The forkhead transcription factor FOXM1 controls cell cycle-dependent gene expression through an atypical chromatin binding mechanism

Molecular and Cellular Biology

Volumn 33, Issue 2, 2013, Pages 227-236

  Chen, Xi ^a   Müller, Gerd A ^b   Quaas, Marianne ^b   Fischer, Martin ^b   Han, Namshik ^a   Stutchbury, Benjamin ^a   Sharrocks, Andrew D ^a   Engeland, Kurt ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; CCNB1 PROTEIN; FZR1 PROTEIN; POLO LIKE KINASE 1; PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXM1; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL STRAIN HEK293; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL CYCLE; CELL DIVISION; CELL LINE, TUMOR; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; DNA-BINDING PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GENES, CDC; HCT116 CELLS; HEK293 CELLS; HUMANS; MICE; MITOSIS; NIH 3T3 CELLS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84871881824     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00881-12     Document Type: Article

References (37)

1. Carlsson P, Mahlapuu M. 2002. Forkhead transcription factors: key players in development and metabolism. Dev. Biol. 250:1-23.
2. Hannenhalli S, Kaestner KH. 2009. The evolution of Fox genes and their role in development and disease. Nat. Rev. Genet. 10:233-240.
3. Breeden LL. 2000. Cyclin transcription: timing is everything. Curr. Biol.10:R586 -R588.
4. Alvarez B, Martinez AC, Burgering BM, Carrera AC. 2001. Forkhead transcription factors contribute to execution of the mitotic programme in mammals. Nature 413:744 -747.
5. Laoukili J, Kooistra MR, Bras A, Kauw J, Kerkhoven RM, Morrison A,Clevers H, Medema RH. 2005. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat. Cell Biol. 7:126 -136.
6. Wang IC, Chen YJ, Hughes D, Petrovic V, Major ML, Park HJ, Tan Y,Ackerson T, Costa RH. 2005. Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol. Cell. Biol. 25:10875-10894.
7. Darieva Z, Bulmer R, Pic-Taylor A, Doris KS, Geymonat M, Sedgwick SG, Morgan BA, Sharrocks AD. 2006. Polo kinase controls cell-cycledependent transcription by targeting a coactivator protein. Nature 444:494-498.
8. Fu Z, Malureanu L, Huang J, Wang W, Li H, van Deursen JM, Tindal DJ, Chen J. 2008. Plk1-dependent phosphorylation of FoxM1 regulates a transcriptional programme required for mitotic progression. Nat. Cell Biol. 10:1076 -1082.
9. Muller GA, Engeland K. 2010. The central role of CDE/CHR promoter elements in the regulation of cell cycle-dependent gene transcription.FEBS J. 277:877- 893.
10. Muller GA, Quaas M, Schumann M, Krause E, Padi M, Fischer M,Litovchick L, DeCaprio JA, Engeland K. 2012. The CHR promoter element controls cell cycle-dependent gene transcription and binds the DREAM and MMB complexes. Nucleic Acids Res. 40:1561-1578.
11. Litovchick L, Sadasivam S, Florens L, Zhu X, Swanson SK, Velmurugan S, Chen R, Washburn MP, Liu XS, DeCaprio JA. 2007. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell 26:539 -551.
12. Schmit F, Cremer S, Gaubatz S. 2009. LIN54 is an essential core subunit of the DREAM/LINC complex that binds to the cdc2 promoter in a sequence-specific manner. FEBS J. 276:5703-5716.
13. Wasner M, Tschop K, Spiesbach K, Haugwitz U, Johne C, Mossner J, Mantovani R, Engeland K. 2003. Cyclin B1 transcription is enhanced by the p300 coactivator and regulated during the cell cycle by a CHRdependent repression mechanism. FEBS Lett. 536:66 -70.
14. O'Donnell A, Yang SH, Sharrocks AD. 2008. MAP kinase-mediated c-fos regulation relies on a histone acetylation relay switch. Mol. Cell 29:780-785.
15. Tavner F, Frampton J, Watson RJ. 2007. Targeting an E2F site in the mouse genome prevents promoter silencing in quiescent and post-mitotic cells. Oncogene 26:2727-2735.
16. Marais A, Ji Z, Child ES, Krause E, Mann DJ, Sharrocks AD. 2010. Cell cycle-dependent regulation of the forkhead transcription factor FOXK2 by CDK-cyclin complexes. J. Biol. Chem. 285:35728 -35739.
