FOXM1 confers to epithelial-mesenchymal transition, stemness and chemoresistance in epithelial ovarian carcinoma cells

Oncotarget

Volumn 6, Issue 4, 2015, Pages 2349-2365

  Chiu, Wen Tai ^a   Huang, Yu Fang ^b   Tsai, Huei Yu ^b   Chen, Chien Chin ^c,d   Chang, Chang Hwa ^a   Huang, Soon Cen ^e   Hsu, Keng Fu ^b   Chou, Cheng Yang ^b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^c CHIA YI CHRISTIAN HOSPITAL   (Taiwan)

^d CHIA NAN UNIVERSITY OF PHARMACY AND SCIENCE   (Taiwan)

^e CHI MEI MEDICAL CENTER   (Taiwan)

Author keywords

Chemoresistance; FOXM1; Ovarian cancer; Stemness; CATENIN

Indexed keywords

BETA CATENIN; CARBOPLATIN; CISPLATIN; CYCLOPHOSPHAMIDE; FORKHEAD TRANSCRIPTION FACTOR; PACLITAXEL; THIOSTREPTON; TRANSCRIPTION FACTOR FOXM1; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; FORKHEAD BOX PROTEIN M1; FOXM1 PROTEIN, HUMAN; TUMOR MARKER;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER PROGNOSIS; CANCER RESISTANCE; CELL INVASION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; DRUG SENSITIVITY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; OVARIAN CANCER CELL LINE; OVARY CARCINOMA; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; TUMOR GROWTH; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER STEM CELL; CELL PROLIFERATION; DISEASE COURSE; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; NEOPLASMS, GLANDULAR AND EPITHELIAL; NONOBESE DIABETIC MOUSE; OVARIAN NEOPLASMS; PATHOLOGY; RNA INTERFERENCE; SCID MOUSE; SURVIVAL ANALYSIS; TUMOR CELL LINE; TUMOR VOLUME; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FORKHEAD BOX PROTEIN M1; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE, INBRED NOD; MICE, SCID; NEOPLASMS, GLANDULAR AND EPITHELIAL; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; PACLITAXEL; RNA INTERFERENCE; SURVIVAL ANALYSIS; THIOSTREPTON; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84923052543     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2957     Document Type: Article

References (49)

