Transcription regulation of E-cadherin by zinc finger E-box binding homeobox proteins in solid tumors

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Wong, Thian Sze ^a   Gao, Wei ^a   Chan, Jimmy Yu Wai ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZEB1; TRANSCRIPTION FACTOR ZEB2; UNCLASSIFIED DRUG; UVOMORULIN; CADHERIN; HOMEODOMAIN PROTEIN; ZINC FINGER PROTEIN;

BLADDER CANCER; BRAIN CANCER; BREAST CANCER; COLON CANCER; DOWN REGULATION; ENDOMETRIUM CANCER; GENETIC CODE; HEAD AND NECK CANCER; HUMAN; KIDNEY CANCER; LIVER CANCER; LUNG CANCER; NONHUMAN; PANCREAS CANCER; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; REVIEW; SOLID TUMOR; STOMACH CANCER; TRANSCRIPTION REGULATION; UPREGULATION; UTERINE CERVIX CANCER; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NEOPLASM;

CADHERINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; NEOPLASMS; TRANSCRIPTION, GENETIC; ZINC FINGERS;

EID: 84907404695     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/921564     Document Type: Review

References (132)

1. M. Takeichi, "The cadherins: cell-cell adhesion molecules controlling animal morphogenesis," Development, vol. 102, no. 4, pp. 639-655, 1988.
2. M. Takeichi, "Cadherin cell adhesion receptors as a morphogenetic regulator," Science, vol. 251, no. 5000, pp. 1451-1455, 1991.
3. H. Peinado, D. Olmeda, and A. Cano, "Snail, ZEB and bHLH factors in tumour progression: an alliance against the epithelial phenotype?" Nature Reviews Cancer, vol. 7, no. 6, pp. 415-428, 2007.
4. J. P. Thiery, H. Acloque, R. Y. J. Huang, and M. A. Nieto, "Epithelial-mesenchymal transitions in development and disease," Cell, vol. 139, no. 5, pp. 871-890, 2009.
5. T. Murai, S. Yamada, B. C. Fuchs et al., "Epithelial-to-mesenchymal transition predicts prognosis in clinical gastric cancer," Journal of Surgical Oncology, vol. 109, no. 7, pp. 684-689, 2014.
6. R. Kalluri and E. G. Neilson, "Epithelial-mesenchymal transition and its implications for fibrosis," Journal of Clinical Investigation, vol. 112, no. 12, pp. 1776-1784, 2003.
7. M. Bensimhon, J. Gabarro-Arpa, R. Ehrlich, and C. Reiss, "Physical characteristics in eucaryotic promoters," Nucleic Acids Research, vol. 11, no. 13, pp. 4521-4540, 1983.
8. A. Cano, M. A. Pérez-Moreno, I. Rodrigo et al., "The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression," Nature Cell Biology, vol. 2, no. 2, pp. 76-83, 2000.
9. K. M. Hajra and E. R. Fearon, "The SLUG zinc-finger protein represses E-cadherin in breast cancer," Cancer Research, vol. 62, no. 6, pp. 1613-1618, 2002.
10. J. Behrens, O. Löwrick, L. Klein-Hitpass, and W. Birchmeier, "The E-cadherin promoter: functional analysis of a G.C-rich region and an epithelial cell-specific palindromic regulatory element," Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 24, pp. 11495-11499, 1991.
11. L. A. Giroldi, P. Bringuier, M. de Weijert, C. Jansen, A. van Bokhoven, and J. A. Schalken, "Role of E boxes in the repression of E-cadherin expression," Biochemical and Biophysical Research Communications, vol. 241, no. 2, pp. 453-458, 1997.
12. J. Weinberger, D. Baltimore, and P. A. Sharp, "Distinct factors bind to apparently homolgous sequences in the immunoglobulin heavy-chain enhancer," Nature, vol. 322, no. 6082, pp. 846-848, 1986.
13. M. E. Massari and C. Murre, "Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms," Molecular and Cellular Biology, vol. 20, no. 2, pp. 429-440, 2000.
14. J. Behrens, O. Lowrick, L. Klein-Hitpass, and W. Birchmeier, "The E-cadherin promoter: functional analysis of a G·C-rich region and an epithelial cell-specific palindromic regulatory element," Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 24, pp. 11495-11499, 1991.
15. J. Comijn, G. Berx, P. Vermassen et al., "The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion," Molecular Cell, vol. 7, no. 6, pp. 1267-1278, 2001.
