FoxM1 overexpression promotes epithelial-mesenchymal transition and metastasis of hepatocellular carcinoma

World Journal of Gastroenterology

Volumn 21, Issue 1, 2015, Pages 196-213

  Meng, Fan Di ^a   Wei, Ji Chao ^a   Qu, Kai ^a   Wang, Zhi Xin ^a   Wu, Qi Fei ^a   Tai, Ming Hui ^a   Liu, Hao Chen ^a   Zhang, Rui Yao ^a   Liu, Chang ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

E cadherin; Epithelial mesenchymal transition; Forkhead box protein M1; Hepatocellular carcinoma; Snail homolog 1

Indexed keywords

FORKHEAD BOX PROTEIN M1; PROTEIN; SCATTER FACTOR; SMALL INTERFERING RNA; SNAIL HOMOLOGUE 1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; CADHERIN; CDH1 PROTEIN, HUMAN; FORKHEAD TRANSCRIPTION FACTOR; FOXM1 PROTEIN, HUMAN; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ADULT; ARTICLE; CANCER CELL LINE; CANCER RECURRENCE; CELL MIGRATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORRELATION ANALYSIS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KAPLAN MEIER METHOD; LIVER CELL CARCINOMA; LUCIFERASE ASSAY; MALE; METASTASIS; MIDDLE AGED; OVERALL SURVIVAL; PLASMID; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STATISTICAL ANALYSIS; STRUCTURE ANALYSIS; TISSUE MICROARRAY; TUMOR INVASION; TUMOR VOLUME; WESTERN BLOTTING; CANCER STAGING; CARCINOMA, HEPATOCELLULAR; CASE CONTROL STUDY; CELL MOTION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HEPG2 CELL LINE; LIVER NEOPLASMS; LIVER RESECTION; METABOLISM; MORTALITY; PATHOLOGY; RNA INTERFERENCE; SECONDARY; TIME; TREATMENT OUTCOME; TUMOR RECURRENCE; UPREGULATION;

CADHERINS; CARCINOMA, HEPATOCELLULAR; CASE-CONTROL STUDIES; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HEPATECTOMY; HUMANS; KAPLAN-MEIER ESTIMATE; LIVER NEOPLASMS; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM RECURRENCE, LOCAL; NEOPLASM STAGING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; TREATMENT OUTCOME; UP-REGULATION;

EID: 84920869453     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v21.i1.196     Document Type: Article

