Transcription factor FOXM1c is repressed by RB and activated by cyclin D1/Cdk4

Biological Chemistry

Volumn 387, Issue 7, 2006, Pages 949-962

  Wierstra, Inken ^a   Alves, Jürgen ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Cyclin D1 Cdk4; Cyclin E Cdk2; FOXM1c; RB

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE 4; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR FOXM1C; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CONFERENCE PAPER; CONTROLLED STUDY; DNA BINDING; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; TRANSACTIVATION;

ANIMALS; BLOTTING, WESTERN; CELL LINE; CYCLIN D1; CYCLIN-DEPENDENT KINASE 4; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOPRECIPITATION; PLASMIDS; RETINOBLASTOMA PROTEIN;

EID: 33746216564     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2006.119     Document Type: Conference Paper

References (69)

1. Adams, P.D. (2001). Regulation of the retinoblastoma tumor suppressor protein by cyclin/Cdks. Biochim. Biophys. Acta 1471, M123-133.
2. Adams, P.D. and Kaelin, W.G. (1995). Transcriptional control by E2F. Cancer Biol. 6, 99-108.
3. Blais, A. and Dynlacht, B.D. (2004). Hitting their targets: an emerging picture of E2F and cell cycle control. Curr. Opin. Genet. Dev. 14, 527-532.
4. Bousset, K., Oelgeschläger, M., Henriksson, M., Schreek, S., Burkhardt, H., Litchfield, D.W., Lüscher-Firzlaff, J.M., and Lüscher, B. (1994). Regulation of transcription factors c-Myc, Max and c-Myb by casein kinase II. Cell. Mol. Biol. Res. 40, 501-511.
5. Bracken, A.P., Ciro, M., Cocito, A., and Helin, K. (2004). E2F target genes: unraveling the biology. Trends Biochem. Sci. 29, 409-417.
6. Cam, H. and Dynlacht, B.D. (2003). Emerging roles for E2F: beyond the G1/S transition and DNA replication. Cancer Cell 3, 311-316.
7. Chen, C.A. and Okayama, H. (1988). Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechnology 6, 632-638.
8. Ciemerych, M.A. and Sicinski, P. (2005). Cell cycle in mouse development. Oncogene 24, 2877-2898.
9. Classon, M. and Harlow, E. (2002). The retinoblastoma tumour suppressor in development and cancer. Nat. Rev. Cancer 2, 910-917.
10. Cobrinik, D. (2005). Pocket proteins and cell cycle control. Oncogene 24, 2796-2809.
11. DeGregori, J. (2002). The genetics of the E2F family of transcription factors: shared functions and unique roles. Biochim. Biophys. Acta 1602, 131-150.
12. Dimova, D.K. and Dyson, N.J. (2005). The E2F transcriptional network: old acquaintances with new faces. Oncogene 24, 2810-2826.
13. Dyson, N. (1998). The regulation of E2F by pRB-family proteins. Genes Dev. 12, 2245-2262.
14. Evan, G.I. and Vousden, K.H. (2001). Proliferation, cell cycle and apoptosis in cancer. Nature 411, 342-348.
15. Ezhevsky, S.A., Nagahara, H., Vocero-Akbani, A.M., Gius, D.R., Wei, M.C., and Dowdy, S.F. (1997). Hypo-phosphorylation of the retinoblastoma protein (pRb) by cyclinD-Cdk4/6 complexes results in active pRb. Proc. Natl. Acad. Sci. USA 94, 10699-10704.
16. Fernandez, P.C., Frank, S.R., Wang, L., Schroeder, M., Liu, S., Greene, J., Cocito, A., and Amati, B. (2003). Genomic targets of the human c-Myc protein. Genes Dev. 17, 1115-1129.
