Cell cycle-regulated expression of mammalian CDC6 is dependent on E2F

Molecular and Cellular Biology

Volumn 18, Issue 11, 1998, Pages 6679-6697

  Hateboer, Guus ^a,b   Wobst, Albrecht ^a   Petersen, Birgit Otzen ^a   Le Cam, Laurent ^c   Vigo, Elena ^a   Sardet, Claude ^c   Helin, Kristian ^a  

^a EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^b CRUCELL HOLLAND BV   (Netherlands)

^c CENTRE NATIONAL DE RECHERCHES MÉTÉOROLOGIQUES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL GROWTH; DNA REPLICATION; DNA SYNTHESIS; GENE EXPRESSION; GENETIC REGULATION; GENETIC TRANSCRIPTION; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 0031796924     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.18.11.6679     Document Type: Article

References (84)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1988. Current protocols in molecular biology. Greene Publishing Associates & Wiley-Interscience, New York, N.Y.
2. Beijersbergen, R. L., and R. Bernards. 1996. Cell cycle regulation by the retinoblastoma family of growth inhibitory proteins. Biochim. Biophys. Acta 1287:103-120.
3. Beijersbergen, R. L., R. M. Kerkhoven, L. Zhu, L. Carlée, 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. Bell, S. P., J. Mitchell, J. Leber, R. Kobayashi, and B. Stillman. 1995. The multidomain structure of Orc1p reveals similarity to regulators of DNA replication and transcriptional silencing. Cell 83:563-568.
5. Bell, S. P., and B. Stillman. 1992. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357:128-134.
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. Botchan, M. 1996. Coordinating DNA replication DNA replication with cell division: current status of the licensing concept. Proc. Natl. Acad. Sci. USA 93:9997-10000.
9. Botz, J., K. Zerfass-Thome, D. Spitkovsky, H. Delius, B. Vogt, M. Eilers, A. Hatzigeorgiou, and P. Jansen-Dürr. 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.
10. Bremner, R., B. L. Cohen, M. Sopta, P. A. Hamel, C. J. Ingles, B. L. Gallie, and R. A. Phillips. 1995. Direct transcriptional repression by pRB and its reversal by specific cyclins. Mol. Cell. Biol. 15:3256-3265.
11. Cartwright, P., H. Müller, C. Wagener, K. Holm, and K. Helin. 1998. E2F-6: a novel member of the E2F family is an inhibitor of E2F-dependent transcription. Oncogene 17:611-624.
12. Cobrinik, D. 1996. Regulatory interactions among E2Fs and cell cycle control proteins. Curr. Top. Microbiol. Immunol. 208:31-60.
13. Cocker, J. H., S. Piatti, C. Santocanale, K. Nasmyth, and J. F. Diffley. 1996. An essential role for the Cdc6 protein in forming prereplicative complexes of budding yeast. Nature 379:180-182.
14. Dalton, S. 1992. Cell cycle regulation of the human cdc2 gene. EMBO J. 11:1797-1804.
15. 1/S-regulatory genes. Mol. Cell. Biol. 15:4215-4224.
16. Diffley, J. F. X. 1996. Once and only once upon a time: specifying and regulating origins of DNA replication in eukaryotic cells. Genes Dev. 10: 2819-2830.
17. Donovan, S., J. Harwood, L. S. Drury, and J. F. X. Diffley. 1997. Cdc6p-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast. Proc. Natl. Acad. Sci. USA 94:5611-5616.
18. Dou, Q.-P., P. J. Markell, and A. B. Pardee. 1992. Thymidine kinase transcription is regulated at G1/S phase by a complex that contains retinoblastoma-like protein and a cdc2 kinase. Proc. Natl. Acad. Sci. USA 89:3256-3260.
19. Drury, L. S., G. Perkins, and J. F. X. Diffley. 1997. The Cdc4/34/53 pathway targets Cdc6p for proteolysis in budding yeast. EMBO J. 16:5966-5976.
20. 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.
21. Gavin, K. A., M. Hidaka, and B. Stillman. 1995. Conserved initiator proteins in eukaryotes. Science 270:1667-1671.
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. Cu, 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. Graham, F. L., and A. J. Van der Eb. 1973. A new technique for the assay of infectivity of human adenovirus. Virology 52:456-467.
