ZEB2 promotes vasculogenic mimicry by TGF-β1 induced epithelial-to-mesenchymal transition in hepatocellular carcinoma

Experimental and Molecular Pathology

Volumn 98, Issue 3, 2015, Pages 352-359

  Yang, Zhihong ^a   Sun, Baocun ^a   Li, Yanlei ^a   Zhao, Xiulan ^a   Zhao, Xueming ^a   Gu, Qiang ^a   An, Jindan ^a   Dong, Xueyi ^a   Liu, Fang ^a   Wang, Yong ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

Epithelial mesenchymal transition; Hepatocellular carcinoma; TGF 1; Vasculogenic mimicry; Zinc finger E box binding homeobox 2

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; ZINC FINGER E BOX BINDING HOMEOBOX 2 PROTEIN; ZINC FINGER PROTEIN; CADHERIN; FLT1 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; LEUKOCYTE ANTIGEN; MATRIX METALLOPROTEINASE; REPRESSOR PROTEIN; ZEB2 PROTEIN, HUMAN;

ADULT; ANGIOGENESIS; ARTICLE; CANCER STAGING; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL NUCLEUS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HEPG2 CELL LINE; HUMAN; HUMAN TISSUE; LIVER CELL CARCINOMA; MAJOR CLINICAL STUDY; MALE; METASTASIS; PROTEIN EXPRESSION; SURVIVAL TIME; UPREGULATION; VASCULOGENIC MIMICRY; GENETICS; LIVER TUMOR; METABOLISM; MIDDLE AGED; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY;

ADULT; ANTIGENS, CD; CADHERINS; CARCINOMA, HEPATOCELLULAR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HEP G2 CELLS; HOMEODOMAIN PROTEINS; HUMANS; LIVER NEOPLASMS; MALE; MATRIX METALLOPROTEINASES; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; REPRESSOR PROTEINS; TRANSFORMING GROWTH FACTOR BETA1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84926327635     PISSN: 00144800     EISSN: 10960945     Source Type: Journal    
DOI: 10.1016/j.yexmp.2015.03.030     Document Type: Article

References (41)

