Negative regulation of the oncogenic transcription factor FoxM1 by thiazolidinediones and mithramycin

Cancer Biology and Therapy

Volumn 9, Issue 12, 2010, Pages 1008-1016

  Petrovic, Vladimir ^a   Costa, Robert H ^a   Lau, Lester F ^a   Raychaudhuri, Pradip ^a   Tyner, Angela L ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

FoxM1; PPAR ; Sp1; Thiazolidinediones; Transcription; Troglitazone

Indexed keywords

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; CENTROMERE PROTEIN B; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DNA; LUCIFERASE; MESSENGER RNA; MITHRAMYCIN; ONCOPROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; RETINOID X RECEPTOR; S PHASE KINASE ASSOCIATED PROTEIN 2; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FORKHEAD BOX M1; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTION FACTOR SP1; TROGLITAZONE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CANCER CELL CULTURE; CANCER GROWTH; CELL CYCLE ARREST; CELL STRAIN; CELL STRAIN HEPG2; CELL STRAIN PLC PRF 5; CHROMATIN IMMUNOPRECIPITATION; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA CONTENT; DRUG MECHANISM; DRUG TARGETING; FLOW CYTOMETRY; GC RICH SEQUENCE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSCRIPTION REGULATION;

ANTIBIOTICS, ANTINEOPLASTIC; CELL DIVISION; CELL LINE, TUMOR; CHROMANS; DOWN-REGULATION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HUMANS; PLICAMYCIN; PPAR GAMMA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RETINOID X RECEPTORS; SP1 TRANSCRIPTION FACTOR; THIAZOLIDINEDIONES; TRANSCRIPTION FACTORS;

EID: 77954412025     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.9.12.11710     Document Type: Article

References (69)