16. R. Sekido, K. Murai, J. Funahashi et al., "The δ-crystallin enhancer-binding protein δEF1 is a repressor of E2- box-mediated gene activation," Molecular and Cellular Biology, vol. 14, no. 9, pp. 5692-5700, 1994.
17. H. Yasuda, A. Mizuno, T. Tamaoki, and T. Morinaga, "ATBF1, amultiple-homeodomain zinc finger protein, selectively downregulates AT-rich elements of the human α-fetoprotein gene," Molecular and Cellular Biology, vol. 14, no. 2, pp. 1395-1401, 1994.
18. T. Genetta, D. Ruezinsky, and T. Kadesch, "Displacement of an E-box-binding repressor by basic helix-loop-helix proteins: implications for B-cell specificity of the immunoglobulin heavy-chain enhancer," Molecular and Cellular Biology, vol. 14, no. 9, pp. 6153-6163, 1994.
19. N. S. Spoelstra, N. G. Manning, Y. Higashi et al., "The transcription factor ZEB1 is aberrantly expressed in aggressive uterine cancers," Cancer Research, vol. 66, no. 7, pp. 3893-3902, 2006.
20. Y. Higashi, H. Moribe, T. Takagi et al., "Impairment of T cell development in δEF1 mutant mice," The Journal of Experimental Medicine, vol. 185, no. 8, pp. 1467-1479, 1997.
21. T. Takagi, H. Moribe, H. Kondoh, and Y. Higashi, "DeltaEF1, a zinc finger and homeodomain transcription factor, is required for skeleton patterning in multiple lineages," Development, vol. 125, no. 1, pp. 21-31, 1998.
22. A. A. Postigo and D. C. Dean, "Differential expression and function of members of the zfh-1 family of zinc finger/homeodomain repressors," Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 12, pp. 6391-6396, 2000.
23. J. E. Remacle, H. Kraft, W. Lerchner et al., "New mode of DNA binding of multi-zinc finger transcription factors: δEF1 family members bind with two hands to two target sites," The EMBO Journal, vol. 18, no. 18, pp. 5073-5084, 1999.
24. H. Lee, S. Y. Jun, Y. S. Lee, H. J. Lee, W. S. Lee, and C. S. Park, "Expression of miRNAs and ZEB1 and ZEB2 correlates with histopathological grade in papillary urothelial tumors of the urinary bladder," Virchows Archiv, vol. 464, no. 2, pp. 213-220, 2014.
25. E. Oztas, M. E. Avci, A. Ozcan, A. E. Sayan, E. Tulchinsky, and T. Yagci, "Novel monoclonal antibodies detect Smad-interacting protein 1 (SIP1) in the cytoplasm of human cells from multiple tumor tissue arrays," Experimental and Molecular Pathology, vol. 89, no. 2, pp. 182-189, 2010.
26. L. A. van Grunsven, V. Taelman, C. Michiels et al., "XSip1 neuralizing activity involves the co-repressor CtBP and occurs through BMP dependent and independent mechanisms," Developmental Biology, vol. 306, no. 1, pp. 34-49, 2007.
27. G. Verstappen, L. A. Van Grunsven, C. Michiels et al., "Atypical Mowat-Wilson patient confirms the importance of the novel association between ZFHX1B/SIP1 and NuRD corepressor complex," Human Molecular Genetics, vol. 17, no. 8, pp. 1175-1183, 2008.
28. A. A. Postigo and D. C. Dean, "ZEB represses transcription through interaction with the corepressor CtBP," Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 12, pp. 6683-6688, 1999.
29. A. Sundqvist, K. Sollerbrant, and C. Svensson, "The carboxyterminal region of adenovirus E1A activates transcription through targeting of a C-terminal binding protein-histone deacetylase complex," FEBS Letters, vol. 429, no. 2, pp. 183-188, 1998.
30. L. Zhao, M. Kuppuswamy, S. Vijayalingam, and G. Chinnadurai, "Interaction of ZEB and histone deacetylase with the PLDLS-binding cleft region of monomeric C-terminal binding protein 2," BMC Molecular Biology, vol. 10, article 89, 2009.
31. T. Furusawa, H. Moribe, H. Kondoh, and Y. Higashi, "Identification of CtBP1 and CtBP2 as corepressors of zinc finger-homeodomain factor δEF1," Molecular and Cellular Biology, vol. 19, no. 12, pp. 8581-8590, 1999.
32. L. A. van Grunsven, C. Michiels, T. van de Putte et al., "Interaction between Smad-interacting protein-1 and the corepressor C-terminal binding protein is dispensable for transcriptional repression of E-cadherin," Journal of Biological Chemistry, vol. 278, no. 28, pp. 26135-26145, 2003.
