FOXM1c promotes pancreatic cancer epithelial-to-mesenchymal transition and metastasis via upregulation of expression of the urokinase plasminogen activator system

Clinical Cancer Research

Volumn 20, Issue 6, 2014, Pages 1477-1488

  Huang, Chen ^a,b   Xie, Dacheng ^a   Cui, Jiujie ^a,e   Li, Qi ^c,d   Gao, Yong ^c,d   Xie, Keping ^e  

^a SHANGHAI FIRST PEOPLE S HOSPITAL   (China)

^b General Surgery   (China)

^c Departments of Oncology Shanghai Jiaotong University Affiliated First People's Hospital ^*  (China)

^d TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN FOXM1; PROTEIN FOXM1C; SMALL INTERFERING RNA; TUMOR PROTEIN; UNCLASSIFIED DRUG; UROKINASE; UROKINASE RECEPTOR; FORKHEAD TRANSCRIPTION FACTOR; FOXM1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER PROGNOSIS; CANCER TISSUE; CLINICAL FEATURE; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FOXM1 GENE; FOXM1B GENE; FOXM1C GENE; GENE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INHIBITION KINETICS; METASTASIS; MOLECULAR MODEL; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR GENE; TUMOR INVASION; UPAR GENE; UPREGULATION; ADENOCARCINOMA; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; METABOLISM; PANCREAS TUMOR; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE MICROARRAY;

ADENOCARCINOMA; ANIMALS; CHROMATIN IMMUNOPRECIPITATION; EPITHELIAL-MESENCHYMAL TRANSITION; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOHISTOCHEMISTRY; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PANCREATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TISSUE ARRAY ANALYSIS; TRANSFECTION; UP-REGULATION;

EID: 84893146306     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-2311     Document Type: Article