17. Firzlaff, J.M., Lüscher, B., and Eisenman, R.N. (1991). Negative charge at the casein kinase II phosphorylation site is important for transformation but not for Rb binding by the E7 protein of human papillomavirus type 16. Proc. Natl. Acad. Sci. USA 88, 5187-5191.
18. Flemington, E.K., Speck, S.H., and Kaelin, W.G. (1993). E2F-1 mediated transactivation is inhibited by complex formation with the retinoblastoma susceptibility gene product. Proc. Natl. Acad. Sci. USA 90, 6914-6918.
19. Frolov, M.V. and Dyson, N.J. (2004). Molecular mechanisms of E2F-dependent activation and RB-mediated repression. J. Cell Sci. 117, 2173-2181.
20. Hahn, W.C. and Weinberg, R.A. (2002). Modelling the molecular circuitry of cancer. Nat. Rev. Cancer 2, 331-341.
21. Hanahan, D. and Weinberg, R.A. (2000). The hallmarks of cancer. Cell 100, 57-70.
22. Harbour, J.W. and Dean, D.C. (2000). The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev. 14, 2393-2409.
23. Harbour, J.W., Luo, R.X., Dei Santi, A., Postigo, A.A., and Dean, D.C. (1999). Cdk phosphorylation triggers sequential intramolecular interactions that progressively block Rb functions as cells move through G1. Cell 98, 859-869.
24. Helin, K., Harlow, E., and Fattaey, A. (1993). Inhibition of E2F-1 transactivation by direct binding of the retinoblastoma protein. Mol. Cell. Biol. 13, 6501-6508.
25. Hiebert, S.W. (1993). Regions of the retinoblastoma gene product required for its interaction with the E2F transcription factor are necessary for E2 promoter repression and pRb-mediated growth suppression. Mol. Cell. Biol. 13, 3384-3391.
26. Janknecht, R., Ernst, W.H., Pingoud, V., and Nordheim, A. (1993). Activation of ternary complex factor Elk-1 by MAP kinases. EMBO J. 12, 5097-5104.
27. Kalinichenko, V.V., Gusariva, G.A., Tan, Y., Wang, I.C., Major, M.L., Wang, X., Yoder, H.M., and Costa, R.H. (2003). Ubiquitous expression of the Forkhead Box M1B transgene accelerates proliferation of distinct pulmonary cell types following lung injury. J. Biol. Chem. 39, 37888-37894.
28. ARF tumor suppressor. Genes Dev. 18, 830-850.
29. Korver, W., Roose, J., and Clevers, H. (1997a). The winged-helix transcription factor Trident is expressed in cycling cells. Nucleic Acids Res. 25, 1715-1719.
30. Korver, W., Roose, J., Heinen, K., Weghuis, D.O., de Bruijn, D., van Kessel, A.G., and Clevers, H. (1997b). The human TRIDENT/HFH-11/FKHL16 gene: structure, localization, and promoter characterization. Genomics 46, 435-442.
31. Korver, W., Roose, J., Wilson, A., and Clevers, H. (1997c). The winged-helix transcription factor Trident is expressed in actively dividing lymphocytes. Immunobiol. 198, 157-161.
32. Krupczak-Hollis, K., Wang, X., Dennewitz, M.B., and Costa, R.H. (2003). Growth hormone stimulates proliferation of old-aged regenerating liver through Forkhead Box m1b. Hepatology 38, 1552-1562.
33. Krupczak-Hollis, K., Wang, X., Kalinichenko, V.V., Gusarova, G.A., Wang, I.C., Dennewitz, M.B., Yoder, H.M., Kiyokawa, H., Kaestner, K., and Costa, R.H. (2004). The mouse Forkhead Box m1 transcription factor is essential for hepatoblast mitosis and development of intrahepatic bile ducts and vessels during liver morphogenesis. Dev. Biol. 276, 74-88.
34. Lai, J.S. and Herr, W. (1992). Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations. Proc. Natl. Acad. Sci. USA 89, 6958-6962.
