pRB and p107/p130 are required for the regulated expression of different sets of E2F responsive genes

Genes and Development

Volumn 11, Issue 11, 1997, Pages 1447-1463

  Hurford Jr , Robert K ^a   Cobrinik, David ^b   Lee, Myung Ho ^c   Dyson, Nicholas ^a  

^a MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^b New York Presbyterian Columbia University Medical Center   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell cycle regulation; E2F; p107; p130; pRB

Indexed keywords

RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2F;

ANIMAL CELL; ARTICLE; CELL CYCLE; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; GENE CONTROL; GENE EXPRESSION REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

ANIMALIA;

EID: 15444353328     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.11.11.1447     Document Type: Article

References (85)

1. Adams, P.D. and W.G. Kaelin Jr. 1996. The cellular effects of E2F overexpression. Curr. Top. Microbiol. Immunol. 208: 79-93.
2. Almasan, A., Y. Yin, R.E. Kelly, E.Y. Lee, A. Bradley, W. Li, J.R. Bertino, and G.M. Wahl. 1995. Deficiency of retinoblastoma protein leads to inappropriate S-phase entry, activation of E2F-responsive genes, and apoptosis. Proc. Natl. Acad. Sci. 92: 5436-5440.
3. 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.
4. Botz, J., K. Zerfass-Thome, D. Spitkovsky, H. Delius, B. Vogt, M. Eilers, A. Hatzigeorgiou, and P. Jansen-Durr. 1996. Cell cycle regulation of the murine cyclin E gene depends on an E2F binding site in the promoter. Mol. Cell. Biol. 16: 3401-3409.
5. 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 355: 176-179.
6. Chen, P.-C., D.J. Riley, and W.-H. Lee. 1995. The retinoblastoma protein as a fundamental mediator of growth and differentiation signals. Crit. Rev. Eukaryotic Gene Expression 5: 79-95.
7. Chittenden, T., D.M. Livingston, and J.A. DeCaprio. 1993. Cell cycle analysis of E2F in primary human T cells reveals novel E2F complexes and biochemically distinct forms of free E2F. Mol. Cell. Biol. 13: 3975-3983.
8. Clarke, A.R., E.R. Maandag, M. van Roon, N.M. van der Lugt, M. van der Valk, M.L. Hooper, A. Berns, and H. te Riele. 1992. Requirement for a functional Rb-1 gene in murine development. Nature 359: 328-330.
9. Cobrinik, D. 1996. Regulatory interactions among E2Fs and cell cycle control proteins. Curr. Top. Microbiol. Immunol. 208: 31-61.
10. 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.
11. Cobrinik, D., M.H. Lee, G. Hannon, G. Mulligan, R.T. Bronson, N. Dyson, E. Harlow, D. Beach, R.A. Weinberg, and T. Jacks. 1996. Shared role of the pRB-related p130 and p107 proteins in limb development. Genes & Dev. 10: 1633-1644.
12. Corbeil, H.B., P. Whyte, and P.E. Branton. 1995. Characterization of transcription factor E2F complexes during muscle and neuronal differentiation. Oncogene 11: 909-920.
13. Cress, W.D., D.G. Johnson, and J.R. Nevins. 1993. A genetic analysis of the E2F1 gene distinguishes regulation by Rb, p107, and adenovirus E4. Mol. Cell. Biol. 13: 6314-6325.
14. Dalton, S. 1992. Cell cycle regulation of the human cdc2 gene. EMBO J. 11: 1797-1804.
15. DeGregori, J., T. Kowalik, and J.R. Nevins. 1995. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis and G1/S regulatory genes. Mol. Cell. Biol. 15: 4215-4224.
16. Devoto, S.H., M. Mudryj, J. Pines, T. Hunter, and J.R. Nevins. 1992. A cyclin A-protein kinase complex possesses sequence-specific DNA binding activity: p33cdk2 is a component of the E2F-cyclin A complex. Cell 68: 167-176.
17. Dyson, N.J. 1991. Immobilization of nucleic acids and hybridization analysis. In Essential molecular biology: A practical approach (ed. T.A. Brown), pp. 111-156. IRL Press at Oxford University Press, Oxford, UK.