References (48)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010;60:277-300.
2. Nieto J, Grossbard ML, Kozuch P. Metastatic pancreatic cancer 2008: is the glass less empty. Oncologist 2008;13:562-76.
3. Pliarchopoulou K, Pectasides D. Pancreatic cancer: current and future treatment strategies. Cancer Treat Rev 2009;35:431-6.
4. Stathis A, Moore MJ. Advanced pancreatic carcinoma: current treatment and future challenges. Nat Rev Clin Oncol 2010;7:163-72.
5. Clark KL, Halay ED, Lai E, Burley SK. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature 1993;364:412-20.
6. Korver W, Roose J, Clevers H. The winged-helix transcription factor Trident is expressed in cycling cells. Nucleic Acids Res 1997;25: 1715-9.
7. 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.
8. Yao KM, Sha M, Lu Z, Wong GG. Molecular analysis of a novel winged helix protein, WIN. Expression pattern, DNA binding property, and alternative splicing within the DNA binding domain. J Biol Chem 1997;272:19827-36.
9. Raychaudhuri P, Park HJ. FOXM1: a master regulator of tumor metastasis. Cancer Res 2011;71:4329-33.
10. Koo CY, Muir KW, Lam EW. FOXM1: from cancer initiation to progression and treatment. Biochim Biophys Acta 2012;1819:28-37.
11. 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.
12. Chan DW, Yu SY, Chiu PM, Yao KM, Liu VW, Cheung AN, et al. Over-expression of FOXM1 transcription factor is associated with cervical cancer progression and pathogenesis. J Pathol 2008;215: 245-52.
13. Li Q, Zhang N, Jia Z, Le X, Dai B, Wei D, et al. Critical role and regulation of transcription factor FOXM1 in human gastric cancer angiogenesis and progression. Cancer Res 2009;69:3501-9.
14. Liu M, Dai B, Kang SH, Ban K, Huang FJ, Lang FF, et al. FOXM1B is overexpressed in human glioblastomas and critically regulates the tumorigenicity of glioma cells. Cancer Res 2006;66:3593-602.
15. Priller M, Poschl J, Abrao L, von Bueren AO, Cho YJ, Rutkowski S, et al. Expression of FOXM1 is required for the proliferation of medulloblastoma cells and indicates worse survival of patients. Clin Cancer Res 2011;17:6791-801.
16. Wang Z, Banerjee S, Kong D, Li Y, Sarkar FH. Down-regulation of Forkhead BoxM1transcription factor leads to the inhibition of invasion and angiogenesis of pancreatic cancer cells. Cancer Res 2007;67: 8293-300.
17. Bao B, Wang Z, Ali S, Kong D, Banerjee S, Ahmad A, et al. Overexpression of FOXM1 leads to epithelial-mesenchymal transition and cancer stem cell phenotype in pancreatic cancer cells. J Cell Biochem 2011;112:2296-306.
18. Huang C, Qiu Z, Wang L, Peng Z, Jia Z, Logsdon CD, et al. A novel FOXM1-Caveolin signaling pathway promotes pancreatic cancer invasion and metastasis. Cancer Res 2012;72:655-65.
19. Mazar AP, Henkin J, Goldfarb RH. The urokinase plasminogen activator system in cancer: implications for tumor angiogenesis and metastasis. Angiogenesis 1999;3:15-32.
20. Ulisse S, Baldini E, Sorrenti S, D'Armiento M. The urokinase plasminogen activator system: a target for anti-cancer therapy. Curr Cancer Drug Targets 2009;9:32-71.
21. Jo M, Lester RD, Montel V, Eastman B, Takimoto S, Gonias SL. Reversibility of epithelial-mesenchymal transition (EMT) induced in breast cancer cells by activation of urokinase receptor-dependent cell signaling. J Biol Chem 2009;284:22825-33.
22. de Bock CE, Wang Y. Clinical significance of urokinase-type plasminogen activator receptor (uPAR) expression in cancer. Med Res Rev 2004;24:13-39.
23. Wang Y. The role and regulation of urokinase-type plasminogen activator receptor gene expression in cancer invasion and metastasis. Med Res Rev 2001;21:146-70.
24. Harvey SR, Hurd TC, Markus G, Martinick MI, Penetrante RM, Tan D, et al. Evaluation of urinary plasminogen activator, its receptor, matrix metalloproteinase-9, and von Willebrand factor in pancreatic cancer. Clin Cancer Res 2003;9:4935-43.
25. Bauer TW, Liu W, Fan F, Camp ER, Yang A, Somcio RJ, et al. Targeting of urokinase plasminogen activator receptor in human pancreatic carcinoma cells inhibits c-Met-And insulin-like growth factor-I receptor-mediated migration and invasion and orthotopic tumor growth in mice. Cancer Res 2005;65:7775-81.