35. Laoukili, J., Kooistra, M.R.H., Brás, A., Kauw, J., Kerkhoven, R.M., Morrison, A., Clevers, H., and Medema, R.H. (2005). FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat. Cell Biol. 7, 126-136.
36. Lundberg, A.S. and Weinberg, R.A. (1998). Functional inactivation of the retinoblastoma protein requires sequential modification by at least two distinct cyclin-CDK complexes. Mol. Cell. Biol. 18, 753-761.
37. Lüscher-Firzlaff, J.M., Westendorf, J.M., Zwicker, J., Burkhardt, H., Henriksson, M., Müller, R., Pirollet, F., and Lüscher, B. (1999). Interaction of the fork head domain transcription factor MPP2 with the human papilloma virus 16 E7 protein: enhancement of transformation and transactivation. Oncogene 18, 5620-5630.
38. Lüscher-Firzlaff, J.M., Lilischkis, R., and Lüscher, B. (2006). Regulation of transcription factor FOXM1c by Cyclin E/CDK2. FEBS Lett. 580, 1716-1722.
39. Ma, R.Y., Tong, T.H., Cheung, A.M., Tsang, A.C., Leung, W.Y., and Yao, K.M. (2005). Raf/MEK/MAPK signaling stimulates the nuclear translocation and transactivating activity of FOXM1c. J. Cell Sci. 118, 795-806
40. Major, M.L., Lepe, R., and Costa, R.H. (2004). Forkhead Box M1B transcriptional activity requires binding of Cdk-cyclin complexes for phosphorylation-dependent recruitment of p300/CBP coactivators. Mol. Cell. Biol. 24, 2649-2661.
41. Malumbres, M. and Barbacid, M. (2001). To cycle or not to cycle: a critical decision in cancer. Nat. Rev. Cancer 1, 222-231.
42. Meyerson, M. and Harlow, E. (1994). Identification of G1 kinase activity for Cdk6, a novel cyclin D partner. Mol. Cell. Biol. 14, 2077-2086.
43. Obaya, A.J. and Sedivy, J.M. (2002). Regulation of cyclin-Cdk activity in mammalian cells. Cell. Mol. Life Sci. 59, 126-142.
44. Oelgeschläger, M., Krieg, J., Lüscher-Firzlaff, J.M., and Lüscher, B. (1995). Casein kinase II phosphorylation site mutations in c-Myb affect DNA binding and transcriptional cooperativity with NF-M. Mol. Cell. Biol. 15, 5966-5974.
45. Okabe, H., Satoh, S., Kato, T., Kitahara, O., Yanagawa, R., Yamaoka, Y., Tsunoda, T., Furukawa, Y., and Nakamura, Y. (2001). Genome-wide analysis of gene expression in human hepatocellular carcinomas using cDNA microarray: Identification of genes involved in viral carcinogenesis and tumor progression. Cancer Res. 61, 2129-2137.
46. Oster, S.K., Ho, C.S.W., Soucie, E.L., and Penn, L.Z. (2002). The myc oncogene: MarvelouslY Complex. Adv. Cancer Res. 84, 81-154.
47. Pardee, A.B. (1989). G1 events and regulation of proliferation. Science 246, 603-308.
48. Pilarsky, C., Wenzig, M., Specht, T., Saeger, H.D., and Grutzmann, R. (2004). Identification and validation of commonly overexpressed genes in solid tumors by comparison of microarray data. Neoplasia 6, 744-750.
49. Qin, X.Q., Chittenden, T., Livingston, D.M., and Kaelin, W.G. (1992). Identification of a growth suppression domain within the retinoblastoma gene product. Genes Dev. 6, 953-964.
50. Sellers, W.R., Novitch, B.G., Miyake, S., Heith, A., Otterson, G.A., Kaye, F.J., Lassar, A.B., and Kaelin, W.G. (1998). Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev. 12, 95-106.
51. Sherr, C.J. (2001). The INK4A/ARF network in tumour suppression. Nat. Rev. Mol. Cell Biol. 2, 731-737.
