E2F7 represses a network of oscillating cell cycle genes to control S-phase progression

Nucleic Acids Research

Volumn 40, Issue 8, 2012, Pages 3511-3523

  Westendorp, Bart ^a   Mokry, Michal ^b   Groot Koerkamp, Marian J A ^b   Holstege, Frank C P ^b   Cuppen, Edwin ^b   De Bruin, Alain ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; CELL CYCLE PROTEIN 6; CELL PROTEIN; CHECKPOINT KINASE 1; DNA; MINICHROMOSOME MAINTENANCE PROTEIN 2; POLO LIKE KINASE 1; PROTEIN CCNB1; PROTEIN ECT2; RAD51 PROTEIN; REPLICATION LICENSING FACTOR CDT1; TRANSCRIPTION FACTOR E2F7; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE GENE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CHROMATIN IMMUNOPRECIPITATION; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA DAMAGE; DNA METABOLISM; DNA REPAIR; DNA REPLICATION; GENE; GENE ACTIVATION; GENE MAPPING; GENE REPRESSION; GENE TARGETING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN MOTIF; S PHASE CELL CYCLE CHECKPOINT; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; BINDING SITES; CONSENSUS SEQUENCE; DNA DAMAGE; E2F7 TRANSCRIPTION FACTOR; G1 PHASE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENES, CDC; MICE; PERIODICITY; REPRESSOR PROTEINS; S PHASE; S PHASE CELL CYCLE CHECKPOINTS; TRANSCRIPTION, GENETIC;

EID: 84860363212     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1203     Document Type: Article

References (48)

