{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T23:12:10Z","timestamp":1792019530068,"version":"4.4.0"},"reference-count":78,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2013,10,16]],"date-time":"2013-10-16T00:00:00Z","timestamp":1381881600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Epithelial to mesenchymal transition (EMT) is an integral process in the progression of many epithelial tumors. It involves a coordinated series of events, leading to the loss of epithelial features and the acquisition of a mesenchymal phenotype, resulting in invasion and metastasis. The EMT of hepatocellular carcinoma (HCC) cells is thought to be a key event in intrahepatic dissemination and distal metastasis. In this study, we used 12-O-tet-radecanoylphorbol-13-acetate (TPA) to dissect the signaling pathways involved in the EMT of HepG2 hepatocarcinoma cells. The spectacular change in phenotype induced by TPA, leading to a pronounced spindle-shaped fibroblast-like cell morphology, required ERK1\/2 activation. This ERK1\/2-dependent EMT process was characterized by a loss of E-cadherin function, modification of the cytoskeleton, the acquisition of mesenchymal markers and profound changes to extracellular matrix composition and mobility. Snail was essential for E-cadherin repression, but was not sufficient for full commitment of the  TPA-triggered EMT. We found that TPA triggered the formation of a complex between Snail and \u03b2-catenin that activated the Wnt pathway. This study thus provides the first evidence for the existence of a complex network governed by the ERK1\/2 signaling pathway, converging on the coregulation of Snail and the Wnt\/\u03b2-catenin pathway and responsible for the onset and the progression of EMT in hepatocellular carcinoma cells.<\/jats:p>","DOI":"10.3390\/ijms141020768","type":"journal-article","created":{"date-parts":[[2013,10,16]],"date-time":"2013-10-16T12:20:47Z","timestamp":1381926047000},"page":"20768-20792","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":53,"title":["Crosstalk between Beta-Catenin and Snail in the Induction of Epithelial to Mesenchymal Transition in Hepatocarcinoma: Role of the ERK1\/2 Pathway"],"prefix":"10.3390","volume":"14","author":[{"given":"Nathalie","family":"Zucchini-Pascal","sequence":"first","affiliation":[{"name":"Laboratory of Xenobiotic's Cellular and Molecular Toxicology, INRA,  UMR 1331 TOXALIM (Research Centre in Food Toxicology), Sophia Antipolis 06903, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ludovic","family":"Peyre","sequence":"additional","affiliation":[{"name":"Laboratory of Xenobiotic's Cellular and Molecular Toxicology, INRA,  UMR 1331 TOXALIM (Research Centre in Food Toxicology), Sophia Antipolis 06903, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roger","family":"Rahmani","sequence":"additional","affiliation":[{"name":"Laboratory of Xenobiotic's Cellular and Molecular Toxicology, INRA,  UMR 1331 TOXALIM (Research Centre in Food Toxicology), Sophia Antipolis 06903, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2013,10,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2557","DOI":"10.1053\/j.gastro.2007.04.061","article-title":"Hepatocellular carcinoma: Epidemiology and molecular carcinogenesis","volume":"132","author":"Rudolph","year":"2007","journal-title":"Gastroenterology"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1038\/nrc1076","article-title":"Translational strategies for cancer prevention in liver","volume":"3","author":"Kensler","year":"2003","journal-title":"Nat. Rev. Cancer"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"S56","DOI":"10.1053\/j.gastro.2004.09.016","article-title":"Pathogenesis of hepatitis B virus-related hepatocellular carcinoma: Old and new paradigms","volume":"127","year":"2004","journal-title":"Gastroenterology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"573","DOI":"10.2174\/1566524033479546","article-title":"Mechanisms of human hepatocarcinogenesis","volume":"3","author":"Coleman","year":"2003","journal-title":"Curr. Mol. Med"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"S62","DOI":"10.1053\/j.gastro.2004.09.017","article-title":"Pathogenesis of hepatitis C-associated hepatocellular carcinoma","volume":"127","author":"Liang","year":"2004","journal-title":"Gastroenterology"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1038\/ng0802-339","article-title":"Molecular pathogenesis of human hepatocellular carcinoma","volume":"31","author":"Thorgeirsson","year":"2002","journal-title":"Nat. Genet"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1038\/nrc1075","article-title":"Tumour-cell invasion and migration: Diversity