FOXM1c transactivates the human c-myc promoter directly via the two TATA boxes P1 and P2

FEBS Journal

Volumn 273, Issue 20, 2006, Pages 4645-4667

  Wierstra, Inken ^a,b   Alves, Jürgen ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b NONE   (Germany)

Author keywords

c myc; Core promoter; FOXM1; TATA box; TATA binding protein

Indexed keywords

HEAT SHOCK PROTEIN 70; HISTONE H2B; MYC PROTEIN; PROTEIN; PROTEIN C FOS; PROTEIN FOXM 1C; TATA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DATA BASE; GENE TARGETING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; TATA BOX; WILD TYPE;

BASE SEQUENCE; CELL PROLIFERATION; FORKHEAD TRANSCRIPTION FACTORS; GENES, MYC; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; TATA BOX; TATA-BOX BINDING PROTEIN; TRANS-ACTIVATION (GENETICS); TRANSCRIPTIONAL ACTIVATION;

EID: 33749386211     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05468.x     Document Type: Article

References (101)

1. Henriksson M & Lüscher B (1996) Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv Cancer Res 68, 111-182.
2. Facchini LM & Penn LZ (1998) The molecular role of myc in growth and transformation: recent discoveries lead to new insights. FASEB J 12, 633-651.
3. Grandori C, Cowley SM, James LP & Eisenman RN (2000) The Myc/Mad/Max network and the transcriptional control of cell behaviour. Annu Rev Cell Dev Biol 16, 653-699.
4. Oster SK, Ho CSW, Soucle EL & Penn LZ (2002) The myc oncogene: Marvelously Complex. Adv Cancer Res 84, 81-154.
5. Pelengaris S, Khan M & Evan G (2002) c-Myc: more than just a matter of life and death. Nat Rev Cancer 2, 764-776.
6. Hurlin PJ & Dezfouli S (2004) Functions of Myc:Max in the control of cell proliferation and tumorigenesis. Int Rev Cytol 238, 183-226.
7. Adhikary S & Eilers M (2005) Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol 6, 635-645.
8. Korver W, Roose J, Heinen K, Weghuis DO, de Bruijn D, van Kessel AG & Clevers H (1997b) The human TRIDENT/HFH-11/FKHL16 gene: structure, localization, and promoter characterization. Genomics 46, 435-442.
9. Korver W, Roose J, Wilson A & Clevers H (1997c) The winged-helix transcription factor trident is expressed in actively dividing lymphocytes. Immunobiology 198, 157-161.
10. Ye H, Kelly TF, Samadani U, Lim L, Rubio S, Overdier DG, Roebuck KA & Costa RH (1997) Hepatocyte nuclear factor3/fork head homolog 11 is expressed in proliferating epithelial and mesenchymal cells of embryonic and adult tissues. Mol Cell Biol 17, 1626-1641.
11. Ye H, Holterman AX, Yoo KW, Franks RR & Costa RH (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.
12. CIP1/WAF1 levels and accelerates mouse hepatocyte entry into S-phase following carbon tetrachloride liver injury. Hepatology 33, 1404-1414.
13. Wang X, Quail E, Hung NJ, Tan Y, Ye H & Costa RH (2002b) 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.
14. Wang X, Krupczak-Hollis K, Tan Y, Dennewitz MB, Adami GR & Costa RH (2002a) Increased hepatic Forkhead Box M1B (FoxM1B) levels in old-aged mice stimulated liver regeneration through diminished p27 Kip1 protein levels and increased Cdc25B expression. J Biol Chem 277, 44310-44316.
15. Wang X, Kiyokawa H, Dennewitz MB & Costa RH (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.
16. 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.
17. Kalinichenko VV, Gusariva GA, Tan Y, Wang IC, Major ML, Wang X, Yoder HM & Costa RH (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.
18. ARF tumor suppressor. Genes Dev 18, 830-850.
19. Krupczak-Hollis K, Wang X, Dennewitz MB & Costa RH (2003) Growth hormone stimulates proliferation of old-aged regenerating liver through Forkhead box m1b. Hepatology 38, 1552-1562.
20. Krupczak-Hollis K, Wang X, Kalinichenko VV, Gusarova GA, Wang IC, Dennewitz MB, Yoder HM, Kiyokawa H, Kaestner K & Costa RH (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.
21. Laoukili J, Kooistra MRH, Brás 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.
22. Ma R, Tong TH, Cheung AM, Tsang AC, Leung WY & Yao KM (2005) Raf/MEK/MAPK signaling stimulates the nuclear translocation and transactivating activity of FOXM1c. J Cell Sci 118, 795-806.