52. Sherr, C.J. and McCormick, F. (2002). The RB and p53 pathways in cancer. Cancer Cell 2, 103-112.
53. Sherr, C.J. and Roberts, J.M. (1999). CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13, 1501-1512.
54. Sherr, C.J. and Roberts, J.M. (2004). Living with or without cyclins and cyclin-dependent kinases. Genes Dev. 18, 2699-2711.
55. Stevens, C. and La Thangue, N.B. (2002). E2F and cell cycle control: a double-edged sword. Arch. Biochem. Biophys. 412, 157-169.
56. Teh, M.T., Wong, S.T., Neill, G.W., Ghali, L.R., Philpott, M.P., and Quinn, A.G. (2002). FOXM1 is a downstream target of Gli1 in basal cell carcinomas. Cancer Res. 62, 4773-4780.
57. Trimarchi, J.M. and Lees, J.A. (2002). Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 3, 11-20.
58. van den Boom, J., Wolter, M., Kuick, R., Misek, D.E., Youkilis, A.S., Wechsler, D.S., Sommer, C., Reifenberger, G., and Hanash, S.M. (2003). Characterization of gene expression profiles associated with glioma progression using oligonucleotide-based microarray analysis and real-time transcription-polymerase chain reaction. Am. J. Pathol. 163, 1033-1043.
59. Wang, I.C., Chen, Y.J., Hughes, D., Petrovic, V., Major, M.L., Park, H.J., Tan, Y., Ackerson, T., and Costa, R.H. (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.
60. CIP1/WAF1 levels and accelerates mouse hepatocyte entry into S-phase following carbon tetrachloride liver injury. Hepatology 33, 1404-1414.
61. Wang, X., Quail, E., Hung, N.J., Tan, Y., Ye, H., and Costa, R.H. (2001b). Increased levels of forkhead box M1B transcription factor in transgenic mouse hepatocytes prevent age-related proliferation defects in regenerating liver. Proc. Natl. Acad. Sci. USA 98, 11468-11473.
62. Kip1 protein levels and increased Cdc25B expression. J. Biol. Chem. 277, 44310-44316.
63. Wang, X., Kiyokawa, H., Dennewitz, M.B., and Costa, R.H. (2002b). The Forkhead Box m1b transcription factor is essential for hepatocyte DNA replication and mitosis during mouse liver regeneration. Proc. Natl. Acad. Sci. USA 99, 16881-16886.
64. Weinberg, R.A. (1995). The retinoblastoma protein and cell cycle control. Cell 81, 323-330.
65. Wierstra, I. and Alves, J. (2006). Despite its strong transactivation domain transcription factor FOXM1c is kept almost inactive by two different inhibitory domains. Biol. Chem. 387, 963-976.
66. Wonsey, D.R. and Follettie, M.T. (2005). Loss of the forkhead transcription factor FoxM1 causes centrosome amplification and mitotic catastrophe. Cancer Res. 65, 5181-5189.
67. Ye, H., Kelly, T.F., Samadani, U., Lim, L., Rubio, S., Overdier, D.G., Roebuck, K.A., and Costa, R.H. (1997). Hepatocyte nuclear factor 3/fork head homolog 11 is expressed in proliferating epithelial and mesenchymal cells of embryonic and adult tissues. Mol. Cell. Biol. 17, 1626-1641.
68. Ye, H., Holterman, A.X., Yoo, K.W., Franks, R.R., and Costa, R.H. (1999). Premature expression of the winged helix transcription factor HFH-11B in regenerating mouse liver accelerates hepatocyte entry into S-phase. Mol. Cell. Biol. 19, 8570-8580.
69. Zhang, H.S., Gavin, M., Dahiya, A., Postigo, A.A., Ma, D., Luo, R.X., Harbour, W.J., and Dean, D.C. (2000). Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell 101, 79-89.