and escape mechanisms","volume":"3","author":"Friedl","year":"2003","journal-title":"Nat. Rev. Cancer"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1016\/j.gcb.2010.04.017","article-title":"Epithelial-mesenchymal transition in the liver","volume":"34","author":"Firrincieli","year":"2010","journal-title":"Gastroenterol. Clin. Biol"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1169","DOI":"10.2217\/fon.09.91","article-title":"Epithelial-mesenchymal transition in hepatocellular carcinoma","volume":"5","author":"Zulehner","year":"2009","journal-title":"Future Oncol"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1420","DOI":"10.1172\/JCI39104","article-title":"The basics of epithelial-mesenchymal transition","volume":"119","author":"Kalluri","year":"2009","journal-title":"J. Clin. Investig"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"740","DOI":"10.1016\/j.ceb.2003.10.006","article-title":"Epithelial-mesenchymal transitions in development and pathologies","volume":"15","author":"Thiery","year":"2003","journal-title":"Curr. Opin. Cell Biol"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1603","DOI":"10.1126\/science.1105718","article-title":"Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity","volume":"307","author":"Ozdamar","year":"2005","journal-title":"Science"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1387\/ijdb.041794hp","article-title":"Transcriptional regulation of cadherins during development and carcinogenesis","volume":"48","author":"Peinado","year":"2004","journal-title":"Int. J. Dev. Biol"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1016\/j.ceb.2005.08.001","article-title":"Molecular requirements for epithelial-mesenchymal transition during tumor progression","volume":"17","author":"Huber","year":"2005","journal-title":"Curr. Opin. Cell Biol"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1172\/JCI36183","article-title":"Biomarkers for epithelial-mesenchymal transitions","volume":"119","author":"Zeisberg","year":"2009","journal-title":"J. Clin. Investig"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1196\/annals.1294.006","article-title":"Multitasking in tumor progression: Signaling functions of cell adhesion molecules","volume":"1014","author":"Cavallaro","year":"2004","journal-title":"Ann. N. Y. Acad. Sci"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1053\/hp.2000.6683","article-title":"Immunoreactive E-cadherin, alpha-catenin, beta-catenin, and gamma-catenin proteins in hepatocellular carcinoma: Relationships with tumor grade, clinicopathologic parameters, and patients\u2019 survival","volume":"31","author":"Endo","year":"2000","journal-title":"Hum. Pathol"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1038\/nrc2131","article-title":"Snail Zeb bHLH factors in tumour progression: An alliance against the epithelial phenotype?","volume":"7","author":"Peinado","year":"2007","journal-title":"Nat. Rev. Cancer"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"818","DOI":"10.1016\/j.devcel.2008.05.009","article-title":"Epithelial-mesenchymal transition: At the crossroads of development and tumor metastasis","volume":"14","author":"Yang","year":"2008","journal-title":"Dev. Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.1002\/hep.22201","article-title":"Blocking transforming growth factor-beta up-regulates E-cadherin and reduces migration and invasion of hepatocellular carcinoma cells","volume":"47","author":"Fransvea","year":"2008","journal-title":"Hepatology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"24735","DOI":"10.1074\/jbc.272.40.24735","article-title":"Serine phosphorylation-regulated ubiquitination and degradation of beta-catenin","volume":"272","author":"Orford","year":"1997","journal-title":"J. Biol. Chem"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.cell.2006.10.018","article-title":"Wnt\/beta-catenin signaling in development and disease","volume":"127","author":"Clevers","year":"2006","journal-title":"Cell"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1923","DOI":"10.1126\/science.285.5435.1923","article-title":"Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1","volume":"285","author":"Roose","year":"1999","journal-title":"Science"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/S0002-9440(10)65297-2","article-title":"Expression of CD44 in Apc and Tcf mutant mice implies regulation by the WNT