23. Wonsey DR & Follettie MT (2005) Loss of the forkhead transcription factor FoxM1 causes centrosome amplification and mitotic catastrophe. Cancer Res 65, 5181-5189.
24. Kalin TV, Wang IC, Ackerson TJ, Major ML, Detrisac CJ, Kalinichenko VV, Lyubimov A & Costa RH (2006) Increased levels of the FoxM1 transcription factor accelerate development and progression of prostate carcinomas in both TRAMP and LADY transgenic mice. Cancer Res 66, 1712-1720.
25. Kim IM, Ackerson T, Ramakrishna S, Tretiakova M, Wang IC, Kalin TV, Major ML, Gusarova GA, Yoder HM, Costa RH et al. (2006) The Forkhead Box m1 transcription factor stimulates the proliferation of tumor cells during development of lung cancer. Cancer Res 66, 2153-2161.
26. Liu M, Dai B, Kang SH, Ban K, Huang FJ, Lang FF, Aldape KD, Xie TX, Pelloski CE, Xie K et al. (2006) FoxM1B is overexpressed in human glioblastomas and critically regulates the tumorigenicity of glioma cells. Cancer Res 66, 3593-3602.
27. Zhang H, Ackermann AM, Gusarova GA, Lowe D, Feng X, Kopsombut UG, Costa RH & Gannon M (2006) The Foxm1 transcription factor is required to maintain pancreatic beta cell mass. Mol Endocrinol 20, 1853-1866.
28. Lüscher-Firzlaff JM, Westendorf JM, Zwicker J, Burkhardt H, Henriksson M, Müller R, Pirollet F & 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.
29. Wierstra I & Alves J (2006) FOXM1c is activated by cyclin E/Cdk2, cyclin A/Cdk2 and cyclin A/Cdk1, but repressed by GSK-3α. Biochem Biophys Res Commun 348, 99-108.
30. Wierstra I & Alves J (2006a) Despite its strong transactivation domain transcription factor FOXM1c is kept almost inactive by two different inhibitory domains. Biol Chem 387, 963-976.
31. Wierstra I & Alves J (2006b) Transcription factor FOXM1c is repressed by RB and activated by cyclin D1/Cdk4. Biol Chem 387, 949-962.
32. Smale ST (2001) Core promoters: active contributors to combinatorial gene regulation. Genes Dev 15, 2503-2508.
33. Butler J & Kadonaga JT (2002) The RNA polymerase II core promoter: a key component in the regulation of gene expression. Genes Dev 16, 2583-2592.
34. Smale ST & Kadonaga JT (2003) The RNA polymerase II core promoter. Annu Rev Biochem 72, 449-479.
35. Wefald FC, Devlin BH & Williams RS (1990) Functional heterogeneity of mammalian TATA-box sequences revealed by interaction with a cell-specific enhancer. Nature 344, 260-262.
36. Hochheimer A & Tjian R (2003) Diversified transcription initiation complexes expand promoter selectivity and tissue-specific gene expression. Genes Dev 17, 1309-1320.
37. Müller F & Tora L (2004) The multicoloured world of promoter recognition complexes. EMBO J 23, 2-8.
38. Burley SK & Roeder RG (1996) Biochemistry and structural biology of transcription factor IID (TFIID). Annu Rev Biochem 65, 769-799.
39. Roeder RG (1996) The role of general initiation factors in transcription by RNA polymerase II. Trends Biochem Sci 21, 327-335.
40. Verrijzer CP & Tjian R (1996) TAFs mediate transcriptional activation and promoter selectivity. Trends Biochem Sci 21, 338-342.
41. Yean D & Gralla J (1997) Transcription reinitiation: a special role for the TATA-box. Mol Cell Biol 17, 3809-3816.
42. Yean D & Gralla JD (1999) Transcription reinitiation rate: a potential role for TATA-box stabilization of the TFIID:TFIIA:DNA complex. Nucleic Acids Res 27, 831-838.
43. Damania B, Liberman P & Alwine JC (1998) Simian virus 40 large T antigen stabilizes the TATA-binding protein-TFIIA complex on the TATA element. Mol Cell Biol 18, 3926-3935.
44. Knutson A, Castano E, Oehlgeschläger T, Roeder RG & Westin G (2000) Downstream promoter sequences facilitate the formation of a specific transcription factor IID-promoter complex topology required for efficient transcription from the megalin/low density lipoprotein receptor-related protein 2 promoter. J Biol Chem 275, 14190-14197.
45. Lemon B & Tjian R (2000) Orchestrated response: a symphony of transcription factors for gene control. Genes Dev 14, 2551-2569.
46. Gill G (2001) Regulation of the initiation of eukaryotic transcription. Essays Biochem 37, 33-43.
47. Wolner BS & Gralla JD (2001) TATA-flanking sequences influence the rate and stability of TATA-binding protein and TFIIB binding. J Biol Chem 276, 6260-6266.
