Binding of FoxM1 to G2/M gene promoters is dependent upon B-Myb

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1819, Issue 8, 2012, Pages 855-862

  Down, Christin F ^a   Millour, Julie ^a   Lam, Eric W F ^a   Watson, Roger J ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

B Myb (MybL2); Cell cycle; FoxM1; Mitosis; Pioneer transcription factor

Indexed keywords

CRE RECOMBINASE; CYCLIN A2; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; FOCAL ADHESION KINASE; LUCIFERASE; MESSENGER RNA; POLO LIKE KINASE 1; SURVIVIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXM1; TRANSCRIPTION FACTOR MYBL2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE INACTIVATION; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION;

3T3 CELLS; ANIMALS; BINDING SITES; CELL CYCLE PROTEINS; CYCLIN-DEPENDENT KINASES; FORKHEAD TRANSCRIPTION FACTORS; G2 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION; MICE; MICE, KNOCKOUT; MITOSIS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84861944935     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.03.008     Document Type: Article

References (40)

1. Whitfield M.L., George L.K., Grant G.D., Perou C.M. Common markers of proliferation. Nat. Rev. Cancer 2006, 6:99-106.
2. Laoukili J., Kooistra M.R., Bras A., Kauw J., Kerkhoven R.M., Morrison A., Clevers H., Medema R.H. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat. Cell Biol. 2005, 7:126-136.
3. Osterloh L., von Eyss B., Schmit F., Rein L., Hubner D., Samans B., Hauser S., Gaubatz S. The human synMuv-like protein LIN-9 is required for transcription of G2/M genes and for entry into mitosis. EMBO J. 2007, 26:144-157.
4. Thorner A.R., Hoadley K.A., Parker J.S., Winkel S., Millikan R.C., Perou C.M. In vitro and in vivo analysis of B-Myb in basal-like breast cancer. Oncogene 2009, 28:742-751.
5. Knight A.S., Notaridou M., Watson R.J. A Lin-9 complex is recruited by B-Myb to activate transcription of G2/M genes in undifferentiated embryonal carcinoma cells. Oncogene 2009, 28:1737-1747.
6. Tanaka Y., Patestos N.P., Maekawa T., Ishii S. B-myb is required for inner cell mass formation at an early stage of development. J. Biol. Chem. 1999, 274:28067-28070.
7. Garcia P., Frampton J. The transcription factor B-Myb is essential for S-phase progression and genomic stability in diploid and polyploid megakaryocytes. J. Cell Sci. 2006, 119:1483-1493.
8. Tarasov K.V., Tarasova Y.S., Tam W.L., Riordon D.R., Elliott S.T., Kania G., Li J., Yamanaka S., Crider D.G., Testa G., Li R.A., Lim B., Stewart C.L., Liu Y., Van Eyk J.E., Wersto R.P., Wobus A.M., Boheler K.R. B-MYB is essential for normal cell cycle progression and chromosomal stability of embryonic stem cells. PLoS One 2008, 3:e2478.
9. Yamauchi T., Ishidao T., Nomura T., Shinagawa T., Tanaka Y., Yonemura S., Ishii S. A B-Myb complex containing clathrin and filamin is required for mitotic spindle function. EMBO J. 2008, 27:1852-1862.
10. Lam E.W., Watson R.J. An E2F-binding site mediates cell-cycle regulated repression of mouse B-myb transcription. EMBO J. 1993, 12:2705-2713.
11. Tavner F., Frampton J., Watson R.J. Targeting an E2F site in the mouse genome prevents promoter silencing in quiescent and post-mitotic cells. Oncogene 2007, 26:2727-2735.
12. Saville M.K., Watson R.J. The cell-cycle regulated transcription factor B-Myb is phosphorylated by cyclin A/Cdk2 at sites that enhance its transactivation properties. Oncogene 1998, 17:2679-2689.
13. Korver W., Roose J., Clevers H. The winged-helix transcription factor Trident is expressed in cycling cells. Nucleic Acids Res. 1997, 25:1715-1719.
14. Ma R.Y., Tong T.H., Cheung A.M., Tsang A.C., Leung W.Y., Yao K.M. Raf/MEK/MAPK signaling stimulates the nuclear translocation and transactivating activity of FOXM1c. J. Cell Sci. 2005, 118:795-806.
15. Schmit F., Korenjak M., Mannefeld M., Schmitt K., Franke C., Gagrica S., Hanel F., Brehm A., Gaubatz S. LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 2007, 6:1903-1913.
16. Litovchick L., Sadasivam S., Florens L., Zhu X., Swanson S.K., Velmurugan S., Chen R., Washburn M.P., Liu X.S., DeCaprio J.A. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell 2007, 26:539-551.
17. Pilkinton M., Sandoval R., Colamonici O.R. Mammalian Mip/LIN-9 interacts with either the p107, p130/E2F4 repressor complex or B-Myb in a cell cycle-phase-dependent context distinct from the Drosophila dREAM complex. Oncogene 2007, 26:7535-7543.
18. Zhu W., Giangrande P.H., Nevins J.R. E2Fs link the control of G1/S and G2/M transcription. EMBO J. 2004, 23:4615-4626.
19. Leung T.W., Lin S.S., Tsang A.C., Tong C.S., Ching J.C., Leung W.Y., Gimlich R., Wong G.G., Yao K.M. Over-expression of FoxM1 stimulates cyclin B1 expression. FEBS Lett. 2001, 507:59-66.