33. J. Long, D. Zuo, and M. Park, "Pc2-mediated sumoylation of Smad-interacting protein 1 attenuates transcriptional repression of E-cadherin," The Journal of Biological Chemistry, vol. 280, no. 42, pp. 35477-35489, 2005.
34. X. Wang, X. He, F. Zhao et al., "Regulation gene expression of miR200c and ZEB1 positively enhances effect of tumor vaccine B16F10/GPI-IL-21 on inhibition of melanoma growth and metastasis," Journal of Translational Medicine, vol. 12, article 68, 2014.
35. L. Bojmar, E. Karlsson, S. Ellega˚rd et al., "The role of microRNA-200 in progression of human colorectal and breast cancer," PLoS ONE, vol. 8, no. 12, article e84815, 2013.
36. L. Hill, G. Browne, and E. Tulchinsky, "ZEB/miR-200 feedback loop: at the crossroads of signal transduction in cancer," International Journal of Cancer, vol. 132, no.4,pp. 745-754, 2012.
37. S. Brabletz and T. Brabletz, "The ZEB/miR-200 feedback loop-a motor of cellular plasticity in development and cancer?" EMBO Reports, vol. 11, no. 9, pp. 670-677, 2010.
38. Q. Weng, Y. Chen, H. Wang et al., "Dual-mode modulation of Smad signaling by Smad-interacting protein Sip1 is required for myelination in the central nervous system," Neuron, vol. 73, no. 4, pp. 713-728, 2012.
39. L. A. van Grunsven, V. Taelman, C. Michiels, K. Opdecamp, D. Huylebroeck, and E. J. Bellefroid, "δEF1 and SIP1 are differentially expressed and have overlapping activities during Xenopus embryogenesis," Developmental Dynamics, vol. 235, no. 6, pp. 1491-1500, 2006.
40. A. Gheldof, P. Hulpiau, F. van Roy, B. de Craene, and G. Berx, "Evolutionary functional analysis and molecular regulation of the ZEB transcription factors," Cellular and Molecular Life Sciences, vol. 69, no. 15, pp. 2527-2541, 2012.
41. Du. HF, Ou. LP, X. Yang et al., "A new PKCα/β/TBX3/E-cadherin pathway is involved in PLCε-regulated invasion and migration in human bladder cancer cells," Cellular Signalling, vol. 26, no. 3, pp. 580-593, 2014.
42. O. M. Omran, "Cd10 and e-cad expression in urinary bladder urothelial and squamous cell carcinoma," Journal of Environmental Pathology, Toxicology and Oncology, vol. 31, no. 3, pp. 203-212, 2012.
43. B. Keck, S. Wach, F. Kunath et al., "Nuclear E-cadherin expression is associated with the loss of membranous E-cadherin, plasmacytoid differentiation and reduced overall survival in urothelial carcinoma of the bladder," Annals of Surgical Oncology, vol. 20, no. 7, pp. 2440-2445, 2013.
44. S. T. dos Reis, K. R. M. Leite, A. Mosconi Neto et al., "Immune expression of E-cadherin and α, β and γ-catenin adhesion molecules and prognosis for upper urinary tract urothelial carcinomas," International Brazilian Journal of Urology, vol. 38, no. 4, pp. 466-473, 2012.
45. G. Li, Y. Liu, H. Yin et al., "E-cadherin gene promoter hypermethylation may contribute to the risk of bladder cancer among Asian populations," Gene, vol. 534, no. 1, pp. 48-53, 2014.
46. R. H. M. Salama, T. H. Selem, M. El-Gammal, A. A. Elhagagy, and S. M. Bakar, "Urinary tumor markers could predict survival in bladder carcinoma," Indian Journal of Clinical Biochemistry, vol. 28, no. 3, pp. 265-271, 2013.
47. M. Xiong, L. Jiang, Y. Zhou et al., "The miR-200 family regulates TGF-β1-induced renal tubular epithelial to mesenchymal transition through smad pathway by targeting ZEB1 and ZEB2 expression," The American Journal of Physiology - Renal Physiology, vol. 302, no. 3, pp. F369-F379, 2012.
48. S. Oba, S. Kumano, E. Suzuki et al., "miR-200b precursor can ameliorate renal tubulointerstitial fibrosis," PLoS ONE, vol. 5, no. 10, Article ID e13614, 2010.