1. Hannenhalli S, Kaestner KH. The evolution of Fox genes and their role in development and disease. Nat Rev Genet 2009; 10:233-40.
2. Korver W, Roose J, Clevers H. The winged-helix transcription factor Trident is expressed in cycling cells. Nucleic acids research 1997; 25:1715-9. (Pubitemid 27303351)
3. Ye H, Kelly TF, Samadani U, Lim L, Rubio S, Overdier DG, et al. 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; 17:1626-41.
4. Ye H, Holterman AX, Yoo KW, Franks RR, Costa RH. Premature expression of the winged helix transcription factor HFH-11B in regenerating mouse liver accelerates hepatocyte entry into S phase. Mol Cell Biol 1999; 19:8570-80. (Pubitemid 30414050)
5. Laoukili J, Stahl M, Medema RH. FoxM1: at the crossroads of ageing and cancer. Biochim Biophys Acta 2007; 1775:92-102.
6. Korver W, Roose J, Heinen K, Weghuis DO, de Bruijn D, van Kessel AG, Clevers H. The human TRIDENT/HFH-11/FKHL16 gene: structure, localization and promoter characterization. Genomics 1997; 46:435-42.
7. Luscher-Firzlaff JM, Westendorf JM, Zwicker J, Burkhardt H, Henriksson M, Muller R, et al. Interaction of the fork head domain transcription factor MPP2 with the human papilloma virus 16 E7 protein: enhancement of transformation and transactivation. Oncogene 1999; 18:5620-30.
8. Wierstra I, Alves J. FOXM1, a typical proliferation-associated transcription factor. Biological chemistry 2007; 388:1257-74. (Pubitemid 350135573)
9. Costa RH. FoxM1 dances with mitosis. Nat Cell Biol 2005; 7:108-10.
10. Wang IC, Chen YJ, Hughes D, Petrovic V, Major ML, Park HJ, et al. 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; 25:10875-94.
11. Petrovic V, Costa RH, Lau LF, Raychaudhuri P, Tyner AL. FoxM1 regulates growth factor-induced expression of kinase-interacting stathmin (KIS) to promote cell cycle progression. J Biol Chem 2008; 283:453-60.
12. Wang IC, Chen YJ, Hughes DE, Ackerson T, Major ML, Kalinichenko VV, et al. FoxM1 regulates transcription of JNK1 to promote the G1/S transition and tumor cell invasiveness. J Biol Chem 2008; 283:20770-8.
13. Major ML, Lepe R, Costa RH. Forkhead box M1B transcriptional activity requires binding of Cdk-cyclin complexes for phosphorylation-dependent recruitment of p300/CBP coactivators. Mol Cell Biol 2004; 24:2649-61.
14. Chen YJ, Dominguez-Brauer C, Wang Z, Asara JM, Costa RH, Tyner AL, et al. A Conserved Phosphorylation Site within the Forkhead Domain of FoxM1B Is Required for Its Activation by Cyclin-CDK1. J Biol Chem 2009; 284:30695-707.
15. Park HJ, Carr JR, Wang Z, Nogueira V, Hay N, Tyner AL, et al. FoxM1, a critical regulator of oxidative stress during oncogenesis. EMBO J 2009; 28:2908-18.
16. Grommes C, Landreth GE, Heneka MT. Antineoplastic effects of peroxisome proliferator-activated receptor gamma agonists. The lancet oncology 2004; 5:419-29. (Pubitemid 38878045)
17. Palmer CN, Hsu MH, Griffin HJ, Johnson EF. Novel sequence determinants in peroxisome proliferator signaling. J Biol Chem 1995; 270:16114-21.
18. Kliewer SA, Lehmann JM, Milburn MV, Willson TM. The PPARs and PXRs: nuclear xenobiotic receptors that define novel hormone signaling pathways. Recent Prog Horm Res 1999; 54:345-67.
19. Kubota T, Koshizuka K, Williamson EA, Asou H, Said JW, Holden S, et al. Ligand for peroxisome proliferator-activated receptor gamma (troglitazone) has potent antitumor effect against human prostate cancer both in vitro and in vivo. Cancer Res 1998; 58:3344-52.
20. 1 cell cycle regulators. Biochem Biophys Res Commun 2001; 286:916-22.
21. Koga H, Sakisaka S, Harada M, Takagi T, Hanada S, Taniguchi E, et al. Involvement of p21(WAF1/Cip1), p27(Kip1) and p18(INK4c) in troglitazone-induced cell cycle arrest in human hepatoma cell lines. Hepatology 2001; 33:1087-97.
22. 1 arrest by p27(Kip1) induction that is mediated by inhibition of proteasome in human gastric cancer cells. Jpn J Cancer Res 2002; 93:774-82.
23. Yu J, Qiao L, Zimmermann L, Ebert MP, Zhang H, Lin W, et al. Troglitazone inhibits tumor growth in hepatocellular carcinoma in vitro and in vivo. Hepatology 2006; 43:134-43.