pathway","volume":"154","author":"Wielenga","year":"1999","journal-title":"Am. J. Pathol"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1016\/S0002-9440(10)65204-2","article-title":"Beta-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer","volume":"155","author":"Brabletz","year":"1999","journal-title":"Am. J. Pathol"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1038\/18884","article-title":"Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells","volume":"398","author":"Tetsu","year":"1999","journal-title":"Nature"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1007\/s11373-007-9230-y","article-title":"The transcriptional factor Snail simultaneously triggers cell cycle arrest and migration of human hepatoma HepG2","volume":"15","author":"Hu","year":"2008","journal-title":"J. Biomed. Sci"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"10123","DOI":"10.1158\/0008-5472.CAN-07-3127","article-title":"Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts","volume":"67","author":"Zeisberg","year":"2007","journal-title":"Cancer Res"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1016\/j.cell.2004.06.006","article-title":"Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis","volume":"117","author":"Yang","year":"2004","journal-title":"Cell"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1002\/ijc.2910440719","article-title":"Reversible transition towards a fibroblastic phenotype in a rat carcinoma cell line","volume":"4","author":"Boyer","year":"1989","journal-title":"Int. J. Cancer Suppl"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1016\/S0955-0674(99)00017-4","article-title":"Fibronectin fibrillogenesis: A paradigm for extracellular matrix assembly","volume":"11","author":"Schwarzbauer","year":"1999","journal-title":"Curr. Opin. Cell Biol"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3587","DOI":"10.1242\/jcs.00037","article-title":"PKCalpha-mediated ERK, JNK and p38 activation regulates the myogenic program in human rhabdomyosarcoma cells","volume":"115","author":"Mauro","year":"2002","journal-title":"J. Cell Sci"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1038\/ncb1173","article-title":"Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition","volume":"6","author":"Zhou","year":"2004","journal-title":"Nat. Cell Biol"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"7345","DOI":"10.1038\/sj.onc.1207990","article-title":"Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells","volume":"23","author":"Puig","year":"2004","journal-title":"Oncogene"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"6715","DOI":"10.1158\/0008-5472.CAN-10-1377","article-title":"Functional roles of multiple feedback loops in extracellular signal-regulated kinase and Wnt signaling pathways that regulate epithelial-mesenchymal transition","volume":"70","author":"Shin","year":"2010","journal-title":"Cancer Res"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1242\/dev.126.1.119","article-title":"Spatial response to fibroblast growth factor signalling in Xenopus embryos","volume":"126","author":"Christen","year":"1999","journal-title":"Development"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"12759","DOI":"10.1073\/pnas.2134254100","article-title":"Extracellular signal-regulated kinase 2 is necessary for mesoderm differentiation","volume":"100","author":"Yao","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_38","first-page":"4222","article-title":"Transforming growth factor beta1 treatment leads to an epithelial-mesenchymal transdifferentiation of pancreatic cancer cells requiring extracellular signal-regulated kinase 2 activation","volume":"61","author":"Ellenrieder","year":"2001","journal-title":"Cancer Res"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"4227","DOI":"10.1242\/jcs.00091","article-title":"Transforming growth factor-beta and epidermal growth factor synergistically stimulate epithelial to mesenchymal transition (EMT) through a MEK-dependent mechanism in primary cultured pig thyrocytes","volume":"115","author":"Franzen","year":"2002","journal-title":"J. Cell Sci"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1790","DOI":"10.1091\/mbc.e02-09-0583","article-title":"Tumor necrosis factor-alpha stimulates the epithelial-to-mesenchymal transition of human colonic organoids","volume":"14","author":"Bates","year":"2003","journal-title":"Mol. Biol. Cell"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"21113","DOI":"10.1074\/jbc.M211304200","article-title":"Transforming growth factor beta-1 induces snail transcription factor in epithelial cell lines: Mechanisms for epithelial mesenchymal transitions","volume":"278","author":"Peinado","year":"2003","journal-title":"J. Biol. Chem"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1484","DOI":"10.1002\/hep.510260615","article-title":"Altered expression of mitogen-activated protein kinases in a rat model of experimental