49. K. Wu, Z. Ning, J. Zeng et al., "Silibinin inhibits β-catenin/ZEB1 signaling and suppresses bladder cancer metastasis via dual-blocking epithelial-mesenchymal transition and stemness," Cell Signal, vol. 25, no. 12, pp. 2625-2633, 2013.
50. K. Wu, J. Fan, L. Zhang et al., "PI3K/Akt to GSK3β/β-catenin signaling cascade coordinates cell colonization for bladder cancer bone metastasis through regulating ZEB1 transcription," Cellular Signalling, vol. 24, no. 12, pp. 2273-2282, 2012.
51. Y. Matsui, K. Assi, O. Ogawa et al., "Theimportance of integrin-linked kinase in the regulation of bladder cancer invasion," International Journal of Cancer, vol. 130, no. 3, pp. 521-531, 2012.
52. S. Majid, A. A. Dar, S. Saini et al., "MicroRNA-23b functions as a tumor suppressor by regulating Zeb1 in bladder cancer," PLoS ONE, vol. 8, no. 7, Article ID e67686, 2013.
53. L. Ying, Q. Chen, Y. Wang, Z. Zhou, Y. Huang, and F. Qiu, "Upregulated MALAT-1 contributes to bladder cancer cell migration by inducing epithelial-to-mesenchymal transition," Molecular BioSystems, vol. 8, no. 9, pp. 2289-2294, 2012.
54. K. Iwami, A. Natsume, and T. Wakabayashi, "Cytokine networks in glioma," Neurosurgical Review, vol. 34, no. 3, pp. 253-263, 2011.
55. R. Stupp, W. P. Mason, M. J. van den Bent et al., "Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma," The New England Journal of Medicine, vol. 352, no. 10, pp. 987-996, 2005.
56. L. Yang, M. Liu, C. Deng, Z. Gu, and Y. Gao, "Expression of transforming growth factor-β1 (TGF-β1) and E-cadherin in glioma," Tumor Biology, vol. 33, no. 5, pp. 1477-1484, 2012.
57. W. Wu, Y. Tian, H. Wan et al., "Expression of β-catenin and E-and N-cadherin in human brainstem gliomas and clinicopathological correlations," International Journal of Neuroscience, vol. 123, no. 5, pp. 318-323, 2013.
58. C. Perego, C. Vanoni, S. Massari et al., "Invasive behaviour of glioblastoma cell lines is associated with altered organisation of the cadherin-catenin adhesion system," Journal of Cell Science, vol. 115, no. 16, pp. 3331-3340, 2002.
59. L. J. Lewis-Tuffin, F. Rodriguez, C. Giannini et al., "Misregulated E-Cadherin expression associated with an aggressive brain tumor phenotype," PLoS ONE, vol. 5, no. 10, Article ID e13665, 2010.
60. M. Ebinger, L. Senf, O. Wachowski, and W. Scheurlen, "Promoter methylation pattern of caspase-8, P16INK4A, MGMT, TIMP-3, and E-cadherin in medulloblastoma," Pathology and Oncology Research, vol. 10, no. 1, pp. 17-21, 2004.
61. L. A. Edwards, K. Woolard, M. J. Son et al., "Effect of brain- and tumor-derived connective tissue growth factor on glioma invasion," Journal of the National Cancer Institute, vol. 103, no. 15, pp. 1162-1178, 2011.
62. S. Qi, Y. Song, Y. Peng et al., "ZEB2 mediates multiple pathways regulating cell proliferation, migration, invasion, and apoptosis in glioma," PLoS ONE, vol. 7, no. 6, Article ID e38842, 2012.
63. D. Sarrió, B. Pérez-Mies, D. Hardisson et al., "Cytoplasmic localization of p120ctn and E-cadherin loss characterize lobular breast carcinoma from preinvasive to metastatic lesions," Oncogene, vol. 23, no. 19, pp. 3272-3283, 2004.
64. J. K. Richer, B. M. Jacobsen, N. G. Manning, M. G. Abel, D. M. Wolf, and K. B. Horwitz, "Differential gene regulation by the two progesterone receptor isoforms in human breast cancer cells," Journal of Biological Chemistry, vol. 277, no. 7, pp. 5209-5218, 2002.
65. P. Bhat-Nakshatri, H. Appaiah, C. Ballas et al., "SLUG/SNAI2 and Tumor Necrosis Factor Generate Breast Cells With CD44+/CD24- Phenotype," BMC Cancer, vol. 10, article 411, 2010.