24. Sarraf P, Mueller E, Jones D, King FJ, DeAngelo DJ, Partridge JB, et al. Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nat Med 1998; 4:1046-52.
25. Bae MA, Song BJ. Critical role of c-Jun N-terminal protein kinase activation in troglitazone-induced apoptosis of human HepG2 hepatoma cells. Mol Pharmacol 2003; 63:401-8.
26. Baek SJ, Wilson LC, Hsi LC, Eling TE. Troglitazone, a peroxisome proliferator-activated receptor gamma (PPARgamma) ligand, selectively induces the early growth response-1 gene independently of PPAR gamma. A novel mechanism for its anti-tumorigenic activity. J Biol Chem 2003; 278:5845-53.
27. Okura T, Nakamura M, Takata Y, Watanabe S, Kitami Y, Hiwada K. Troglitazone induces apoptosis via the p53 and Gadd45 pathway in vascular smooth muscle cells. Eur J Pharmacol 2000; 407:227-35.
28. Yang CC, Wang YC, Wei S, Lin LF, Chen CS, Lee CC, Lin CC. Peroxisome proliferator-activated receptor gamma-independent suppression of androgen receptor expression by troglitazone mechanism and pharmacologic exploitation. Cancer Res 2007; 67:3229-38.
29. Kim IM, Ackerson T, Ramakrishna S, Tretiakova M, Wang IC, Kalin TV, et al. The Forkhead Box m1 transcription factor stimulates the proliferation of tumor cells during development of lung cancer. Cancer Res 2006; 66:2153-61.
30. ARF tumor suppressor. Genes Dev 2004; 18:830-50.
31. Wei S, Yang J, Lee SL, Kulp SK, Chen CS. PPARgamma-independent antitumor effects of thiazolidinediones. Cancer Lett 2008.
32. Wells J, Farnham PJ. Characterizing transcription factor binding sites using formaldehyde crosslinking and immunoprecipitation. Methods 2002; 26:48-56. (Pubitemid 34969217)
33. Kip1-associated cell cycle arrest through down-regulating Skp2 in human hepatoma cells. Hepatology 2003; 37:1086-96.
34. Scheen AJ. Pharmacokinetic interactions with thiazolidinediones. Clin Pharmacokinet 2007; 46:1-12.
35. Sahi J, Black CB, Hamilton GA, Zheng X, Jolley S, Rose KA, et al. Comparative effects of thiazolidinediones on in vitro P450 enzyme induction and inhibition. Drug Metab Dispos 2003; 31:439-46.
36. Werner AL, Travaglini MT. A review of rosiglitazone in type 2 diabetes mellitus. Pharmacotherapy 2001; 21:1082-99.
37. Loi CM, Young M, Randinitis E, Vassos A, Koup JR. Clinical pharmacokinetics of troglitazone. Clin Pharmacokinet 1999; 37:91-104.
38. Bryne JC, Valen E, Tang MH, Marstrand T, Winther O, da Piedade I, et al. JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic acids research 2008; 36:102-6.
39. Jia Z, Zhang J, Wei D, Wang L, Yuan P, Le X, et al. Molecular basis of the synergistic antiangiogenic activity of bevacizumab and mithramycin A. Cancer Res 2007; 67:4878-85.
40. Vega VB, Bangarusamy DK, Miller LD, Liu ET, Lin CY. BEARR: Batch Extraction and Analysis of cis-Regulatory Regions. Nucleic Acids Res 2004; 32:257-60.
41. Gee JE, Blume S, Snyder RC, Ray R, Miller DM. Triplex formation prevents Sp1 binding to the dihydrofolate reductase promoter. J Biol Chem 1992; 267:11163-7.
42. Pilarsky C, Wenzig M, Specht T, Saeger HD, Grutzmann R. Identification and validation of commonly overexpressed genes in solid tumors by comparison of microarray data. Neoplasia 2004; 6:744-50. (Pubitemid 40041492)
43. Gartel AL. FoxM1 inhibitors as potential anticancer drugs. Expert Opin Ther Targets 2008; 12:663-5.
44. Roman J. Peroxisome proliferator-activated receptor gamma and lung cancer biology: implications for therapy. J Investig Med 2008; 56:528-33.
45. Radhakrishnan SK, Gartel AL. The PPARgamma agonist pioglitazone post-transcriptionally induces p21 in PC3 prostate cancer but not in other cell lines. Cell Cycle 2005; 4:582-4.
46. Wang IC, Meliton L, Tretiakova M, Costa RH, Kalinichenko VV, Kalin TV. Transgenic expression of the forkhead box M1 transcription factor induces formation of lung tumors. Oncogene 2008; 27:4137-49.
47. Yoshida Y, Wang IC, Yoder HM, Davidson NO, Costa RH. The forkhead box M1 transcription factor contributes to the development and growth of mouse colorectal cancer. Gastroenterology 2007; 132:1420-31.
48. Kalin TV, Wang IC, Ackerson TJ, Major ML, Detrisac CJ, Kalinichenko VV, et al. Increased levels of the FoxM1 transcription factor accelerate development and progression of prostate carcinomas in both TRAMP and LADY transgenic mice. Cancer Res 2006; 66:1712-20.