48. Fairley JA, Evans R, Hawkes NA & Roberts SGE (2002) Core promoter-dependent TFIIB conformation and a role for TFIIB conformation in transcription start site selection. Mol Cell Biol 22, 6697-6705.
49. Nikolov DB, Chen H, Halay ED, Hoffmann A, Roeder RG & Burley SK (1996) Crystal structure of a human TATA-box-binding protein/TATA element complex. Proc Natl Acad Sci USA 93, 4862-4867.
50. Patikoglou GA, Kim JL, Sun L, Yang SH, Kodadek T & Burley SK (1999) TATA element recognition by the TATA-box-binding protein has been conserved throughout evolution. Genes Dev 13, 3217-3230.
51. Hampsey M (1998) Molecular genetics of the RNA polymerase II general transcriptional machinery. Microbiol Mol Biol Rev 62, 465-503.
52. Tora L (2002) A unified nomenclature for TATA box binding protein (TBP)-associated factors (TAFs) involved in RNA polymerase II transcription. Genes Dev 16, 673-675.
53. Clark KL, Halay ED, Lai E & Burley SK (1993) Co-crystal structure of the HNF-3/fork head-DNA-recognition motif resembles histone H5. Nature 364, 412-420.
54. Ayer DE & Eisenman RN (1993) A switch from Myc: Max to Mad:Max heterocomplexes accompanies monocyte/macrophage differentiation. Genes Dev 7, 2110-2119.
55. Latchman DS (2001) Transcription factors: bound to activate or repress. Trend Biochem Sci 26, 211-213.
56. Lefstin JA & Yamamoto KR (1998) Allosteric effects of DNA on transcriptional regulators. Nature 392, 885-888.
57. Starr DB, Hoopes BC & Hawley DK (1995) DNA bending is an important component of site-specific recognition by the TATA binding protein. J Mol Biol 250, 434-446.
58. Bareket-Samish A, Cohen I & Haran TE (2000) Signals for TBP/TATA-box recognition. J Mol Biol 299, 965-977.
59. Nelson HC, Finch JT, Luisi BF & Klug A (1987) The structure of an oligo(dA)-oligo(dT) tract and its biological implications. Nature 330, 221-226.
60. Koo HS, Drak J, Rice JA & Crothers DM (1990) Determination of the extent of DNA bending by an adenine-thymine tract. Biochemistry 29, 4227-4234.
61. Hoopes BC, LeBlanc JF & Hawley DK (1998) Contributions of the TATA-box sequence to rate-limiting steps in transcription initiation by RNA polymerase II. J Mol Biol 277, 1015-1031.
62. Parvin JD, McCormick RJ, Sharp PA & Fisher DE (1995) Pre-bending of a promote sequence enhances affinity for the TATA-binding factor. Nature 373, 724-727.
63. Simon MC, Fisch TM, Benecke BJ, Nevins JR & Heintz N (1988) Definition of multiple, functionally distinct TATA elements, one of which is a target in the hsp70 promoter for E1A regulation. Cell 52, 723-729.
64. Simon MC, Rooney RJ, Fisch TM, Heintz N & Nevins JR (1990) E1A-dependent trans-activation of the c-fos promoter requires the TATAA sequence. Proc Natl Acad Sci USA 87, 513-517.
65. Shworak NW, O'Connor T, Wong NCW & Gedamu L (1993) Distinct TATA motifs regulate differential expression of human metallothionein I genes MT-IF and MT-IG. J Biol Chem 268, 24460-24466.
66. Takeda S, North DL, Diagana T, Mayagoe Y, Lakich MM & Whalen RG (1995) Myogenic regulatory factors can activate TATA-containing promoter elements via an E-box independent mechanism. J Biol Chem 270, 15664-15670.
67. Diagana TT, North DL, Jabet C, Fiszman MY, Takeda S & Whalen RG (1997) The transcriptional activity of a muscle-specific promoter depends critically on the structure of the TATA element and its binding protein. J Mol Biol 265, 480-493.
68. II130/135 in promoter-specific trans-activation by simian virus 40 small t antigen. J Gen Virol 84, 1887-1897.
69. Lee DK, Wang KC & Roeder RG (1997) Functional significance of the TATA element major groove in transcription initiation by RNA polymerase II. Nucleic Acids Res 25, 4338-4345.
70. Shaulian E & Karin M (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4, E131-E136.
71. Eferl R & Wagner EF (2003) AP-1: a double edged sword in tumorigenesis. Nat Rev Cancer 3, 859-868.
72. Milde-Langosch K (2005) The Fos family of transcription factors and their role in tumourigenesis. Eur J Cancer 41, 2449-2461.
73. Beere HM & Green DR (2001) Stress management - heat shock protein-70 and the regulation of apoptosis. Trends Cell Biol 11, 6-10.