hepatocellular carcinoma","volume":"26","author":"McKillop","year":"1997","journal-title":"Hepatology"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1002\/hep.510270409","article-title":"Activation of mitogen-activated protein kinases\/extracellular signal-regulated kinases in human hepatocellular carcinoma","volume":"27","author":"Ito","year":"1998","journal-title":"Hepatology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.jhep.2007.08.018","article-title":"Activation of the ERK and AKT signalling pathway predicts poor prognosis in hepatocellular carcinoma and ERK activation in cancer tissue is associated with hepatitis C virus infection","volume":"48","author":"Schmitz","year":"2008","journal-title":"J. Hepatol"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"5078","DOI":"10.1128\/MCB.23.14.5078-5089.2003","article-title":"Phosphorylation regulates the subcellular location and activity of the snail transcriptional repressor","volume":"23","author":"Guaita","year":"2003","journal-title":"Mol. Cell. Biol"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/j.ydbio.2009.05.544","article-title":"The timing of emergence of muscle progenitors is controlled by an FGF\/ERK\/SNAIL1 pathway","volume":"333","author":"Delfini","year":"2009","journal-title":"Dev. Biol"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1038\/sj.bjc.6600017","article-title":"Inverse correlation between E-cadherin and Snail expression in hepatocellular carcinoma cell lines in vitro and in vivo","volume":"86","author":"Jiao","year":"2002","journal-title":"Br. J. Cancer"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1006\/bbrc.1997.7831","article-title":"Role of E boxes in the repression of E-cadherin expression","volume":"241","author":"Giroldi","year":"1997","journal-title":"Biochem. Biophys. Res. Commun"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/S1043-4682(10)80013-3","article-title":"Cell adhesion in invasion and metastasis","volume":"3","author":"Behrens","year":"1992","journal-title":"Semin. Cell Biol"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1016\/0955-0674(93)90029-P","article-title":"Cadherins in cancer: Implications for invasion and metastasis","volume":"5","author":"Takeichi","year":"1993","journal-title":"Curr. Opin. Cell Biol"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S0968-0004(98)01343-7","article-title":"The role of the cell-adhesion molecule E-cadherin as a tumour-suppressor gene","volume":"24","author":"Christofori","year":"1999","journal-title":"Trends Biochem. Sci"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1137","DOI":"10.1053\/gast.1996.v110.pm8613003","article-title":"Expression of cadherins and alpha-catenin in primary epithelial tumors of the liver","volume":"110","author":"Kozyraki","year":"1996","journal-title":"Gastroenterology"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"5665","DOI":"10.3748\/wjg.14.5665","article-title":"Reduced expression of E-cadherin\/catenin complex in hepatocellular carcinomas","volume":"14","author":"Zhai","year":"2008","journal-title":"World J. Gastroenterol"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1038\/sj.bjc.6602266","article-title":"Snail accelerates cancer invasion by upregulating MMP expression and is associated with poor prognosis of hepatocellular carcinoma","volume":"92","author":"Miyoshi","year":"2005","journal-title":"Br. J. Cancer"},{"key":"ref_55","first-page":"2657","article-title":"Transcriptional repressor snail and progression of human hepatocellular carcinoma","volume":"9","author":"Sugimachi","year":"2003","journal-title":"Clin. Cancer Res"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1038\/nrm757","article-title":"The snail superfamily of zinc-finger transcription factors","volume":"3","author":"Nieto","year":"2002","journal-title":"Nat. Rev. Mol. Cell Biol"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"8184","DOI":"10.1128\/MCB.21.23.8184-8188.2001","article-title":"The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition","volume":"21","author":"Carver","year":"2001","journal-title":"Mol. Cell. Biol"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1769","DOI":"10.1038\/sj.bjc.6605369","article-title":"Hypoxia Snail incomplete epithelial-mesenchymal transition in breast cancer","volume":"101","author":"Lundgren","year":"2009","journal-title":"Br. J. Cancer"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"5764","DOI":"10.1038\/sj.onc.1208927","article-title":"TGF-beta and epithelial-to-mesenchymal transitions","volume":"24","author":"Zavadil","year":"2005","journal-title":"Oncogene"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1038\/nrc822","article-title":"Epithelial-mesenchymal