HIF-1α promotes epithelial-mesenchymal transition and metastasis through direct regulation of ZEB1 in colorectal cancer

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Zhang, Wenjing ^a,b   Shi, Xinpeng ^a   Peng, Ying ^a   Wu, Meiyan ^a   Zhang, Pei ^a   Xie, Ruyi ^a   Wu, Yao ^a   Yan, Qingqing ^a   Liu, Side ^a   Wang, Jide ^a  

^a FIRST MILITARY MEDICAL UNIVERSITY   (China)

^b KUNMING UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRIDAE;

CADHERIN; HOMEODOMAIN PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZEB1; VIMENTIN; ZEB1 PROTEIN, HUMAN;

ANIMAL; COLORECTAL TUMOR; DNA RESPONSIVE ELEMENT; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENETICS; HCT 116 CELL LINE; HT-29 CELL LINE; HUMAN; LIVER TUMOR; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PATHOLOGY; SECONDARY;

ANIMALS; BASE SEQUENCE; CADHERINS; COLORECTAL NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HOMEODOMAIN PROTEINS; HT29 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER NEOPLASMS; MICE, NUDE; MOLECULAR SEQUENCE DATA; RESPONSE ELEMENTS; TRANSCRIPTION FACTORS; VIMENTIN; ZINC FINGER E-BOX-BINDING HOMEOBOX 1;

EID: 84936804324     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129603     Document Type: Article

References (32)

1. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009, 119:1420-1428. doi: 10.1172/JCI39104 PMID: 19487818
2. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 2009, 119:1429-1437. doi: 10.1172/JCI36183 PMID: 19487819
3. Le Bras GF, Taubenslag KJ, Andl CD. The regulation of cell-cell adhesion during epithelial-mesenchymal transition, motility and tumor progression. Cell Adh Migr 2012, 6:365-373. doi: 10.4161/cam.21326 PMID: 22796940
4. Higgins DF, Kimura K, Bernhardt WM, Shrimanker N, Akai Y, Hohenstein B, et al. Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 2007, 117:3810-3820. PMID: 18037992
5. Choi JY, Jang YS, Min SY, Song JY. Overexpression of MMP-9 and HIF-1alpha in Breast Cancer Cells under Hypoxic Conditions. J Breast Cancer 2011, 14:88-95. doi: 10.4048/jbc.2011.14.2.88 PMID: 21847402
6. Zhang L, Huang G, Li X, Zhang Y, Jiang Y, Shen J, et al. Hypoxia induces epithelial-mesenchymal transition via activation of SNAI1 by hypoxia-inducible factor -1alpha in hepatocellular carcinoma. BMC Cancer 2013, 13:108. doi: 10.1186/1471-2407-13-108 PMID: 23496980
7. Kaidi A, Williams AC, Paraskeva C. Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nat Cell Biol 2007, 9:210-217. PMID: 17220880
8. Spaderna S, Schmalhofer O, Wahlbuhl M, Dimmler A, Bauer K, Sultan A, et al. The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res 2008, 68:537-544. doi: 10.1158/0008-5472.CAN-07-5682 PMID: 18199550
9. Xiong H, Hong J, Du W, Lin YW, Ren LL, Wang YC, et al. Roles of STAT3 and ZEB1 proteins in E-cadherin down-regulation and human colorectal cancer epithelial-mesenchymal transition. J Biol Chem 2012, 287:5819-5832. doi: 10.1074/jbc.M111.295964 PMID: 22205702
10. Romero-Perez L, Lopez-Garcia MA, Diaz-Martin J, Biscuola M, Castilla MA, Tafe LJ, et al.ZEB1 overexpression associated with E-cadherin and microRNA-200 downregulation is characteristic of undifferentiated endometrial carcinoma. Mod Pathol 2013, 26:1514-1524. doi: 10.1038/modpathol.2013.93 PMID: 23743934
11. Barriga EH, Maxwell PH, Reyes AE, Mayor R. The hypoxia factor Hif-1alpha controls neural crest chemotaxis and epithelial to mesenchymal transition. J Cell Biol 2013, 201:759-776. doi: 10.1083/jcb.201212100 PMID: 23712262
12. Zhang W, Wu Y, Yan Q, Ma F, Shi X, Zhao Y, et al.Deferoxamine enhances cell migration and invasion through promotion of HIF-1alpha expression and epithelial-mesenchymal transition in colorectal cancer. Oncol Rep 2014, 31:111-116. doi: 10.3892/or.2013.2828 PMID: 24173124
13. Giaccia A, Siim BG, Johnson RS. HIF-1 as a target for drug development. Nat Rev Drug Discov 2003, 2:803-811. PMID: 14526383
14. Zhou Q, Chen T, Ibe JC, Raj JU, Zhou G. Loss of either hypoxia inducible factor 1 or 2 promotes lung cancer cell colonization. Cell Cycle 2011, 10:2233-2234. PMID: 21610325
15. Imamura T, Kikuchi H, Herraiz MT, Park DY, Mizukami Y, Mino-Kenduson M, et al.HIF-1alpha and HIF-2alpha have divergent roles in colon cancer. Int J Cancer 2009, 124:763-771. doi: 10.1002/ijc.24032 PMID: 19030186
16. Chien W, Lee KL, Ding LW, Wuensche P, Kato H, Doan NB, et al.PIAS4 is an activator of hypoxia signalling via VHL suppression during growth of pancreatic cancer cells. Br J Cancer 2013, 109:1795-1804. doi: 10.1038/bjc.2013.531 PMID: 24002598
17. Imai T, Horiuchi A, Wang C, Oka K, Ohira S, Nikaido T, et al.Hypoxia attenuates the expression of E-cadherin via up-regulation of SNAIL in ovarian carcinoma cells. Am J Pathol 2003, 163:1437-1447. PMID: 14507651
18. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, Liu CJ, et al.Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 2008, 10:295-305. doi: 10.1038/ncb1691 PMID: 18297062
19. Krishnamachary B, Zagzag D, Nagasawa H, Rainey K, Okuyama H, Baek JH, et al.Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal cell carcinoma mediated by TCF3, ZFHX1A, and ZFHX1B. Cancer Res 2006, 66:2725-2731. PMID: 16510593
20. Eger A, Aigner K, Sonderegger S, Dampier B, Oehler S, Schreiber M, et al.DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 2005, 24:2375-2385. PMID: 15674322
21. Singh AB, Sharma A, Smith JJ, Krishnan M, Chen X, Eschrich S, et al.Claudin-1 up-regulates the repressor ZEB-1 to inhibit E-cadherin expression in colon cancer cells. Gastroenterology 2011, 141:2140-2153. doi: 10.1053/j.gastro.2011.08.038 PMID: 21878201
22. Shah PP, Kakar SS. Pituitary tumor transforming gene induces epithelial to mesenchymal transition by regulation of Twist, Snail, Slug, and E-cadherin. Cancer Lett 2011, 311:66-76. doi: 10.1016/j.canlet.2011.06.033 PMID: 21839581
23. Luo D, Wang J, Li J, Post M. Mouse snail is a target gene for HIF. Mol Cancer Res 2011, 9:234-245. doi: 10.1158/1541-7786.MCR-10-0214 PMID: 21257819
24. Tsai CC, Chen YJ, Yew TL, Chen LL, Wang JY, Chiu CH, et al.Hypoxia inhibits senescence and maintains mesenchymal stem cell properties through down-regulation of E2A-p21 by HIF-TWIST. Blood 2011, 117:459-469. doi: 10.1182/blood-2010-05-287508 PMID: 20952688
25. Espada J, Peinado H, Lopez-Serra L, Setien F, Lopez-Serra P, Portela A, et al.Regulation of SNAIL1 and E-cadherin function by DNMT1 in a DNA methylation-independent context. Nucleic Acids Res 2011, 39:9194-9205. doi: 10.1093/nar/gkr658 PMID: 21846773
26. Zhang W, Jiang B, Guo Z, Sardet C, Zou B, Lam CS, et al. Four-and-a-half LIM protein 2 promotes invasive potential and epithelial-mesenchymal transition in colon cancer. Carcinogenesis 2010, 31:1220-1229. doi: 10.1093/carcin/bgq094 PMID: 20460358
27. Zhang W, Guo Z, Jiang B, Niu L, Xia G, Wang X, et al.Identification of a functional p53 responsive element within the promoter of XAF1 gene in gastrointestinal cancer cells. Int J Oncol 2010, 36:1031-1037. PMID: 20198350
28. Guo Z, Zhang W, Xia G, Niu L, Zhang Y, Wang X, et al.Sp1 upregulates the four and half lim 2 (FHL2) expression in gastrointestinal cancers through transcription regulation. Mol Carcinog 2010, 49:826-836. doi: 10.1002/mc.20659 PMID: 20607723
29. Zhang W, Wang J, Zou B, Sardet C, Li J, Lam CS, et al. Four and a half LIM protein 2 (FHL2) negatively regulates the transcription of E-cadherin through interaction with Snail1. Eur J Cancer 2011, 47:121-130. doi: 10.1016/j.ejca.2010.07.045 PMID: 20801642
30. Jeong JS, Lee SW, Hong SH, Lee YJ, Jung HI, Cho KS, et al. Antitumor effects of systemically delivered adenovirus harboring trans-splicing ribozyme in intrahepatic colon cancer mouse model. Clin Cancer Res 2008, 14:281-290. doi: 10.1158/1078-0432.CCR-07-1524 PMID: 18172280
31. Giavazzi R, Jessup JM, Campbell DE, Walker SM, Fidler IJ. Experimental nude mouse model of human colorectal cancer liver metastases. J Natl Cancer Inst 1986, 77:1303-1308. PMID: 3467119
32. Marchio S, Soster M, Cardaci S, Muratore A, Bartolini A, Barone V, et al. A complex of alpha6 integrin and E-cadherin drives liver metastasis of colorectal cancer cells through hepatic angiopoietin-like 6. EMBO Mol Med 2012, 4:1156-1175. doi: 10.1002/emmm.201101164 PMID: 23070965