References (36)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90 [PMID: 21296855 DOI: 10.3322/caac.20107]
2. Nordenstedt H, White DL, El-Serag HB. The changing pattern of epidemiology in hepatocellular carcinoma. Dig Liver Dis 2010; 42 Suppl 3: S206-S214 [PMID: 20547305 DOI: 10.1016/S1590-8658(10)60507-5]
3. Bruix J, Gores GJ, Mazzaferro V. Hepatocellular carcinoma: clinical frontiers and perspectives. Gut 2014; 63 : 844-855 [PMID: 24531850 DOI: 10.1136/gutjnl-2013-306627]
4. Tang ZY, Ye SL, Liu YK, Qin LX, Sun HC, Ye QH, Wang L, Zhou J, Qiu SJ, Li Y, Ji XN, Liu H, Xia JL, Wu ZQ, Fan J, Ma ZC, Zhou XD, Lin ZY, Liu KD. A decade's studies on metastasis of hepatocellular carcinoma. J Cancer Res Clin Oncol 2004; 130: 187-196 [PMID: 14685850 DOI: 10.1007/s00432-003-0511-1]
5. Lee SC, Tan HT, Chung MC. Prognostic biomarkers for prediction of recurrence of hepatocellular carcinoma: current status and future prospects. World J Gastroenterol 2014; 20 : 3112-3124 [PMID: 24696598 DOI: 10.3748/wjg.v20.i12.3112]
6. Tung-Ping Poon R, Fan ST, Wong J. Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg 2000; 232 : 10-24 [PMID: 10862190]
7. Rodríguez-Perálvarez M, Luong TV, Andreana L, Meyer T, Dhillon AP, Burroughs AK. A systematic review of microvascular invasion in hepatocellular carcinoma: diagnostic and prognostic variability. Ann Surg Oncol 2013; 20: 325-339 [PMID: 23149850 DOI: 10.1245/s10434-012-2513-1]
8. Toyosaka A, Okamoto E, Mitsunobu M, Oriyama T, Nakao N, Miura K. Intrahepatic metastases in hepatocellular carcinoma: evidence for spread via the portal vein as an efferent vessel. Am J Gastroenterol 1996; 91: 1610-1615 [PMID: 8759671]
9. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004; 117 : 927-939 [PMID: 15210113 DOI: 10.1016/j.cell.2004.06.006]
10. Hirohashi S, Kanai Y. Cell adhesion system and human cancer morphogenesis. Cancer Sci 2003; 94: 575-581 [PMID: 12841864 DOI: 10.1111/j.1349-7006]
11. Sugimachi K, Taguchi K, Aishima S, Tanaka S, Shimada M, Kajiyama K, Sugimachi K, Tsuneyoshi M. Altered expression of beta-catenin without genetic mutation in intrahepatic cholangiocarcinoma. Mod Pathol 2001; 14: 900-905 [PMID: 11557787]
12. Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, McAllister F, Reichert M, Beatty GL, Rustgi AK, Vonderheide RH, Leach SD, Stanger BZ. EMT and dissemination precede pancreatic tumor formation. Cell 2012; 148: 349-361 [PMID: 22265420 DOI: 10.1016/j.cell.2011.11.025]
13. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007; 7: 415-428 [PMID: 17508028 DOI: 10.1038/nrc2131]
14. Nagai T, Arao T, Furuta K, Sakai K, Kudo K, Kaneda H, Tamura D, Aomatsu K, Kimura H, Fujita Y, Matsumoto K, Saijo N, Kudo M, Nishio K. Sorafenib inhibits the hepatocyte growth factor-mediated epithelial mesenchymal transition in hepatocellular carcinoma. Mol Cancer Ther 2011; 10: 169-177 [PMID: 21220499 DOI: 10.1158/1535-7163]
15. Peinado H, Portillo F, Cano A. Transcriptional regulation of cadherins during development and carcinogenesis. Int J Dev Biol 2004; 48 : 365-375 [PMID: 15349812 DOI: 10.1387/ijdb.041794hp]
16. Nieto MA. The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 2002; 3 : 155-166 [PMID: 11994736 DOI: 10.1038/nrm757]
17. Carlsson P, Mahlapuu M. Forkhead transcription factors: key players in development and metabolism. Dev Biol 2002; 250: 1-23 [PMID: 12297093 DOI: 10.1006/dbio.2002.0780]
18. Kaestner KH, Knochel W, Martinez DE. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev 2000; 14: 142-146 [PMID: 10702024 DOI: 10.1101/gad.14.2.142]
19. Laoukili J, Stahl M, Medema RH. FoxM1: at the crossroads of ageing and cancer. Biochim Biophys Acta 2007; 1775: 92-102 [PMID: 17014965 DOI: 10.1016/j.bbcan.2006.08.006]