25. Grange, T., E. Bertrand, M. L. Espinas, M. Fromont-Racine, G. Rigaud, J. Roux, and R. Pictet. 1997. In vivo footprinting of the interaction of proteins with DNA and RNA. Methods 11:151-163.
26. Harlow, E., B. J. 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.
27. Helin, K. 1998. Regulation of cell proliferation by the E2F transcription factors. Curr. Opin. Genet. Dev. 8:28-35.
28. Helin, K., E. Harlow, and A. R. Fattaey. 1993. Inhibition of E2F-1 transactivation by direct binding of the retinoblastoma protein. Mol. Cell. Biol. 13:6501-6508.
29. 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.
30. 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 transactivation. Genes Dev. 7:1850-1861.
31. Hljmans, 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. Hinds, P. W., S. Mittnacht, V. Dulic, A. Arnold, S. I. Reed, and R. A. Weinberg. 1992. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell 70:993-1006.
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. Hu, Q., C. Bautista, G. Edwards, D. Defeo-Jones, R. Jones, and E. Harlow. 1991. Antibodies specific for the human retinoblastoma protein identify a family of related polypeptides. Mol. Cell. Biol. 11:5792-5799.
35. Huet, X., J. Rech, A. Plet, A. Vié, and J. M. Blanchard. 1996. Cyclin A expression is under negative transcriptional control during the cell cycle. Mol. Cell. Biol. 16:3789-3798.
36. Hurford, R. K. J., D. Cobrinik, M.-H. Lee and N. Dyson. 1997. pRB and p107/p130 are required for the regulated expression of different sets of E2F responsive genes. Genes Dev. 11:1447-1463.
37. Ikeda, M. A., L. Jakoi, and J. R. Nevins. 1996. A unique role for the Rb protein in controlling E2F accumulation during cell growth and differentiation. Proc. Natl. Acad. Sci. USA 93:3215-3220.
38. 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.
39. Karlseder, J., H. Rothender, and E. Wintersberger. 1996. Interaction of Sp1 with the growth-and cell cycle-regulated transcription factor E2F. Mol. Cell. Biol. 16:1659-1667.
40. Kelly, T. J., G. S. Martin, S. L. Forsburg, R. J. Stephen, A. Russo, and P. Nurse. 1993. The fission yeast cdc18+ gene product couples S phase to START and mitosis. Cell 74:371-382.
41. Koch, C., and K. Nasmyth. 1994. Cell cycle regulated transcription in yeast. Curr. Opin. Cell Biol. 6:451-459.
42. Kovesdi, I., R. Reichel, and J. R. Nevins. 1986. Identification of a cellular transcription factor involved in E1A trans-activation. Cell 45:219-228.
43. Krude, T., M. Jackman. J. Pines, and R. A. Laskey. 1997. Cyclin/Cdk-dependent initiation of DNA replication in a human cell-free system. Cell 88:109-119.
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., 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.
46. Lennon, G., C. Auffray, M. Polymeropoulos, and M. B. Soares. 1996. The I.M.A.G.E. consortium: an integrated molecular analysis of genomes and their expression. Genomics 33:151-152.
47. Liang, C., M. Weinreich, and B. Stillman. 1995. ORC and Cdc6p interact and determine the frequency of initiation of DNA replication in the genome. Cell 81:667-676.
48. Lindeman, G. J., S. Gaubatz, D. M. Livingston, and D. Ginsberg. 1997. The subcellular localization of E2F-4 is cell-cycle dependent. Proc. Natl. Acad. Sci. USA 94:5095-5100.
49. INK4A-mediated growth suppression. Mol. Cell. Biol. 16:1047-1057.
50. Means, A. L., J. E. Slansky, S. L. McMahon, M. W. Knuth, and P. J. Farnham. 1992. The HIP binding site is required for growth regulation of the dihydrofolate reductase promoter. Mol. Cell. Biol. 12:1054-1063.
51. 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.
52. Mueller, P. R., and B. Wold. 1989. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science 246:780-786.