1. Hunn J and Rodriguez GC. Ovarian cancer: epitology, risk factors, and epidemiology. Clin Obstet Gynecol. 2012; 55(1):3-23.
2. Wernyj RP and Morin PJ. Molecular mechanisms of platinum resistance: still searching for the Achilles' heel. Drug Resist Updat. 2004; 7(4-5):227-232.
3. Shafee N, Smith CR, Wei S, Kim Y, Mills GB, Hortobagyi GN, Stanbridge EJ and Lee EY. Cancer stem cells contribute to cisplatin resistance in Brca1/p53-mediated mouse mammary tumors. Cancer Res. 2008; 68(9):3243-3250.
4. Zhang Q, Shi S, Yen Y, Brown J, Ta JQ and Le AD. A subpopulation of CD 133+ cancer stem-like cells characterized in human oral squamous cell carcinoma confer resistance to chemotherapy. Cancer Lett. 2010; 289(2):151-160.
5. Crea F, Danesi R and Farrar WL. Cancer stem cell epigenetics and chemoresistance. Epigenomics. 2009; 1(1):63-79.
6. Ahmed N, Abubaker K, Findlay J and Quinn M. Cancerous ovarian stem cells: obscure targets for therapy but relevant to chemoresistance. J Cell Biochem. 2013; 114(1):21-34.
7. Hunag Y and Sadée W. Membrane transporters and channels in chemoresistance and-sensitivity of tumor cells. Cancer Lett. 2006; 239(2):168-182.
8. Korver W, Roose J, Heinen K, Weghuis DO, de Bruijn D, van Kessel AG and Clevers H. The human TRIDENT/HFH-11/FKHL16 gene: structure, localization, and promoter characterization. Genomics. 1997:46(3):435-442.
9. Wang IC, Chen YJ, Hughes D, Petrovic V, Major ML, Park HJ, Tan Y, Ackerson T and Costa RH. Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-1) ubiquitin ligase. Mol Cell Biol. 2005; 25(24):10875-10894.
10. Petrovic V, Costa RH, Lau LF, Raychaudhuri P and Tyner AL. FoxM1 regulates growth factor-induced expression of kinase-interacting stathmin (KIS) to promote cell cycle progression. J Biol Chem. 2008; 283(1):453-460.
11. Leung TW, Lin SS, Tsang AC, Tong CS, Ching JC, Leung WY, Gimlich R, Wong GG and Yao KM. Over-expression of FoxM1 stimulates cyclin B1 expression. FEBS Lett. 2001; 507(1):59-66.
12. Madureira PA, Varshochi R, Constantinidou D, Francis RE, Coombes RC, Yao KM and Lam EW. The Forkhead box M1 protein regulates the transcription of the estrogen receptor alpha in breast cancer cells. J Biol Chem. 2006; 281(35):25167-25176.
13. Wang Z, Banerjee S, Kong D, Li Y and Sarkar FH. Down-regulation of Forkhead Box M1 transcription factor leads to the inhibition of invasion and angiogenesis of pancreatic cancer cells. Cancer Res. 2007; 67(17):8293-8300.
14. Tan Y, Raychaudhuri P and Costa RH. Chk2 mediates stabilization of the FoxM1 transcription factor to stimulate expression of DNA repair genes. Mol Cell Biol. 2007; 27(3):1007-1016.
15. Pilarsky C, Wenzig M, Specht T, Saeger HD and Grützmann R. Identification and validation of commonly overexpressed genes in solid tumors by comparison of microarray data. Neoplasia. 2004; 6(6):744-750.
16. Sakai W, Swisher EM, Karlan BY, Agarwal MK, Higgins J, Friedman C, Villegas E, Jacquemont C, Farrugia DJ, Couch FJ, Urban N and Taniguchi T. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature. 2008; 451(7182):1116-1120.
17. Swisher EM, Sakai W, Karlan BY, Wurz K, Urban N and Taniguchi T. Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance. Cancer Res. 2008; 68(8):2581-2586.
18. Kwok JM, Peck B, Monteiro LJ, Schwenen HD, Millour J, Coombes RC, Myatt SS and Lam EW. FOXM1 confers acquired cisplatin resistance in breast cancer cells. Mol Cancer Res. 2010; 8(1):24-34.
19. Carr JR, Park HJ, Wang Z, Kiefer MM and Raychaudhuri P. FoxM1 mediates resistance to herceptin and paclitaxel. Cancer Res. 2010; 70(12):5054-5063.
20. Karsten SL, Kudo LC, Jackson R, Sabatti C, Kornblum HI and Geschwind DH. Global analysis of gene expression in neural progenitors reveals specific cell-cycle, signaling, and metabolic networks. Dev Biol. 2003; 261(1):165-182.
21. Ahn JI, Lee KH, Shin DM, Shim JW, Kim CM, Kim H, Lee SH and Lee YS. Temporal expression changes during differentiation of neural stem cells derived from mouse embryonic stem cell. J Cell Biochem. 2004; 93(3):563-578.
22. Xie Z, Tan G, Ding M, Dong D, Chen T, Meng X and Tan Y. FoxM1 transcription factor is required for maintenance of pluripotency of P19 embryonal carcinoma cells. Nucleic Acids Res. 2010; 38(22):8027-8038.
23. Gemenetzidis E, Elena-Costea D, Parkinson EK, Waseem A, Wan H and Teh MT. Induction of human epithelial stem/progenitor expansion by FOXM1. Cancer Res. 2010; 70(22):9515-9526.
24. Wend P, Holland JD and Birchmeier W. Wnt signaling in stem and cancer stem cells. Semin Cell Dev Biol. 2010; 21(8):855-863.
25. Behrens J. Control of beta-catenin signaling in tumor development. Ann NY Acad Sci. 2000; 910(1):21-33.
26. Mirza MK, Sun Y, Zhao YD, Potula HH, Frey RS, Vogel SM, Malik AB and Zhao YY. FoxM1 regulates re-annealing of endothelial adherens junctions through transcriptional control of beta-catenin expression. J Exp Med. 2010; 207(8):1675-1685.