66. A. Ahmad, S. H. Sarkar, B. Bitar et al., "Garcinol regulates EMT and Wnt signaling pathways in vitro and in vivo, leading to anticancer activity against breast cancer cells," Molecular Cancer Therapeutics, vol. 11, no. 10, pp. 2193-2201, 2012.
67. C. J. Vessey, J. Wilding, N. Folarin et al., "Altered expression and function of E-cadherin in cervical intraepithelial neoplasia and invasive squamous cell carcinoma," Journal of Pathology, vol. 176, no. 2, pp. 151-159, 1995.
68. S. Liao, D. Deng, W. Zhang et al., "Human papillomavirus 16/18 E5 promotes cervical cancer cell proliferation, migration and invasion in vitro and accelerates tumor growth in vivo," Oncology Reports, vol. 29, no. 1, pp. 95-102, 2013.
69. J. Wilding, K. H. Vousden, W. P. Soutter, P. D. McCrea, R. Del Buono, and M. Pignatelli, "E-cadherin transfection downregulates the epidermal growth factor receptor and reverses the invasive phenotype of human papilloma virus- transfected keratinocytes," Cancer Research, vol. 56, no. 22, pp. 5285-5292, 1996.
70. A. Widschwendter, L. Ivarsson, A. Blassnig et al., "CDH1 AND CDH13 methylation in serum is an independent prognostic marker in cervical cancer patients," International Journal of Cancer, vol. 109, no. 2, pp. 163-166, 2004.
71. D. Feng, J. Wu, Y. Tian et al., " Targeting of histone deacetylases to reactivate tumour suppressor genes and its therapeutic potential in a human cervical cancer xenograft model," PLoS ONE, vol. 8, no. 11, article e80657, 2013.
72. C. Cunniffe, F. Ryan, H. Lambkin, and B. Brankin, "Expression of tight and adherens junction proteins in cervical neoplasia," British Journal of Biomedical Science, vol. 69, no. 4, pp. 147-153, 2012.
73. C. Tai, C. Cheng, H. Su et al., "Thrombomodulin mediates the migration of cervical cancer cells through the regulation of epithelial-mesenchymal transition biomarkers," Tumor Biology, vol. 35, no. 1, pp. 47-54, 2014.
74. S. Yan, Y. Wang, Q. Yang et al., "Low-dose radiation-induced epithelial-mesenchymal transition through NF-κB in cervical cancer cells," International Journal of Oncology, vol. 42, no. 5, pp. 1801-1806, 2013.
75. A. Mayer, M. Höckel, N. Schlischewsky, H. Schmidberger, L. C. Horn, and P. Vaupel, "Lacking hypoxia-mediated downregulation of E-cadherin in cancers of the uterine cervix," British Journal of Cancer, vol. 108, no. 2, pp. 402-408, 2013.
76. A. Doʇan, Z. D. Wang, and J. Spencer, "E-cadherin expression in intestinal epithelium," Journal of Clinical Pathology, vol. 48, no. 2, pp. 143-146, 1995.
77. M. J. Wheelock, "Catenin association with E-cadherin changes with the state of polarity of HT-29 cells," Experimental Cell Research, vol. 191, no. 2, pp. 186-193, 1990.
78. M. Pignatelli, D. Liu, M. M. Nasim, G. W. H. Stamp, S. Hirano, and M. Takeichi, "Morphoregulatory activities of E-cadherin and beta-1 integrins in colorectal tumour cells," British Journal of Cancer, vol. 66, no. 4, pp. 629-634, 1992.
79. E. Breen, G. Steele Jr., and A. M. Mercurio, "Role of the Ecadherin/α-catenin complex in modulating cell-cell and cellmatrix adhesive properties of invasive colon carcinoma cells," Annals of Surgical Oncology, vol. 2, no. 5, pp. 378-385, 1995.
80. S. B. Munro, I. M. Turner, R. Farookhi, O. W. Blaschuk, and S. Jothy, "E-cadherin and OB-cadherin mRNA levels in normal human colon and colon carcinoma," Experimental and Molecular Pathology, vol. 62, no. 2, pp. 118-122, 1995.
81. M. Katayama, S. Hirai, M. Yasumoto et al., "Soluble fragments of E-cadherin cell adhesion molecule increase in urinary excretion of cancer patients, potentially indicating its shedding from epithelial tumor cells," International Journal of Oncology, vol. 5, no. 5, pp. 1049-1057, 1994.
82. A. R. Paek, C. H. Lee, and H. J. You, "A role of zinc-finger protein 143 for cancer cell migration and invasion through ZEB1 and Ecadherin in colon cancer cells," Molecular Carcinogenesis, vol. 53, no. S1, pp. E161-E168, 2014.