74. Jolly C & Morimoto RI (2000) Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J Natl Cancer Inst 92, 1564-1572.
75. Spencer CA & Groudine M (1991) Control of c-myc regulation in normal and neoplastic cells. Adv Cancer Res 56, 1-48.
76. Marcu KB, Bossone SA & Patel AJ (1992) Myc function and regulation. Annu Rev Biochem 61, 809-860.
77. Marcu K, Patel AJ & Yang Y (1997) Differential regulation of the c-MYC P1 and P2 promoters in the absence of functional tumor suppressors: implications for mechanisms of deregulated MYC transcription. Curr Topics Microbiol Immunol 224, 47-56.
78. Levens D, Duncan RC, Tomonaga T, Michelotti GA, Collins I, Davis-Smyth T, Zheng T & Michelotti EF (1997) DNA conformation, topology, and the regulation of c-myc expression. Curr Topics Microbiol Immunol 224, 33-46.
79. Potter M & Marcu KB (1997) The c-myc story: where we've been, where we seem to be going. Curr Topics Microbiol Immunol 224, 1-17.
80. Liu J & Levens D (2006) Making Myc. Curr Topics Microbiol Immunol 302, 1-32.
81. Bousset K, Oelgeschläger M, Henriksson M, Schreek S, Burkhardt H, Litchfield DW, Lüscher-Firzlaff JM & Lüscher B (1994) Regulation of transcription factors c-Myc, Max and c-Myb by casein kinase II. Cell Mol Biol Res 40, 501-511.
82. Lüscher-Firzlaff JM, Lilischkis R & Lüscher B (2006) Regulation of transcription factor FOXM1c by cyclin E/CDK2. FEBS Lett 580, 1716-1722.
83. Austen M, Lüscher B & Lüscher-Firzlaff JM (1997) Characterization of the transcriptional regulator YY1. J Biol Chem 272, 1709-1717.
84. Nordeen SK (1988) Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques 6, 454-457.
85. Firzlaff JM, Lüscher B & Eisenman RN (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.
86. Chen CA & Okayama H (1988) Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechniques 6, 632-638.
87. Lai JS & Herr W (1992) Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations. Proc Natl Acad Sci USA 89, 6958-6962.
88. Oelgeschläger M, Krieg J, Lüscher-Firzlaff JM & Lüscher B (1995) Casein kinase II phosphorylation site mutations in c-Myc affect DNA binding and transcriptional cooperativity with NF-M. Mol Cell Biol 15, 5966-5974.
89. Bouchard C, Dittrich O, Kiermaier A, Dohmann K, Menkel A, Eilers M & Lüscher B (2001) Regulation of cyclin D2 gene expression by the Myc/Max/Mad network: Myc-dependent TRRAP recruitment and histone acetylation at the cyclin D2 promoter. Genes Dev 15, 2042-2047.
90. Bucher P (1990) Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol 212, 563-568.
91. Schmidt M, Nazarov V, Stevens L, Watson R & Wolff L (2000) Regulation of the resident chromosomal copy of c-myc by c-Myb is involved in myeloid leukemogenesis. Mol Cell Biol 20, 1970-1981.
92. Wang X, Bhattacharyya D, Dennewitz MB, Kalinichenko VV, Zhou Y, Lepe R & Costa RH (2003) Rapid hepatocyte nuclear translocation of the Forkhead Box M1B (FoxM1B) transcription factor caused a transient increase in size of regenerating transgenic hepatocytes. Gene Expr 11, 149-162.
93. Kim IM, Ramakrishna S, Gusarova GA, Yoder HM, Costa RH & Kalinichenko VV (2005) The Forkhead Box M1 transcription factor is essential for embryonic development of pulmonary vasculature. J Biol Chem 280, 22278-22286.
94. Nasi S, Ciarapica R, Jucker R, Rosati J & Soucek L (2001) Making decisions through Myc. FEBS Lett 490, 153-162.
95. Patel JH, Loboda AP, Showe MK, Showe LC & McMahon SB (2004) Analysis of genomic targets reveals complex functions of MYC. Nat Rev Cancer 4, 562-568.
96. Lee LA & Dang CV (2006) Myc target transcriptomes. Curr Topics Microbiol Immunol 302, 145-167.
97. Claassen GF & Hann SR (1999) Myc-mediated transformation: the repression connection. Oncogene 18, 2925-2933.
98. Cole MD & McMahon SB (1999) The Myc oncoprotein: a critical evaluation of transactivation and target gene regulation. Oncogene 18, 2916-2924.
99. Dang CV (1999) c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol Cell Biol 19, 1-11.
100. Vogt PK (2001) Jun, the oncoprotein. Oncogene 20, 2365-2377.
101. van Dam H & Castellazzi M (2001) Distinct roles of Jun:Fos and Jun:ATF dimers in oncogenesis. Oncogene 20, 2453-2464.