17. Shore P, Sharrocks AD. 1994. The transcription factors Elk-1 and serum response factor interact by direct protein-protein contacts mediated by a short region of Elk-1. Mol. Cell. Biol. 14:3283-3291.
18. Lee TI, Johnstone SE, Young RA. 2006. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc.1:729 -748.
19. Boros J, Donaldson IJ, O'Donnell A, Odrowaz ZA, Zeef L, Lupien M,Meyer CA, Liu XS, Brown M, Sharrocks AD. 2009. Elucidation of the ELK1 target gene network reveals a role in the coordinate regulation of core components of the gene regulation machinery. Genome Res. 19:1963-1973.
20. Schmidt D, Wilson MD, Spyrou C, Brown GD, Hadfield J, Odom DT.2009. ChIP-seq: using high-throughput sequencing to discover protein-DNA interactions. Methods 48:240 -248.
21. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nussbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9:R137.
22. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX,Murre C, Singh H, Glass CK. 2010. Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38:576 -589.
23. Shin H, Liu T, Manrai AK, Liu XS. 2009. CEAS: cis-regulatory element annotation system. Bioinformatics 25:2605-2606.
24. Ye T, Krebs AR, Choukrallah MA, Keime C, Plewniak F, Davidson I, Tora L. 2011. seqMINER: an integrated ChIP-seq data interpretation platform. Nucleic Acids Res. 39:e35.
25. Sadasivam S, Duan S, DeCaprio JA. 2012. The MuvB complex sequentially recruits B-Myb and FoxM1 to promote mitotic gene expression. Genes Dev. 26:474-489.
26. Ji Z, Donaldson IJ, Liu J, Hayes A, Zeef LA, Sharrocks AD. 2012. The forkhead transcription factor FOXK2 promotes AP-1-mediated transcriptional regulation. Mol. Cell. Biol. 32:385-398.
27. Skaar JR, Pagano M. 2009. Control of cell growth by the SCF and APC/C ubiquitin ligases. Curr. Opin. Cell Biol. 21:816-824.
28. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB,Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28:495-501.
29. Pierrou S, Hellqvist M, Samuelsson L, Enerback S, Carlsson P. 1994. Cloning and characterization of seven human forkhead proteins: binding site specificity and DNA bending. EMBO J. 13:5002-5012.
30. Katoh H, Qin ZS, Liu R, Wang L, Li W, Li X, Wu L, Du Z, Lyons R, Liu CG, Liu X, Dou Y, Zheng P, Liu Y. 2011. FOXP3 orchestrates H4K16 acetylation and H3K4 trimethylation for activation of multiple genes by recruiting MOF and causing displacement of PLU-1. Mol. Cell 44:770-784.
31. Motallebipour M, Ameur A, Reddy Bysani MS, Patra K, Wallerman O, Mangion J, Barker MA, McKernan KJ, Komorowski J, Wadelius C. 2009. Differential binding and co-binding pattern of FOXA1 and FOXA3 and their relation to H3K4me3 in HepG2 cells revealed by ChIP-seq. Genome Biol. 10:R129.
32. Wallerman O, Motallebipour M, Enroth S, Patra K, Bysani MS, Komorowski J, Wadelius C. 2009. Molecular interactions between HNF4a, FOXA2 and GABP identified at regulatory DNA elements through ChIP-sequencing. Nucleic Acids Res. 37:7498 -7508.
33. Littler DR, Alvarez-Fernandez M, Stein A, Hibbert RG, Heidebrecht T, Aloy P, Medema RH, Perrakis A. 2010. Structure of the FoxM1 DNArecognition domain bound to a promoter sequence. Nucleic Acids Res.38:4527- 4538.
34. Down CF, Millour J, Lam EW, Watson RJ. 2012. Binding of FoxM1 to G2/M gene promoters is dependent upon B-Myb. Biochim. Biophys. Acta 1819:855- 862.
35. Laoukili J, Alvarez M, Meijer LA, Stahl M, Mohammed S, Kleij L, Heck AJ, Medema RH. 2008. Activation of FoxM1 during G2 requires cyclin A/Cdk-dependent relief of autorepression by the FoxM1 N-terminal domain. Mol. Cell. Biol. 28:3076 -3087.
36. Schmit F, Korenjak M, Mannefeld M, Schmitt K, Franke C, von Eyss B, Gagrica S, Hanel F, Brehm A, Gaubatz S. 2007. LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 6:1903-1913.
37. Major ML, Lepe R, Costa RH. 2004. Forkhead box M1B transcriptional activity requires binding of Cdk-cyclin complexes for phosphorylationdependent recruitment of p300/CBP coactivators. Mol. Cell. Biol. 24:2649-2661