1. Reichel, R., Kovesdi, I. and Nevins, J.R. (1987) Developmental control of a promoter-specific factor that is also regulated by the E1A gene product. Cell, 48, 501-506.
2. Van Den Heuvel, S. and Dyson, N.J. (2008) Conserved functions of the pRB and E2F families. Nat. Rev. Mol. Cell Biol., 9, 713-724.
3. Attwooll, C., Lazzerini Denchi, E. and Helin, K. (2004) The E2F family: specific functions and overlapping interests. EMBO J., 23, 4709-4716.
4. Dimova, D.K. and Dyson, N.J. (2005) The E2F transcriptional network: old acquaintances with new faces. Oncogene, 24, 2810-2826.
5. Chen, H.Z., Tsai, S.Y. and Leone, G. (2009) Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat. Rev. Cancer., 9, 785-797.
6. De Bruin, A., Maiti, B., Jakoi, L., Timmers, C., Buerki, R. and Leone, G. (2003) Identification and characterization of E2F7, a novel mammalian E2F family member capable of blocking cellular proliferation. J. Biol. Chem., 278, 42041-42049.
7. Di Stefano, L., Jensen, M.R. and Helin, K. (2003) E2F7, a novel E2F featuring DP-independent repression of a subset of E2F-regulated genes. EMBO J., 22, 6289-6298.
8. Logan, N., Delavaine, L., Graham, A., Reilly, C., Wilson, J., Brummelkamp, T.R., Hijmans, E.M., Bernards, R. and La Thangue, N.B. (2004) E2F-7: a distinctive E2F family member with an unusual organization of DNA-binding domains. Oncogene, 23, 5138-5150.
9. Logan, N., Graham, A., Zhao, X., Fisher, R., Maiti, B., Leone, G. and La Thangue, N.B. (2005) E2F-8: an E2F family member with a similar organization of DNA-binding domains to E2F-7. Oncogene, 24, 5000-5004.
10. Christensen, J., Cloos, P., Toftegaard, U., Klinkenberg, D., Bracken, A.P., Trinh, E., Heeran, M., Di Stefano, L. and Helin, K. (2005) Characterization of E2F8, a novel E2F-like cell-cycle regulated repressor of E2F-activated transcription. Nucleic Acids Res., 33, 5458-5470.
11. Maiti, B., Li, J., De Bruin, A., Gordon, F., Timmers, C., Opavsky, R., Patil, K., Tuttle, J., Cleghorn, W. and Leone, G. (2005) Cloning and characterization of mouse E2F8, a novel mammalian E2F family member capable of blocking cellular proliferation. J. Biol. Chem., 280, 18211-18220.
12. Ishida, S., Huang, E., Zuzan, H., Spang, R., Leone, G., West, M. and Nevins, J.R. (2001) Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol. Cell. Biol., 21, 4684-4699.
13. Ren, B., Cam, H., Takahashi, Y., Volkert, T., Terragni, J., Young, R.A. and Dynlacht, B.D. (2002) E2F integrates cell cycle progression with DNA repair, replication, and G(2)/M checkpoints. Genes Dev., 16, 245-256.
14. Zhu, W., Giangrande, P.H. and Nevins, J.R. (2004) E2Fs link the control of G1/S and G2/M transcription. EMBO J., 23, 4615-4626.
15. Polager, S., Kalma, Y., Berkovich, E. and Ginsberg, D. (2002) E2Fs up-regulate expression of genes involved in DNA replication, DNA repair and mitosis. Oncogene, 21, 437-446.
16. Xu, X.Q., Bieda, M., Jin, V.X., Rabinovich, A., Oberley, M.J., Green, R. and Farnham, P.J. (2007) A comprehensive chip-chip analysis of E2F1, E2F4, and E2F6 in normal and tumor cells reveals interchangeable roles of E2F family members. Genome Res., 17, 1550-1561.
17. Cao, A.R., Rabinovich, R., Xu, M., Xu, X., Jin, V.X. and Farnham, P.J. (2011) Genome-wide analysis of transcription factor E2F1 mutant proteins reveals that N-and C-terminal protein interaction domains do not participate in targeting E2F1 to the human genome. J. Biol. Chem., 286, 11985-11996.
18. Lee, B.K., Bhinge, A.A. and Iyer, V.R. (2011) Wide-ranging functions of E2F4 in transcriptional activation and repression revealed by genome-wide analysis. Nucleic Acids Res., 39, 3558-3573.
19. Rabinovich, A., Jin, V.X., Rabinovich, R., Xu, X. and Farnham, P.J. (2008) E2F in vivo binding specificity: Comparison of consensus versus nonconsensus binding sites. Genome Res., 18, 1763-1777.
20. Li, J., Ran, C., Li, E., Gordon, F., Comstock, G., Siddiqui, H., Cleghorn, W., Chen, H.Z., Kornacker, K., Liu, C.G. et al. (2008) Synergistic function of E2F7 and E2F8 is essential for cell survival and embryonic development. Dev. Cell, 14, 62-75.
21. Zalmas, L.P., Zhao, X., Graham, A.L., Fisher, R., Reilly, C., Coutts, A.S. and La Thangue, N.B. (2008) DNA-damage response control of E2F7 and E2F8. EMBO Rep., 9, 252-259.
22. Sharma, N., Timmers, C., Trikha, P., Saavedra, H.I., Obery, A. and Leone, G. (2006) Control of the P53-P21(CIP1) axis by E2f1, E2f2, and E2f3 is essential for G(1)/S progression and cellular transformation. J. Biol. Chem., 281, 36124-36131.
23. Wu, L., Timmers, C., Maiti, B., Saavedra, H.I., Sang, L., Chong, G.T., Nuckolls, F., Giangrande, P., Wright, F.A., Field, S.J. et al. (2001) The E2F1-3 transcription factors are essential for cellular proliferation. Nature, 414, 457-462.
24. Macphail, S.H., Banath, J.P., Yu, Y., Chu, E. and Olive, P.L. (2003) Cell cycle-dependent expression of phosphorylated histone H2AX: reduced expression in unirradiated but not X-irradiated G1-phase cells. Radiat. Res., 159, 759-767.