18. Dyson, N., M. Dembski, A. Fattaey, C. Ngwu, M. Ewen, and K. Helin. 1993. Analysis of p107-associated proteins: p107 associates with a form of E2F that differs from pRB-associated E2F-1. J. Virol. 67: 7641-7647.
19. Farnham, P.J. 1996. Transcriptional control of cell growth: The E2F family. Springer Verlag, New York, N.Y.
20. 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.
21. 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.
22. Gill, R.M., P.A. Hamel, J. Zhe, E. Zacksenhaus, B.L. Gallie, and R.A. Phillips. 1994. Characterization of the human RBl promoter and of elements involved in transcriptional regulation. Cell Growth Differ. 5: 467-474.
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. 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 RB1 by the product of the RB1 gene. Mol. Cell. Biol. 12: 3431-3438.
25. Harlow, E. 1996. A research shortcut from a common cold virus to human cancer. Cancer 78: 558-565.
26. Harlow, E. and D. Lane. 1988. Antibodies: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
27. Hateboer, G., R.M. Kerkhoven, A. Shvarts, R. Bernards, and R.L. Beijersbergen. 1996. Degradation of E2F by the ubiquitin-proteosome pathway: Regulation by retinoblastoma family proteins and adenovirus transforming proteins. Genes & Dev. 8 10: 2960-2970.
28. Herrera, R.E., V.P. Sah, B.O. Williams, T.P. Makela, R.A. Weinberg, and T. Jacks. 1996a. Altered cell cycle kinetics, gene expression, and G1 restriction point regulation in Rb-deficient fibroblasts. Mol. Cell. Biol. 16: 2402-2407.
29. Herrera, R.E., F. Chen, and R.A. Weinberg. 1996b. Increased histone H1 phosphorylation and relaxed chromatin structure in Rb-deficient fibroblasts. Proc. Natl. Acad. Sci 93: 11510-11515.
30. Hiebert, S.W., M. Lipp, and J.R. Nevins. 1989. E1A-dependent trans-activation of the human MYC promoter is mediated by the E2F factor. Proc. Natl. Acad. Sci. 86: 3594-3598.
31. 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.
32. Hofmann, F., F. Martelli, D.M. Livingston, and Z. Wang. 1996. The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway. Genes & Dev. 10: 2949-2959.
33. 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.
34. Huet, X., J. Rech, A. Plet, A. Vie, and J.M. Blanchard. 1996. Cyclin A expression is under negative transcriptional control during the cell cycle. Mol. Cell. Biol. 16: 3789-3798.
35. Jacks, T., A. Fazeli, E.M. Schmitt, R.T. Bronson, M.A. Goodell, and R.A. Weinberg. 1992. Effects of an Rb mutation in the mouse. Nature 359: 295-300.
36. 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 365: 349-352.
37. 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.
38. Johnson, L.F. 1992. G1 events and the regulation of genes for S-phase enzymes. Curr. Opin. Cell. Biol. 4: 149-154.
39. 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.
40. Kim, K.K., M.H. Soonpaa, H. Wang, and L.J. Field. 1995. Developmental expression of p107 mRNA and evidence for alternative splicing of the p107 (RBL1) gene product. Genomics 28: 520-529.
41. Laborda, J. 1991. 36B4 cDNA used as an estradiol-independent mRNA control is the cDNA for human acidic ribosumal phosphoprotein PO. Nucleic Acids Res. 19: 3998.
42. Lam, E.W. and R.J. Watson. 1993. An E2F-binding site mediates cell-cycle regulated repression of mouse B-myb transcription. EMBO J. 12: 2705-2713.
43. Lam, E.W., J.D. Morris, R. Davies, T. Crook, R.J. Watson, and K.H. Vousden. 1994. HPV16 E7 oncoprotein deregulates B-myb expression: correlation with targeting of p107/E2F complexes. EMBO J. 13: 871-878.