26. Gorantla B, Asuthkar S, Rao JS, Patel J, Gondi CS. Suppression of the uPAR-uPA system retards angiogenesis, invasion, and in vivo tumor development in pancreatic cancer cells. Mol Cancer Res 2011;9:377-89.
27. 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.
28. Huang C, Jiang T, Zhu L, Liu J, Cao J, Huang KJ, et al. STAT3-targeting RNA interference inhibits pancreatic cancer angiogenesis in vitro and in vivo. Int J Oncol 2011;38:1637-44.
29. Zhang Y, Zhang N, Dai B, Liu M, Sawaya R, Xie K, et al. FOXM1B transcriptionally regulates vascular endothelial growth factor expression and promotes the angiogenesis and growth of glioma cells. Cancer Res 2008;68:8733-42.
30. Smith R, Xue A, Gill A, Scarlett C, Saxby A, Clarkson A, et al. High expression of plasminogen activator inhibitor-2 (PAI-2) is a predictor of improved survival in patients with pancreatic adenocarcinoma. World J Surg 2007;31:493-502.
31. Kong X, Li L, Li Z, Le X, Huang C, Jia Z, et al. Dysregulated expression of FOXM1 isoforms drives progression of pancreatic cancer. Cancer Res 2013;73:3987-96.
32. Dai B, Kang SH, Gong W, Liu M, Aldape KD, Sawaya R, et al. Aberrant FOXM1B expression increases matrix metalloproteinase-2 transcription and enhances the invasion of glioma cells. Oncogene 2007;26: 6212-9.
33. Wierstra I, Alves J. FOXM1, a typical proliferation-Associated transcription factor. Biol Chem 2007;388:1257-74.
34. Wang Z, Ahmad A, Li Y, Banerjee S, Kong D, Sarkar FH. Forkhead box M1 transcription factor: a novel target for cancer therapy. Cancer Treat Rev 2010;36:151-6.
35. Laoukili J, Stahl M, Medema RH. FOXM1: at the crossroads of ageing and cancer. Biochim Biophys Acta 2007;1775:92-102.
36. Kalin TV, Ustiyan V, Kalinichenko VV. Multiple faces of FOXM1 transcription factor: lessons from transgenic mouse models. Cell Cycle 2011;10:396-405.
37. Wierstra I, Alves J. FOXM1c is activated by cyclin E/Cdk2, cyclin A/Cdk2, and cyclin A/Cdk1, but repressed by GSK-3alpha. Biochem Biophys Res Commun 2006;348:99-108.
38. Wierstra I. The transcription factor FOXM1c is activated by protein kinase CK2, protein kinase A (PKA), c-Src and Raf-1. Biochem Biophys Res Commun 2011;413:230-5.
39. Wierstra I, Alves J. FOXM1c transactivates the human c-myc promoter directly via the two TATA boxes P1 and P2. FEBS J 2006;273:4645-67.
40. Lok GT, Chan DW, Liu VW, Hui WW, Leung TH, Yao KM, et al. Aberrant activation of ERK/FOXM1 signaling cascade triggers the cell migration/invasion in ovarian cancer cells. PLoS ONE 2011;6:e23790.
41. Prager GW, Breuss JM, Steurer S, Olcaydu D, Mihaly J, Brunner PM, et al. Vascular endothelial growth factor receptor-2-induced initial endothelial cell migration depends on the presence of the urokinase receptor. Circ Res 2004;94:1562-70.
42. Margheri F, Chilla A, Laurenzana A, Serrati S, Mazzanti B, Saccardi R, et al. Endothelial progenitor cell-dependent angiogenesis requires localization of the full-length form of uPAR in caveolae. Blood 2011;118:3743-55.
43. Lester RD, Jo M, Montel V, Takimoto S, Gonias SL. uPAR induces epithelial-mesenchymal transition in hypoxic breast cancer cells. J Cell Biol 2007;178:425-36.
44. Zannetti A, Del VS, Carriero MV, Fonti R, Franco P, Botti G, et al. Coordinate up-regulation of Sp1 DNA-binding activity and urokinase receptor expression in breast carcinoma. Cancer Res 2000;60:1546-51.
45. Shi Q, Le X, Abbruzzese JL, Peng Z, Qian CN, Tang H, et al. Constitutive Sp1 activity is essential for differential constitutive expression of vascular endothelial growth factor in human pancreatic adenocarcinoma. Cancer Res 2001;61:4143-54.
46. Shyu KG, Hsu FL,Wang MJ,Wang BW, Lin S. Hypoxia-inducible factor 1alpha regulates lung adenocarcinoma cell invasion. Exp Cell Res 2007;313:1181-91.
47. Chang Q, Qin R, Huang T, Gao J, Feng Y. Effect of antisense hypoxiainducible factor 1alpha on progression, metastasis and chemosensitivity of pancreatic cancer. Pancreas 2006;32:297-305.
48. Huang C, Xie K. Crosstalk of Sp1 and Stat3 signaling in pancreatic cancer pathogenesis. Cytokine Growth Factor Rev 2012;23:25-35.