27. Zhang N, Wei P, Gong A, Chiu WT, Lee HT, Colman H, Huang H, Xue J, Liu M, Wang Y, Sawaya R, Xie K, Yung WK, et al. FoxM1 promotes β-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell. 2011; 20(4):427-442.
28. Gartel AL. FoxM1 inhibitors as potential anticancer drugs. Expert Opin Ther Targets. 2008; 12(6):663-665.
29. Kwork JM, Myatt SS, Marson CM, Coombes RC, Constantinidou D and Lam EW. Thiostrepton selectively targets bresat cancer cells through inhibition of forkhead box M1 expression. Mol Cancer Ther. 2008; 7(7):2022-2032.
30. Wang Z, Ahmad A, Li Y, Banerjee S, Kong D and Sarkar FH. Forkhead box M1 transcription factor: a novel target for cancer therapy. Cancer Treat Rev. 2010; 36(2):151-156.
31. Cancer Genome Atlas Research Network. Integratd genomic analyses of ovarian carcinoma. Nature. 2011; 474(7353):609-615.
32. Ghosh-Choudhury T, Loomans HA, Wan YW, Liu Z, Hawkins SM and Anderson ML. Hyperactivation of FOXM1 drives ovarian cancer growth and metastasis independent of the G2-M cell cycle checkpoint. Cancer Res. 2013; 73(8 Suppl):Abstract nr 3113.
33. Lok GT, Chan DW, Liu VW, Hui WW, Leung TH, Yao KM and Ngan HY. Aberrant activation of ERK/FOXM1 signaling cascade triggers the cell migration/invasion in ovarian cancer cells. PLoS One. 2011; 6(8):e23790.
34. Sharom FJ. ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics. 2008; 9(1):105-127.
35. Zhang N, Wu X, Yang L, Xiao F, Zhang H, Zhou A, Huang Z and Huang S. FoxM1 inhibition sensitizes resistant glioblastoma cells to temozolomide by downregulating the expression of DNA-repair gene Rad51. Clin Cancer Res. 2012; 18(21):5961-5971.
36. Khongkow P, Karunarathna U, Khongkow M, Gong C, Gomes AR, Yagüe E, Monteiro LJ, Kongsema M, Zona S, Man EP, Tsang JW, Coombes RC, Wu J, et al. FoxM1 targets NBS1 to regulate DNA damage-induced senescence and epirubicin resistance. Oncogene. 2014; 33(32):4144-4155.
37. Monteiro LJ, Khongkow P, Khongkow M, Morris JR, Man C, Weekes D, Koo CY, Gomes AR, Pinto PH, Varghese V, Kenny LM, Coombes RC, Freire R, et al. The Forkhead Box M1 protein regulates BRIP1 expression and DNA damage repair in epirubicin treatment. Oncogenes. 2013; 32(39):4634-4645.
38. Wang Z, Li Y, Ahmad A, Banerjee S, Azmi AS, Kong D and Sarkar FH. Pancreatic cancer: understanding and overcoming chemoresistance. Nat Rev Gastroenterol Hepatol. 2011; 8(1):27-33.
39. Dave B, Mittal V, Tan NM and Chang JC. Epithelial-mesenchymal transition, cancer stem cells and treatment resistance. Breast Cancer Res. 2012; 14(1): 202.
40. Arend RC, Londoño-Joshi AI, Straughn JM Jr and Buchsbaum DJ. The Wnt/β-catenin pathway in ovarian cancer: a review. Gynecol Oncol. 2013; 131(3):772-779.
41. Xue J, Lin X, Chiu WT, Chen YH, Yu G, Liu M, Feng XH, Sawaya R, Medema RH, Hung MC and Huang S. Sustained activation of SMAD3/SMAD4 by FOXM1 promoted TGF-β-dependent cancer metastasis. J Clin Invest. 2014; 124(2):564-579.
42. Katsumata N, Yasuda M, Takahashi F, Isonishi S, Jobo T, Aoki D, Tsuda H, Sugiyama T, Kodama S, Kimura E, Ochiai K and Noda K. Dose-dense paclitaxel once a week in combination with carboplatin every 3 weeks for advanced ovarian cancer: a phase 3, open-label, randomised controlled trial. Lancet. 2009; 374(9698):1331-1338.
43. Markman M, Liu PY, Moon J, Monk BJ, Copeland L, Wilczynski S and Alberts D. Impact on survival of 12 versus 3 monthly cycles of paclitaxel (175 mg/m2) administered to patients with advanced ovarian cancer who attained a complete response to primary platinum-paclitaxel: follow-up of a Southwest Oncology Group and Gynecologic Oncology Group phase 3 trial. Gynecol Oncol. 2009; 114(2):195-198.
44. Monk BJ, Dalton H, Farley JH, Chase DM and Benjamin I. Antiangiogenic agents as a maintenance strategy for advanced epithelial ovarian cancer. Crit Rev Oncol Hematol. 2013; 86(2):161-175.
45. Liu M, Dai B, Kang SH, Ban K, Huang FJ, Lang FF, Aldape KD, Xie TX, Pelloski CE, Xie K, Sawaya R and Huang S. FoxM1B is overexpressed in human glioblastomas and critically regulates the tumorigenicity of glioma cells. Cancer Res. 2006; 66(7):3593-3602.
46. Dai B, Kang SH, Gong W, Liu M, Aldape KD, Sawaya R and Huang S. Aberrant FoxM1B expression increases matrix metalloproteinase-2 transcription and enhances the invasion of glioma cells. Oncogene. 2007; 26(42):6212-6219.
47. Su HY, Lai HC, Lin YW, Liu CY, Chen CK, Chou YC, Lin SP, Lin WC, Lee HY and Yu MH. Epigenetic silencing of SFRP5 is related to malignant phenotype and chemoresistance of ovarian cancer through Wnt signaling pathway. Int J Cancer. 2010; 127(3):555-567.
48. Ledermann JA and Kristeleit RS. Optimal treatment for relapsing ovarian cancer. Ann Oncol. 2010; 21(Suppl 7):vii218-222.
49. Sehouli J, Alfaro V and Gonzalez-Martin A. Trabectedin plus pegylated liposomal doxorubicin in the treatment of patients with partially platinum-sensitive ovarian cancer: current evidence and future perspectives. Ann Oncol. 2012; 23(3):556-562.