20. Gartel AL. FoxM1 inhibitors as potential anticancer drugs. Expert Opin Ther Targets 2008; 12: 663-665 [PMID: 18479213 DOI: 10.1517/14728222.12.6.663]
21. Park HJ, Gusarova G, Wang Z, Carr JR, Li J, Kim KH, Qiu J, Park YD, Williamson PR, Hay N, Tyner AL, Lau LF, Costa RH, Raychaudhuri P. Deregulation of FoxM1b leads to tumour metastasis. EMBO Mol Med 2011; 3: 21-34 [PMID: 21204266 DOI: 10.1002/emmm.201000107]
22. Bao B, Wang Z, Ali S, Kong D, Banerjee S, Ahmad A, Li Y, Azmi AS, Miele L, Sarkar FH. Over-expression of FoxM1 leads to epithelial-mesenchymal transition and cancer stem cell phenotype in pancreatic cancer cells. J Cell Biochem 2011; 112: 2296-2306 [PMID: 21503965 DOI: 10.1002/jcb.23150]
23. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010; 60 : 277-300 [PMID: 20610543 DOI: 10.3322/caac.20073]
24. Franco-Chuaire ML, Magda Carolina SC, Chuaire-Noack L. Epithelial-mesenchymal transition (EMT): principles and clinical impact in cancer therapy. Invest Clin 2013; 54: 186-205 [PMID: 23947008]
25. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 2011; 331 : 1559-1564 [PMID: 21436443 DOI: 10.1126/science.1203543]
26. Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013; 19 : 1423-1437 [PMID: 24202395 DOI: 10.1038/nm.3394]
27. Choi C, Helfman DM. The Ras-ERK pathway modulates cytoskeleton organization, cell motility and lung metastasis signature genes in MDA-MB-231 LM2. Oncogene 2014; 33: 3668-3676 [PMID: 23995792 DOI: 10.1038/onc.2013.341]
28. Hugo H, Ackland ML, Blick T, Lawrence MG, Clements JA, Williams ED, Thompson EW. Epithelial - mesenchymal and mesenchymal - epithelial transitions in carcinoma progression. J Cell Physiol 2007; 213: 374-383 [PMID: 17680632 DOI: 10.1002/jcp.21223]
29. Huber MA, Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 2005; 17: 548-558 [PMID: 16098727 DOI: 10.1016/j.ceb.2005.08.001]
30. Zheng H, Kang Y. Multilayer control of the EMT master regulators. Oncogene 2014; 33: 1755-1763 [PMID: 23604123 DOI: 10.1038/onc.2013.128]
31. Cañadas I, Rojo F, Taus Á, Arpí O, Arumí-Uría M, Pijuan L, Menéndez S, Zazo S, Dómine M, Salido M, Mojal S, García de Herreros A, Rovira A, Albanell J, Arriola E. Targeting epithelial-to-mesenchymal transition with Met inhibitors reverts chemoresistance in small cell lung cancer. Clin Cancer Res 2014; 20 : 938-950 [PMID: 24284055 DOI: 10.1158/1078-0432.CCR-13-1330]
32. Wierstra I. FOXM1 (Forkhead box M1) in tumorigenesis: overexpression in human cancer, implication in tumorigenesis, oncogenic functions, tumor-suppressive properties, and target of anticancer therapy. Adv Cancer Res 2013; 119: 191-419 [PMID: 23870513 DOI: 10.1016/B978-0-12-407190-2.00016-2]
33. Balli D, Ustiyan V, Zhang Y, Wang IC, Masino AJ, Ren X, Whitsett JA, Kalinichenko VV, Kalin TV. Foxm1 transcription factor is required for lung fibrosis and epithelial-tomesenchymal transition. EMBO J 2013; 32: 231-244 [PMID: 23288041 DOI: 10.1038/emboj.2012.336]
34. Yang C, Chen H, Tan G, Gao W, Cheng L, Jiang X, Yu L, Tan Y. FOXM1 promotes the epithelial to mesenchymal transition by stimulating the transcription of Slug in human breast cancer. Cancer Lett 2013; 340: 104-112 [PMID: 23856032 DOI: 10.1016/j.canlet.2013.07.004]
35. Ahmad A, Wang Z, Kong D, Ali S, Li Y, Banerjee S, Ali R, Sarkar FH. FoxM1 down-regulation leads to inhibition of proliferation, migration and invasion of breast cancer cells through the modulation of extra-cellular matrix degrading factors. Breast Cancer Res Treat 2010; 122: 337-346 [PMID: 19813088 DOI: 10.1007/s10549-009-0572-1]
36. Wang X, Quail E, Hung NJ, Tan Y, Ye H, Costa RH. 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 2001; 98: 11468-11473 [PMID: 11572993 DOI: 10.1073/pnas.201360898]