83. A. B. Singh, A. Sharma, J. J. Smith et al., "Claudin-1 up-regulates the repressor ZEB-1 to inhibit E-cadherin expression in colon cancer cells," Gastroenterology, vol. 141, no. 6, pp. 2140-2153, 2011.
84. L. K. Mell, J. J. Meyer, M. Tretiakova et al., "Prognostic significance of E-cadherin protein expression in pathological stage I-III endometrial cancer," Clinical Cancer Research, vol. 10, no. 16, pp. 5546-5553, 2004.
85. P. W. Schlosshauer, L. H. Ellenson, and R. A. Soslow, "β-catenin and E-cadherin expression patterns in high-grade endometrial carcinoma are associated with histological subtype," Modern Pathology, vol. 15, no. 10, pp. 1032-1037, 2002.
86. Y. T. Kim, E. K. Choi, J. W. Kim, D. K. Kim, S. H. Kim, and W. I. Yang, "Expression of E-cadherin and α-, β-, γ-catenin proteins in endometrial carcinoma," Yonsei Medical Journal, vol. 43, no. 6, pp. 701-711, 2002.
87. J. H. Park, B. I. Lee, E. S. Song, S. O. Whang, W. Y. Lee, and S. J. Cho, "Hypermethylation of E-cadherin in endometrial carcinoma," Journal of Gynecologic Oncology, vol. 19, no. 4, pp. 241-245, 2008.
88. A. A. Postigo, "Opposing functions of ZEB proteins in the regulation of the TGFβ/BMP signaling pathway," The EMBO Journal, vol. 22, no. 10, pp. 2443-2452, 2003.
89. M. Singh, N. S. Spoelstra, A. Jean et al., "ZEB1 expression in type I vs type II endometrial cancers: a marker of aggressive disease," Modern Pathology, vol. 21, no. 7, pp. 912-923, 2008.
90. P. Carneiro, J. Figueiredo, R. Bordeira-Carric¸o et al., "Therapeutic targets associated to E-cadherin dysfunction in gastric cancer," Expert Opinion on Therapeutic Targets, vol. 17, no. 10, pp. 1187-201, 2013.
91. Y. Qu, S. Dang, and P. Hou, "Gene methylation in gastric cancer," Clinica Chimica Acta, vol. 424, pp. 53-65, 2013.
92. G. Carrasco and A. H. Corvalan, "Helicobacter pylori-induced chronic gastritis and assessing risks for gastric cancer," Gastroenterology Research and Practice, vol. 2013, Article ID 393015, 8 pages, 2013.
93. A. O. O. Chan and A. Rashid, "CpG island methylation in precursors of gastrointestinal malignancies," Current Molecular Medicine, vol. 6, no. 4, pp. 401-408, 2006.
94. J. Baud, C. Varon, S. Chabas, L. Chambonnier, F. Darfeuille, and C. Staedel, "Helicobacter pylori initiates a mesenchymal transition through ZEB1 in gastric epithelial cells," PLoS ONE, vol. 8, no. 4, Article ID e60315, 2013.
95. H. S. Ryu, J. Park do, H. H. Kim, W. H. Kim, and H. S. Lee, "Combination of epithelial-mesenchymal transition and cancer stem cell-like phenotypes has independent prognostic value in gastric cancer," Human Pathology, vol. 43, no. 4, pp. 520-528, 2012.
96. J. Kurashige, H. Kamohara, M. Watanabe et al., "MicroRNA-200b regulates cell proliferation, invasion, and migration by directly targeting ZEB2 in gastric carcinoma," Annals of Surgical Oncology, vol. 19, no. 3, pp. S656-S664, 2012.
97. Y. Lien, W. Wang, L. Kuo et al., "Nicotine promotes cell migration through alpha7 nicotinic acetylcholine receptor in gastric cancer cells," Annals of Surgical Oncology, vol. 18, no. 9, pp. 2671-2679, 2011.
98. Y. Kato, M. Yashiro, S. Noda et al., "Establishment and characterization of a new hypoxia-resistant cancer cell line, OCUM-12/Hypo, derived from a scirrhous gastric carcinoma," British Journal of Cancer, vol. 102, no. 5, pp. 898-907, 2010.
99. V. Matijssen, H. M. Peters, L. Schalkwijk et al., "E-cadherin expression in head and neck squamous-cell carcinoma is associated with clinical outcome," International Journal of Cancer, vol. 55, no. 4, pp. 580-585, 1993.
