15:3552-3562.
85. Zwicker, J., N. Liu, K. Engeland, F. C. Lucibello, and R. Muller. 1996. Cell cycle regulation of E2F site occupation in vivo. Science 271-1595-1597.