49. Weng JR, Chen CY, Pinzone JJ, Ringel MD, Chen CS. Beyond peroxisome proliferator-activated receptor gamma signaling: the multi-facets of the antitumor effect of thiazolidinediones. Endocr Relat Cancer 2006; 13:401-13.
50. Black AR, Black JD, Azizkhan-Clifford J. Sp1 and kruppel-like factor family of transcription factors in cell growth regulation and cancer. J Cell Physiol 2001; 188:143-60.
51. Wang L, Wei D, Huang S, Peng Z, Le X, Wu TT, et al. Transcription factor Sp1 expression is a significant predictor of survival in human gastric cancer. Clin Cancer Res 2003; 9:6371-80. (Pubitemid 38031822)
52. Yao JC, Wang L, Wei D, Gong W, Hassan M, Wu TT, et al. Association between expression of transcription factor Sp1 and increased vascular endothelial growth factor expression, advanced stage, and poor survival in patients with resected gastric cancer. Clin Cancer Res 2004; 10:4109-17.
53. Zhang J, Zhu ZG, Ji J, Yuan F, Yu YY, Liu BY, Lin YZ. Transcription factor Sp1 expression in gastric cancer and its relationship to long-term prognosis. World J Gastroenterol 2005; 11:2213-7. (Pubitemid 40691326)
54. Jiang NY, Woda BA, Banner BF, Whalen GF, Dresser KA, Lu D. Sp1, a new biomarker that identifies a subset of aggressive pancreatic ductal adenocarcinoma. Cancer Epidemiol Biomarkers Prev 2008; 17:1648-52.
55. Wierstra I. Sp1: emerging roles - beyond constitutive activation of TATA-less housekeeping genes. Biochem Biophys Res Commun 2008; 372:1-13.
56. Necela BM, Su W, Thompson EA. Peroxisome proliferator-activated receptor gamma downregulates follistatin in intestinal epithelial cells through SP1. J Biol Chem 2008; 283:29784-94.
57. Hsu MC, Huang CC, Chang HC, Hu TH, Hung WC. Overexpression of Jab1 in hepatocellular carcinoma and its inhibition by peroxisome proliferator-activated receptor{gamma} ligands in vitro and in vivo. Clin Cancer Res 2008; 14:4045-52.
58. Halasi M, Gartel AL. A novel mode of FoxM1 regulation: positive auto-regulatory loop. Cell Cycle 2009; 8:1966-7.
59. Ondrey F. Peroxisome proliferator-activated receptor gamma pathway targeting in carcinogenesis: implications for chemoprevention. Clin Cancer Res 2009; 15:2-8.
60. Albertini V, Jain A, Vignati S, Napoli S, Rinaldi A, Kwee I, et al. Novel GC-rich DNA-binding compound produced by a genetically engineered mutant of the mithramycin producer Streptomyces argillaceus exhibits improved transcriptional repressor activity: implications for cancer therapy. Nucleic Acids Res 2006; 34:1721-34.
61. Lee TJ, Jung EM, Lee JT, Kim S, Park JW, Choi KS, Kwon TK. Mithramycin A sensitizes cancer cells to TRAIL-mediated apoptosis by downregulation of XIAP gene promoter through Sp1 sites. Mol Cancer Ther 2006; 5:2737-46.
62. Phillips A, Darley M, Blaydes JP. GC-selective DNA-binding antibiotic, mithramycin A, reveals multiple points of control in the regulation of Hdm2 protein synthesis. Oncogene 2006; 25:4183-93.
63. Wang L, Guan X, Zhang J, Jia Z, Wei D, Li Q, et al. Targeted inhibition of Sp1-mediated transcription for antiangiogenic therapy of metastatic human gastric cancer in orthotopic nude mouse models. Int J Oncol 2008; 33:161-7.
64. Yang TP, Chiou HL, Maa MC, Wang CJ. Mithramycin inhibits human epithelial carcinoma cell proliferation and migration involving downregulation of Eps8 expression. Chemico-biological interactions 2009.
65. Yuan P, Wang L, Wei D, Zhang J, Jia Z, Li Q, et al. Therapeutic inhibition of Sp1 expression in growing tumors by mithramycin a correlates directly with potent antiangiogenic effects on human pancreatic cancer. Cancer 2007; 110:2682-90.
66. Adami GR, Ye H. Future roles for FoxM1 inhibitors in cancer treatments. Future Oncol 2007; 3:1-3.
67. Pandit B, Halasi M, Gartel AL. p53 negatively regulates expression of FoxM1. Cell Cycle 2009; 8:3425-7.
68. Barsotti AM, Prives C. Pro-proliferative FoxM1 is a target of p53-mediated repression. Oncogene 2009.
69. Bhat UG, Halasi M, Gartel AL. Thiazole antibiotics target FoxM1 and induce apoptosis in human cancer cells. PLoS ONE 2009; 4:5592.