100. J. G. Eriksen, T. Steiniche, H. Søgaard, and J. Overgaard, "Expression of integrins and E-cadherin in squamous cell carcinomas of the head and neck," APMIS, vol. 112, no. 9, pp. 560-568, 2004.
101. A. M. Tomson, J. Scholma, B. Meijer, J. G. J. Koning, K. M. D. de Jong, and M. van der Werf, "Adhesion properties, intermediate filaments and malignant behaviour of head and neck squamous cell carcinoma cells in vitro," Clinical and Experimental Metastasis, vol. 14, no. 6, pp. 501-511, 1996.
102. E. Zvrko, A. Mikić, and S. Jancić, "Relationship of E-cadherin with cervical lymph node metastasis in laryngeal cancer," Collegium Antropologicum, vol. 36, Supplement 2, pp. 119-124, 2012.
103. E. Mittari, A. Charalabopoulos, A. Batistatou, and K. Charalabopoulos, "The role of E-cadherin/catenin complex in laryngeal cancer," Experimental Oncology, vol. 27, no. 4, pp. 257-261, 2005.
104. A. Franchi, O. Gallo, V. Boddi, and M. Santucci, "Prediction of occult neck metastases in laryngeal carcinoma: Role of proliferating cell nuclear antigen, MIB-1, and E-cadherin immunohistochemical determination," Clinical Cancer Research, vol. 2, no. 10, pp. 1801-1808, 1996.
105. C. J. Marsit, M. R. Posner, M. D. McClean, and K. T. Kelsey, "Hypermethylation of E-cadherin is an independent predictor of improved survival in head and neck squamous cell carcinoma," Cancer, vol. 113, no. 7, pp. 1566-1571, 2008.
106. A. Al Moustafa, W. D. Foulkes, N. Benlimame et al., "E6/E7 proteins of HPV type 16 and ErbB-2 cooperate to induce neoplastic transformation of primary normal oral epithelial cells," Oncogene, vol. 23, no. 2, pp. 350-358, 2004.
107. M. Dohadwala, G. Wang, E. Heinrich et al., "The role of ZEB1 in the inflammation-induced promotion of EMT in HNSCC," Otolaryngology - Head and Neck Surgery, vol. 142, no. 5, pp. 753-759, 2010.
108. K. Sakamoto, Y. Imanishi, T. Tomita et al., "Overexpression of SIP1 and downregulation of e-cadherin predict delayed neck metastasis in stage I/II oral tongue squamous cell carcinoma after partial glossectomy," Annals of Surgical Oncology, vol. 19, no. 2, pp. 612-619, 2012.
109. Y. Zhou, J. Liu, J. Li et al., "Ionizing radiation promotes migration and invasion of cancer cells through transforming growth factor-beta-mediated epithelial-mesenchymal transition," International Journal of Radiation Oncology Biology Physics, vol. 81, no. 5, pp. 1530-1537, 2011.
110. W. Chen, S. Wu, G. Zhang, W. Wang, and Y. Shi, "Effect of AKT inhibition on epithelial-mesenchymal transition and ZEB1-potentiated radiotherapy in nasopharyngeal carcinoma," Oncology Letters, vol. 6, no. 5, pp. 1234-1240, 2013.
111. W. Ding, H. You, H. Dang et al., "Epithelial-to-mesenchymal transition of murine liver tumor cells promotes invasion," Hepatology, vol. 52, no. 3, pp. 945-953, 2010.
112. T. Liu, Y. Jan, B. Ko et al., "14-3-3ε overexpression contributes to epithelial-mesenchymal transition of hepatocellular carcinoma," PLoS ONE, vol. 8, no. 3, Article ID e57968, 2013.
113. T. Grosse-Steffen, T. Giese, N. Giese et al., "Epithelial-to-mesenchymal transition in pancreatic ductal adenocarcinoma and pancreatic tumor cell lines: the role of neutrophils and neutrophil-derived elastase," Clinical and Developmental Immunology, vol. 2012, Article ID 720768, 12 pages, 2012.
114. M. Hashiguchi, S. Ueno, M. Sakoda et al., "Clinical implication of ZEB-1 and E-cadherin expression in hepatocellular carcinoma (HCC)," BMC Cancer, vol. 13, article 572, 2013.
115. J. Iqbal, S. McRae, T. Mai, K. Banaudha, M. Sarkar-Dutta, and G. Waris, "Role of hepatitis C virus induced osteopontin in epithelial to mesenchymal transition, migration and invasion of hepatocytes," PLoS One, vol. 9, no. 1, Article ID e87464, 2014.