44. Lee, E.Y., C.Y. Chang, N. Hu, Y.C. Wang, C.C. Lai, K. Herrup, W.H. Lee, and A. Bradley. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359: 288-294.
45. Lee, E.Y.-H.P., N. Hu, S.-S.F. Yuan, L. Cox, A. Bradley, W.-H. Lee and K. Herrup. 1994. Dual roles of the retinoblastoma proteins in cell cycle regulation and neuron differentiation. Genes & Dev. 8: 2008-2021.
46. Lee, H.H., W.H. Chiang, S.H. Chiang, Y.C. Liu, J. Hwang, and S.Y. Ng. 1995. Regulation of cyclin D1, DNA topoisomerase I, and proliferating cell nuclear antigen promoters during the cell cycle. Gene Expr. 4: 95-109.
47. Lee, M.H., B.O. Williams, G. Mulligan, S. Mukai, R.T. Bronson, N. Dyson, E. Harlow, and T. Jacks. 1996. Targeted disruption of p107: Functional overlap between p107 and Rb. Genes & Dev. 10: 1621-1632.
48. Lees, J.A., M. Saito, M. Vidal, M. Valentine, T. Look, E. Harlow, N. Dyson, and K. Helin. 1993. The retinoblastoma protein binds to a family of E2F transcription factors. Mol. Cell. Biol. 13: 7813-7825.
49. Lukas, J., J. Bartkova, M. Rohde, M. Strauss, and J. Bartek. 1995. Cyclin D1 is dispensable for G1 control in retinoblastoma gene-deficient cells independently of cdk4 activity. Mol. Cell. Biol. 15: 2600-2611.
50. Lukas, J., B.O. Petersen, K. Holm, J. Bartek, and K. Helin. 1996. Deregulated expression of E2F family members induces S-phase entry and overcomes p16INK4A-mediated growth suppression. Mol. Cell. Biol. 16: 1047-1057.
51. Means, A.L., J.E. Slansky, S.L. McMahon, M.W. Knuth, and P.J. Farnham. 1992. The HIP1 binding site is required for growth regulation of the dihydrofolate reductase gene promoter. Mol. Cell. Biol. 12: 1054-1063.
52. 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.
53. Neuman, E., E.K. Flemington, W.R. Sellers, and W.G. Kaelin, Jr. 1994. Transcription of the E2F-1 gene is rendered cell cycle dependent by E2F DNA-binding sites within its promoter [published erratum appears in Mol. Cell. Biol. 1995. 15: 4660].
54. Ogris, E., H. Rotheneder, I. Mudrak, A. Pichler, and E. Wintersberger. 1993. A binding site for transcription factor E2F is a target for trans activation of murine thymidine kinase by polyomavirus large T antigen and plays an important role in growth regulation of the gene. J. Virol. 67: 1765-1771.
55. Ohtani, K., J. DeGregori, and J.R. Nevins. 1995. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. 92: 12146-12150.
56. Ohtani-Fujita, N., T. Fujita, R. Takahashi, P.D. Robbins, and T.P. Dryja. 1994. A silencer element in the retinoblastoma tumor-suppressor gene. Oncogene 9: 1703-1711.
57. Ohtsubo, M. and J.M. Roberts. 1993. Cyclin-dependent regulation of G1 in mammalian fibroblasts. Science 259: 1908-1912.
58. Pearson, B.E., H.P. Nasheuer, and T.S. Wang. 1991. Human DNA polymerase alpha gene: sequences controlling expression in cycling and serum-stimulated cells. Mol. Cell. Biol. 11: 2081-2095.
59. Porcu, P., X. Grana, S. Li, J. Swantek, A. De Luca, A. Giordano, and R. Baserga. 1994. An E2F binding sequence negatively regulates the response of the insulin-like growth factor 1 (IGF-I) promoter to simian virus 40T antigen and to serum. Oncogene 9: 2125-2134.
60. Philipp, A., A. Schneider, I. Vasrik, K. Finke, Y. Xiong, D. Beach, K. Alitalo, and M. Eilers. 1994. Repression of cyclin D1: A novel function of MYC. Mol. Cell. Biol. 14: 4032-4043.
61. Qian, Y., C. Luckey, L. Horton, M. Esser, and D.J. Templeton. 1992. Biological function of the retinoblastoma protein requires distinct domains for hyperphosphorylation and transcription factor binding. Mol. Cell. Biol. 12: 5363-5372.
62. Resnitzky, D., M. Gossen, H. Bujard, and S.I. Reed. 1994. Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol. 14: 1669-1679.