53. Müller, H., M. C. Moroni, E. Vigo, B. O. Petersen, J. Bartek, and K. Helin. 1997. Induction of S-phase entry by E2F transcription factors depends on their nuclear localization. Mol. Cell. Biol. 17:5508-5520.
54. + regulates initiation of DNA replication in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 93:1666-1670.
55. Muzi-Falconi, M., G. W. Brown, and T. J. Kelly. 1996. DNA replication: controlling initiation during the cell cycle. Curr. Biol. 6:229-233.
56. 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. Mol. Cell. Biol. 14:6607-6615. (Author's correction, 15:4660, 1995.)
57. cdc18 plays a major role controlling the initiation of DNA replication in fission yeast. Cell 83:397-405.
58. 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.
59. 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.
60. 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.
61. Petersen, B. O., and K. Helin. Unpublished data.
62. Piatti, S., T. Böhm, J. H. Cocker, J. F. X. Diffley, and K. Nasmyth. 1996. Activation of S-phase-promoting CDKs in late G1 defines a "point of no return" after which Cdc6 synthesis cannot promote DNA replication in yeast. Genes Dev. 10:1516-1531.
63. Piatti, S., C. Lengauer, and K. Nasmyth. 1995. Cdc6 is an unstable protein whose de novo synthesis in G1 is important for the onset of S phase and for preventing a 'reductional' anaphase in the budding yeast Saccharomyces cerevisiae. EMBO J. 14:3788-3799.
64. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
65. Santocanale, C., and J. F. X. Diffley. 1996. ORC-and Cdc6-dependent complexes at active and inactive chromosomal replication origins in Saccharomyces cerevisiae. EMBO J. 15:6671-6679.
66. Sardet, C., M. Vidal, D. Cobrinik, Y. Geng, C. Onufryk, A. Chen, and R. A. Weinberg. 1995. E2F-4 and E2F-5, two members of the E2F family, are expressed in the early phases of the cell cycle. Proc. Natl. Acad. Sci. USA 92:2403-2407.
67. Schulze, A., K. Zerfass, D. Spitkovsky, S. Middendorp, J. Berges, K. Helin, P. Jansen-Dürr, 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.
68. Sears, R., K. Ohtani, and J. R. Nevins. 1997. Identification of positively and negatively acting elements regulating expression of the E2F2 gene in response to cell growth signals. Mol. Cell. Biol. 17:5227-5235.
69. Sellers, W. R., J. W. Rodgers, and W. G. Kaelin, Jr. 1995. A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. Proc. Natl. Acad. Sci. USA 92:11544-11548.
70. Sherr, C. J. 1996. Cancer cell cycles. Science 274:1672-1677.
71. Slansky, J., 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. Mol. Cell. Biol. 13:1610-1618.
72. 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.
73. Stillman, B. 1996. Cell cycle control of DNA replication. Science 274:1659-1664.
74. Tanaka, T., D. Knapp, and K. Nasmyth. 1997. Loading of an Mcm protein onto DNA replication origins is regulated by Cdc6p and CDKs. Cell 90:649-660.
75. Tommasi, S., and G. P. Pfeifer. 1995. In vivo structure of the human cdc2 promoter: release of a 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.
76. Vigo, E., and K. Helin. Unpublished data.
77. 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.
78. 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.
79. Williams, R. S., R. V. Shohet, and B. Stillman. 1997. A human protein related to yeast Cdc6p. Proc. Natl. Acad. Sci. USA 94:142-147.
80. KIP1 blocks cyclin E-dependent transactivation of cyclin A gene expression. Mol. Cell. Biol. 17:407-415.
81. 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.
82. 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.
83. Zwerschke, W., H. W. Rottjakob, and H. Küntzel. 1994. The Saccharomyces cerevisiae CDC6 gene is transcribed in late mitosis and encodes a ATP/ GTPase controlling S phase initiation. J. Biol. Chem. 269:23351-23356.
84. Zwicker, J., and R. Muller. 1997. Cell-cycle regulation of gene expression by transcriptional repression. Trends Genet. 13:3-6.