116. H. Nakagawa, Y. Hikiba, Y. Hirata et al., "Loss of liver E-cadherin induces sclerosing cholangitis and promotes carcinogenesis," Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 3, pp. 1090-1095, 2014.
117. M. Huang, P. Wei, J. Liu et al., "Knockdown of thrombomodulin enhances HCC cell migration through increase of ZEB1 and decrease of E-cadherin gene expression," Annals of Surgical Oncology, vol. 17, no. 12, pp. 3379-3385, 2010.
118. Y. Suh, C. Yoon, R. Kim et al., "Claudin-1 induces epithelial-mesenchymal transition through activation of the c-Abl-ERK signaling pathway in human liver cells," Oncogene, vol. 32, no. 41, pp. 4873-4882, 2013.
119. T. Kim, A. Veronese, F. Pichiorri et al., "p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2," Journal of Experimental Medicine, vol. 208, no. 5, pp. 875-883, 2011.
120. Y. M. Zhou, L. Cao, B. Li et al., "Clinicopathological significance of ZEB1 protein in patients with hepatocellular carcinoma," Annals of Surgical Oncology, vol. 19, no. 5, pp. 1700-1706, 2012.
121. H. Kurahara, S. Takao, K. Maemura et al., "Epithelial-mesenchymal transition and mesenchymal-epithelial transition via regulation of ZEB-1 and ZEB-2 expression in pancreatic cancer," Journal of Surgical Oncology, vol. 105, no. 7, pp. 655-661, 2012.
122. Q. Fei, H. Zhang, X. Chen et al., "Defected expression of E-cadherin in non-small cell lung cancer," Lung Cancer, vol. 37, no. 2, pp. 147-152, 2002.
123. N. H. Myong, "Reduced expression of E-cadherin in human non-small cell lung carcinoma," Cancer Treatment and Research, vol. 36, no. 1, pp. 56-61, 2004.
124. A. Kalogeraki, D. Bouros, O. Zoras et al., "E-cadherin expression on fine-needle aspiration biopsies in primary lung adenocarcinomas is related to tumor differentiation and invasion," Anticancer Research, vol. 23, no. 4, pp. 3367-3371, 2003.
125. W. Liu, Y. J. Huang, C. Liu et al., "Inhibition of TBK1 attenuates radiation-induced epithelial-mesenchymal transition of A549 human lung cancer cells via activation of GSK-3β and repression of ZEB1," Laboratory Investigation, vol. 94, no. 4, pp. 362-370, 2014.
126. G. Y. Bae, S. J. Choi, J. S. Lee et al., "Loss of E-cadherin activates EGFR-MEK/ERK signaling, which promotes invasion via the ZEB1/MMP2 axis in non-small cell lung cancer," Oncotarget, vol. 4, no. 12, pp. 2512-2522, 2013.
127. W. Liao, G. Jordaan, M. K. Srivastava, S. Dubinett, and S. Sharma, "Effect of epigenetic histone modifications on E-cadherin splicing and expression in lung cancer," American Journal of Cancer Research, vol. 3, no. 4, pp. 374-389, 2013.
128. J. Clarhaut, R. M. Gemmill, V. A. Potiron et al., "ZEB-1, a repressor of the semaphorin 3F tumor suppressor gene in lung cancer cells," Neoplasia, vol. 11, no. 2, pp. 157-166, 2009.
129. M. Kakihana, T. Ohira, D. Chan et al., "Induction of E-cadherin in lung cancer and interaction with growth suppression by histone deacetylase inhibition," Journal of Thoracic Oncology, vol. 4, no. 12, pp. 1455-1465, 2009.
130. S. Mateen, K. Raina, C. Agarwal, D. Chan, and R. Agarwal, "Silibinin synergizes with histone deacetylase and DNA methyltransferase inhibitors in upregulating e-cadherin expression together with inhibition of migration and invasion of human non-small cell lung cancer cells," Journal of Pharmacology and Experimental Therapeutics, vol. 345, no. 2, pp. 206-214, 2013.
131. S. E. Witta, R. M. Gemmill, F. R. Hirsch et al., "Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines," Cancer Research, vol. 66, no. 2, pp. 944-950, 2006.
132. M. Dohadwala, S. Yang, J. Luo et al., "Cyclooxygenase-2-dependent regulation of E-cadherin: prostaglandin E(2) induces transcriptional repressors ZEB1 and snail in non-small cell lung cancer," Cancer Research, vol. 66,no. 10, pp. 5338-5345, 2006.