20. Wang I.C., Chen Y.J., Hughes D., Petrovic V., Major M.L., Park H.J., Tan Y., Ackerson T., Costa R.H. 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. 2005, 25:10875-10894.
21. Fu Z., Malureanu L., Huang J., Wang W., Li H., van Deursen J.M., Tindall D.J., Chen J. Plk1-dependent phosphorylation of FoxM1 regulates a transcriptional programme required for mitotic progression. Nat. Cell Biol. 2008, 10:1076-1082.
22. Reichert N., Wurster S., Ulrich T., Schmitt K., Hauser S., Probst L., Götz R., Ceteci F., Moll R., Rapp U., Gaubatz S. Lin9, a subunit of the mammalian DREAM complex, is essential for embryonic development, for survival of adult mice, and for tumor suppression. Mol. Cell. Biol. 2010, 30:2896-2908.
23. Lavrrar J.L., Farnham P.J. The use of transient chromatin immunoprecipitation assays to test models for E2F1-specific transcriptional activation. J. Biol. Chem. 2004, 279:46343-46349.
24. Todaro G.J., Green H. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 1963, 17:299-313.
25. Major M.L., Lepe R., Costa R.H. Forkhead box M1B transcriptional activity requires binding of Cdk-cyclin complexes for phosphorylation-dependent recruitment of p300/CBP coactivators. Mol. Cell. Biol. 2004, 24:2649-2661.
26. Laoukili J., Alvarez M., Meijer L.A., Stahl M., Mohammed S., Kleij L., Heck A.J., Medema R.H. Activation of FoxM1 during G2 requires cyclin A/Cdk-dependent relief of autorepression by the FoxM1 N-terminal domain. Mol. Cell. Biol. 2008, 28:3076-3087.
27. Lindqvist A., Rodriguez-Bravo V., Medema R.H. The decision to enter mitosis: feedback and redundancy in the mitotic entry network. J. Cell Biol. 2009, 185:193-202.
28. Chen Y.J., Dominguez-Brauer C., Wang Z., Asara J.M., Costa R.H., Tyner A.L., Lau L.F., Raychaudhuri P. A conserved phosphorylation site within the Forkhead domain of FoxM1B is required for its activation by cyclin-CDK1. J. Biol. Chem. 2009, 284:30695-30707.
29. Ye H., Kelly T.F., Samadani U., Lim L., Rubio S., Overdier D.G., Roebuck K.A., Costa R.H. Hepatocyte nuclear factor 3/fork head homolog 11 is expressed in proliferating epithelial and mesenchymal cells of embryonic and adult tissues. Mol. Cell. Biol. 1997, 17:1626-1641.
30. Wen H., Andrejka L., Ashton J., Karess R., Lipsick J.S. Epigenetic regulation of gene expression by Drosophila Myb and E2F2-RBF via the Myb-MuvB/dREAM complex. Genes Dev. 2008, 22:601-614.
31. Lewis P.W., Beall E.L., Fleischer T.C., Georlette D., Link A.J., Botchan M.R. Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev. 2004, 18:2929-2940.
32. Johnson L.R., Johnson T.K., Desler M., Luster T.A., Nowling T., Lewis R.E., Rizzino A. Effects of B-Myb on gene transcription: phosphorylation-dependent activity and acetylation by p300. J. Biol. Chem. 2002, 277:4088-4097.
33. Bessa M., Saville M.K., Watson R.J. Inhibition of cyclin A/Cdk2 phosphorylation impairs B-Myb transactivation function without affecting interactions with DNA or the CBP coactivator. Oncogene 2001, 20:3376-3386.
34. Eeckhoute J., Carroll J.S., Geistlinger T.R., Torres-Arzayus M.I., Brown M. A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer. Genes Dev. 2006, 20:2513-2526.
35. Paik S., Shak S., Tang G., Kim C., Baker J., Cronin M., Baehner F.L., Walker M.G., Watson D., Park T., Hiller W., Fisher E.R., Wickerham D.L., Bryant J., Wolmark N. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 2004, 351:2817-2826.
36. Sotiriou C., Wirapati P., Loi S., Harris A., Fox S., Smeds J., Nordgren H., Farmer P., Praz V., Haibe-Kains B., Desmedt C., Larsimont D., Cardoso F., Peterse H., Nuyten D., Buyse M., Van de Vijver M.J., Bergh J., Piccart M., Delorenzi M. Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J. Natl. Cancer Inst. 2006, 98:262-272.
37. Miller L.D., Smeds J., George J., Vega V.B., Vergara L., Ploner A., Pawitan Y., Hall P., Klaar S., Liu E.T., Bergh J. An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13550-13555.
38. Yang D.K., Son C.H., Lee S.K., Choi P.J., Lee K.E., Roh M.S. Forkhead box M1 expression in pulmonary squamous cell carcinoma: correlation with clinicopathologic features and its prognostic significance. Hum. Pathol. 2009, 40:464-470.
39. Bektas N., Haaf A., Veeck J., Wild P.J., Luscher-Firzlaff J., Hartmann A., Knüchel R., Dahl E. Tight correlation between expression of the Forkhead transcription factor FOXM1 and HER2 in human breast cancer. BMC Cancer 2008, 8:42.
40. Martin K.J., Patrick D.R., Bissell M.J., Fournier M.V. Prognostic breast cancer signature identified from 3D culture model accurately predicts clinical outcome across independent datasets. PLoS One 2008, 3:e2994.