1. Bittner M., et al. Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 2000, 406:536-540.
2. Comijn J., et al. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell 2001, 7:1267-1278.
3. Dai Y.H., et al. ZEB2 promotes the metastasis of gastric cancer and modulates epithelial mesenchymal transition of gastric cancer cells. Dig. Dis. Sci. 2012, 57:1253-1260.
4. Hendrix M.J., et al. Expression and functional significance of VE-cadherin in aggressive human melanoma cells: role in vasculogenic mimicry. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8018-8023.
5. Hendrix M.J., et al. Molecular plasticity of human melanoma cells. Oncogene 2003, 22:3070-3075.
6. Hendrix M.J., et al. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nat. Rev. Cancer 2003, 3:411-421.
7. Hess A.R., et al. Phosphoinositide 3-kinase regulates membrane type 1-matrix metalloproteinase (MMP) and MMP-2 activity during melanoma cell vasculogenic mimicry. Cancer Res. 2003, 63:4757-4762.
8. Hsu Y.C., et al. Proline-directed protein kinase FA is a powerful and independent prognostic predictor for progression and patient survival of hepatocellular carcinoma. J. Clin. Oncol. 2006, 24:3780-3788.
9. Imamichi Y., et al. Collagen type I-induced Smad-interacting protein 1 expression downregulates E-cadherin in pancreatic cancer. Oncogene 2007, 26:2381-2385.
10. Jemal A., et al. Cancer statistics, 2007. CA Cancer J. Clin. 2007, 57:43-66.
11. Liu Z., et al. Zinc finger E-box binding homeobox 1 promotes vasculogenic mimicry in colorectal cancer through induction of epithelial-to-mesenchymal transition. Cancer Sci. 2012, 103:813-820.
12. Maeda G., et al. Expression of SIP1 in oral squamous cell carcinomas: implications for E-cadherin expression and tumor progression. Int. J. Oncol. 2005, 27:1535-1541.
13. Maniotis A.J., et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am. J. Pathol. 1999, 155:739-752.
14. Miettinen P.J., et al. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J. Cell Biol. 1994, 127:2021-2036.
15. Millimaggi D., et al. Vasculogenic mimicry of human ovarian cancer cells: role of CD147. Int. J. Oncol. 2009, 35:1423-1428.
16. Miyoshi A., et al. Snail and SIP1 increase cancer invasion by upregulating MMP family in hepatocellular carcinoma cells. Br. J. Cancer 2004, 90:1265-1273.
17. Mourad-Zeidan A.A., et al. Expression profiling of Galectin-3-depleted melanoma cells reveals its major role in melanoma cell plasticity and vasculogenic mimicry. Am. J. Pathol. 2008, 173:1839-1852.
18. Prindull G., Zipori D. Environmental guidance of normal and tumor cell plasticity: epithelial mesenchymal transitions as a paradigm. Blood 2004, 103:2892-2899.
19. Ruf W., et al. Differential role of tissue factor pathway inhibitors 1 and 2 in melanoma vasculogenic mimicry. Cancer Res. 2003, 63:5381-5389.
20. Seftor R.E., et al. Cooperative interactions of laminin 5 gamma2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma. Cancer Res. 2001, 61:6322-6327.
21. Seftor E.A., et al. Expression of multiple molecular phenotypes by aggressive melanoma tumor cells: role in vasculogenic mimicry. Crit. Rev. Oncol. Hematol. 2002, 44:17-27.
22. Shibuya M. Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J. Biochem. Mol. Biol. 2006, 39:469-478.
23. Sun B., et al. Vasculogenic mimicry is associated with poor survival in patients with mesothelial sarcomas and alveolar rhabdomyosarcomas. Int. J. Oncol. 2004, 25:1609-1614.
24. Sun T., et al. Expression and functional significance of Twist1 in hepatocellular carcinoma: its role in vasculogenic mimicry. Hepatology 2010, 51:545-556.
25. Sun T., et al. Promotion of tumor cell metastasis and vasculogenic mimicry by way of transcription coactivation by Bcl-2 and Twist1: a study of hepatocellular carcinoma. Hepatology 2011, 54:1690-1706.
26. Sun D., et al. Slug promoted vasculogenic mimicry in hepatocellular carcinoma. J. Cell. Mol. Med. 2013, 17:1038-1047.
27. Tang Z.Y., et al. A decade's studies on metastasis of hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 2004, 130:187-196.
28. Taylor M.A., et al. The pathophysiology of epithelial-mesenchymal transition induced by transforming growth factor-beta in normal and malignant mammary epithelial cells. J. Mammary Gland Biol. Neoplasia 2010, 15:169-190.
29. Thiery J.P. Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 2003, 15:740-746.
30. van Grunsven L.A., et al. Interaction between Smad-interacting protein-1 and the corepressor C-terminal binding protein is dispensable for transcriptional repression of E-cadherin. J. Biol. Chem. 2003, 278:26135-26145.
31. Vandewalle C., et al. SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Res. 2005, 33:6566-6578.
32. Verschueren K., et al. SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5'-CACCT sequences in candidate target genes. J. Biol. Chem. 1999, 274:20489-20498.
33. Wang J.Y., et al. Functional significance of VEGF-a in human ovarian carcinoma: role in vasculogenic mimicry. Cancer Biol. Ther. 2008, 7:758-766.
34. Wang R., et al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010, 468:829-833.
35. Winder T., Lenz H.J. Vascular endothelial growth factor and epidermal growth factor signaling pathways as therapeutic targets for colorectal cancer. Gastroenterology 2010, 138:2163-2176.
36. Xia M., et al. Identification of the role of Smad interacting protein 1 (SIP1) in glioma. J. Neurooncol. 2010, 97:225-232.
37. Yang J.D., Roberts L.R. Hepatocellular carcinoma: a global view. Nat. Rev. Gastroenterol. Hepatol. 2010, 7:448-458.
38. Yang Y., et al. Patterns and clinicopathologic features of extrahepatic recurrence of hepatocellular carcinoma after curative resection. Surgery 2007, 141:196-202.
39. Yoshihara K., et al. Gene expression profiling of advanced-stage serous ovarian cancers distinguishes novel subclasses and implicates ZEB2 in tumor progression and prognosis. Cancer Sci. 2009, 100:1421-1428.
40. Zhang S., et al. Vasculogenic mimicry: current status and future prospects. Cancer Lett. 2007, 254:157-164.
41. Zhang S., et al. Hypoxia influences linearly patterned programmed cell necrosis and tumor blood supply patterns formation in melanoma. Lab. Investig. 2009, 89:575-586.