25. Van Dijk-Ottens, M., Vos, I.H., Cornelissen, P.W., De Bruin, A. and Everts, M.E. (2010) Thyroid hormone-induced cardiac mechano growth factor expression depends on beating activity. Endocrinology, 151, 830-838.
26. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol., 3, RESEARCH0034.
27. Roepman, P., Wessels, L.F., Kettelarij, N., Kemmeren, P., Miles, A.J., Lijnzaad, P., Tilanus, M.G., Koole, R., Hordijk, G.J., Van Der Vliet, P.C. et al. (2005) An expression profile for diagnosis of lymph node metastases from primary head and neck squamous cell carcinomas. Nat. Genet., 37, 182-186.
28. Yang, Y.H., Dudoit, S., Luu, P., Lin, D.M., Peng, V., Ngai, J. and Speed, T.P. (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res., 30, E15.
29. Thomas, P.D., Campbell, M.J., Kejariwal, A., Mi, H.Y., Karlak, B., Daverman, R., Diemer, K., Muruganujan, A. and Narechania, A. (2003) PANTHER: a library of protein families and subfamilies indexed by function. Genome Res., 13, 2129-2141.
30. Thomas, P.D., Kejariwal, A., Guo, N., Mi, H., Campbell, M.J., Muruganujan, A. and Lazareva-Ulitsky, B. (2006) Applications for protein sequence-function evolution data: MRNA/protein expression analysis and coding SNP scoring tools. Nucleic Acids Res., 34, W645-W650.
31. Huang Da, W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
32. Mokry, M., Hatzis, P., De Bruijn, E., Koster, J., Versteeg, R., Schuijers, J., Van De Wetering, M., Guryev, V., Clevers, H. and Cuppen, E. (2010) Efficient double fragmentation Chip-Seq provides nucleotide resolution protein-DNA binding profiles. PLos One, 5, E15092.
33. Li, H. and Durbin, R. (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics, 25, 1754-1760.
34. Ji, H., Jiang, H., Ma, W., Johnson, D.S., Myers, R.M. and Wong, W.H. (2008) An integrated software system for analyzing Chip-Chip and Chip-Seq data. Nat. Biotechnol., 26, 1293-1300.
35. Zhou, Q. and Wong, W.H. (2004) Cismodule: de novo discovery of cis-regulatory modules by hierarchical mixture modeling. Proc. Natl Acad. Sci. USA, 101, 12114-12119.
36. Merdzhanova, G., Edmond, V., De Seranno, S., Van Den Broeck, A., Corcos, L., Brambilla, C., Brambilla, E., Gazzeri, S. and Eymin, B. (2008) E2F1 controls alternative splicing pattern of genes involved in apoptosis through upregulation of the splicing factor SC35. Cell Death Differ., 15, 1815-1823.
37. Uchiumi, T., Longo, D.L. and Ferris, D.K. (1997) Cell cycle regulation of the human polo-like kinase (PLK) promoter. J. Biol. Chem., 272, 9166-9174.
38. Whitfield, M.L., Sherlock, G., Saldanha, A.J., Murray, J.I., Ball, C.A., Alexander, K.E., Matese, J.C., Perou, C.M., Hurt, M.M., Brown, P.O. et al. (2002) Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol. Biol. Cell, 13, 1977-2000.
39. Saito, S., Tatsumoto, T., Lorenzi, M.V., Chedid, M., Kapoor, V., Sakata, H., Rubin, J. and Miki, T. (2003) Rho exchange factor ECT2 is induced by growth factors and regulates cytokinesis through the N-terminal cell cycle regulator-related domains. J. Cell. Biochem., 90, 819-836.
40. De Feraudy, S., Revet, I., Bezrookove, V., Feeney, L. and Cleaver, J.E. (2010) A minority of foci or pan-nuclear apoptotic staining of gammah2ax in the s phase after UV damage contain DNA double-strand breaks. Proc. Natl Acad. Sci. USA, 107, 6870-6875.
41. Tao, Y., Kassatly, R.F., Cress, W.D. and Horowitz, J.M. (1997) Subunit composition determines E2F DNA-binding site specificity. Mol. Cell. Biol., 17, 6994-7007.
42. Bar-Joseph, Z., Siegfried, Z., Brandeis, M., Brors, B., Lu, Y., Eils, R., Dynlacht, B.D. and Simon, I. (2008) Genome-wide transcriptional analysis of the human cell cycle identifies genes differentially regulated in normal and cancer cells. Proc. Natl Acad. Sci. USA, 105, 955-960.
43. Mirzaei, H., Syed, S., Kennedy, J. and Schmidt, K.H. (2011) Sgs1 truncations induce genome rearrangements but suppress detrimental effects of BLM overexpression in Saccharomyces cerevisiae. J. Mol. Biol., 405, 877-891.
44. Richardson, C., Stark, J.M., Ommundsen, M. and Jasin, M. (2004) Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability. Oncogene, 23, 546-553.
45. Al-Ejeh, F., Kumar, R., Wiegmans, A., Lakhani, S.R., Brown, M.P. and Khanna, K.K. (2010) Harnessing the complexity of DNA-damage response pathways to improve cancer treatment outcomes. Oncogene, 29, 6085-6098.
46. Ciccia, A. and Elledge, S.J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell, 40, 179-204.
47. Wu, L., De Bruin, A., Saavedra, H.I., Starovic, M., Trimboli, A., Yang, Y., Opavska, J., Wilson, P., Thompson, J.C., Ostrowski, M.C. et al. (2003) Extra-embryonic function of Rb is essential for embryonic development and viability. Nature, 421, 942-947.
48. De Bruin, A., Wu, L., Saavedra, H.I., Wilson, P., Yang, Y., Rosol, T.J., Weinstein, M., Robinson, M.L. and Leone, G. (2003) Rb function in extraembryonic lineages suppresses apoptosis in the CNS of Rb-deficient mice. Proc. Natl Acad. Sci. USA, 100, 6546-6551.