63. Sanchez, I. and B.D6. Dynlacht. 1996. Transcriptional control of the cell cycle. Curr. Opin. Cell Biol. 8: 318-324.
64. -/- muscle cells. Science 264: 1467-1471.
65. 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. 92: 11264-11268.
66. Schulze, A., K. Zerfass-Thome, J. Berges, S. Middendorp, P. Jansen-Durr, and B. Henglein. 1996. Anchorage-dependent transcription of the cyclin A gene. Mol. Cell. Biol. 16: 4632-4638.
67. 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.
68. Shan, B., C.Y. Chang, D. Jones, and W.H. Lee. 1994. The transcription factor E2F-1 mediates the autoregulation of RB gene expression. Mol. Cell. Biol. 14: 299-309.
69. Sherr, C.J. 1996. Cancer cell cycles. Science 274: 1672-1677.
70. Shirodkar, S., M. Ewen, J.A. DeCaprio, J. Morgan, D.M. Living-ston, and T. Chittenden. 1992. The transcription factor E2F interacts with the retinoblastoma product and a p107-cyclin A complex in a cell cycle-regulated manner. Cell 68: 157-166.
71. Slansky, J.E. and P.J. Farnham. 1996. Introduction to the E2F family: Protein structure and gene regulation. Curr. Top. Microbiol. Immunol. 208: 1-30.
72. Slansky, J.E., Y. Li, W.G. Kaelin, and P.J. Farnham. 1993. A protein synthesis-dependent increase in E2F1 mRNA correlates with growth regulation of the dihydrofolate reductase promoter [published erratum appears in Mol. Cell. Biol. 1993. 13:7201].
73. Smith, E.J., G. Leone, J. DeGregori, L. Jakoi, and J.R. Nevins. 1996. The accumulation of an E2F-p130 transcriptional repressor distinguishes a G0 cell state from a G1 phase state. Mol. Cell. Biol. 16: 6965-6976.
74. Tabor, S. and K. Struhl. 1994. DNA-dependent DNA polymerases. In Current protocols in molecular biology (ed. F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl), pp. 3.5.1-3.5.15. Wiley/Greene, New York, NY.
75. Thalmeier, K., H. Synovzik, R. Mertz, E.L. Winnacker, and M. Lipp. 1989. Nuclear factor E2F mediates basic transcription and trans-activation by E1a of the human MYC promoter. Genes & Dev. 3: 527-536.
76. Tommasi, S. and G.P. Pfeifer. 1995. In vivo structure of the human cdc2 promoter: Release of a p130-E2F6-4 complex from sequences immediately upstream of the transcription initiation site coincides with induction of cdc2 expression. Mol. Cell. Biol. 15: 6901-6913.
77. Weinberg, R.A. 1995. The retinoblastoma protein and cell cycle control. Cell 81: 323-330.
78. Weintraub, S.J., C.A. Prater, and D.C. Dean. 1992. Retinoblastoma protein switches the E2F site from positive to negative element. Nature 358: 259-261.
79. Weintraub, S.J., K.M. Chow, R.X. Luo, S.H. Zhang, S. He, and D.C. Dean. 1995. Mechanism of active transcriptional repression by the retinoblastoma protein. Nature 375: 812-815.
80. Welch, P.J. and J.Y. Wang. 1995. Disruption of retinoblastoma protein function by coexpression of its C pocket fragment. Genes & Dev. 9: 31-46.
81. Wimmel, A., F.C. Lucibello, A. Sewing, S. Adolph, and R. Muller. 1994. Inducible acceleration of G1 progression through tetracycline-regulated expression of human cyclin E. Oncogene 9: 995-997.
82. Yee, A.S., R. Reichel, I. Kovesdi, and J.R. Nevins. 1987. Promoter interaction of the E1A-inducible factor E2F and its potential role in the formation of a multi-component complex. EMBO J. 6: 2061-2068.
83. Zhu, L., S. van den Heuvel, K. Helin, A. Fattaey, M. Ewen, D. 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., L. Zhu, 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., C. Gross, F.C. Lucibello, M. Truss, K. Engeland and R. Muller. 1996. Cell cycle regulation of the cyclin A, cdc25C and cdc2 genes is based on a common mechanism of transcriptional repression. EMBO J. 14: 4514-4522.