transitions in tumour progression","volume":"2","author":"Thiery","year":"2002","journal-title":"Nat. Rev. Cancer"},{"key":"ref_61","first-page":"4547","article-title":"Wnt pathway activation in mesothelioma: Evidence of Dishevelled overexpression and transcriptional activity of beta-catenin","volume":"63","author":"Uematsu","year":"2003","journal-title":"Cancer Res"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"11740","DOI":"10.1074\/jbc.M413878200","article-title":"Wnt-dependent regulation of the E-cadherin repressor snail","volume":"280","author":"Yook","year":"2005","journal-title":"J. Biol. Chem"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1483","DOI":"10.1126\/science.1094291","article-title":"Convergence of Wnt, beta-catenin, and cadherin pathways","volume":"303","author":"Nelson","year":"2004","journal-title":"Science"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"987","DOI":"10.1172\/JCI0215429","article-title":"The cadherin-catenin adhesion system in signaling and cancer","volume":"109","author":"Zhurinsky","year":"2002","journal-title":"J. Clin. Investig"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"5075","DOI":"10.1038\/onc.2008.140","article-title":"Snail promotes Wnt target gene expression and interacts with beta-catenin","volume":"27","author":"Stemmer","year":"2008","journal-title":"Oncogene"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1298","DOI":"10.1002\/hep.21651","article-title":"WNT\/beta-catenin signaling in liver health and disease","volume":"45","author":"Thompson","year":"2007","journal-title":"Hepatology"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.2174\/138945008786786127","article-title":"Wnt signaling in liver cancer","volume":"9","author":"Takigawa","year":"2008","journal-title":"Curr. Drug Targets"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1763","DOI":"10.1053\/gast.2001.24798","article-title":"Genetic alterations associated with hepatocellular carcinomas define distinct pathways of hepatocarcinogenesis","volume":"120","author":"Legoix","year":"2001","journal-title":"Gastroenterology"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1110","DOI":"10.1053\/j.gastro.2004.07.009","article-title":"Functional consequences of frizzled-7 receptor overexpression in human hepatocellular carcinoma","volume":"127","author":"Merle","year":"2004","journal-title":"Gastroenterology"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/S0304-3835(03)00421-X","article-title":"GSK-3beta phosphorylation and alteration of beta-catenin in hepatocellular carcinoma","volume":"199","author":"Ban","year":"2003","journal-title":"Cancer Lett"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1111\/j.1478-3231.2005.01069.x","article-title":"Coordinated expression of cyclin D1 and LEF-1\/TCF transcription factor is restricted to a subset of hepatocellular carcinoma","volume":"25","author":"Allgaier","year":"2005","journal-title":"Liver Int"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"8847","DOI":"10.1073\/pnas.95.15.8847","article-title":"Somatic mutations of the beta-catenin gene are frequent in mouse and human hepatocellular carcinomas","volume":"95","author":"Romagnolo","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1593\/neo.07469","article-title":"siRNA-mediated beta-catenin knockdown in human hepatoma cells results in decreased growth and survival","volume":"9","author":"Zeng","year":"2007","journal-title":"Neoplasia"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1516","DOI":"10.1002\/1097-0142(19950315)75:6+<1516::AID-CNCR2820751522>3.0.CO;2-7","article-title":"Overexpression of matrix metalloproteinase-7 mRNA in human colon carcinomas","volume":"75","author":"Mori","year":"1995","journal-title":"Cancer"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/0092-8674(91)90403-L","article-title":"A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells","volume":"65","author":"Hofmann","year":"1991","journal-title":"Cell"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.tox.2008.11.004","article-title":"Lindane and cell death: At the crossroads between apoptosis, necrosis and autophagy","volume":"256","author":"Rahmani","year":"2009","journal-title":"Toxicology"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"265","DOI":"10.2144\/000113083","article-title":"TScratch: A novel and simple software tool for automated analysis of monolayer wound healing assays","volume":"46","author":"Schulz","year":"2009","journal-title":"Biotechniques"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"6919","DOI":"10.1158\/0008-5472.CAN-05-3697","article-title":"SYT-SSX1 and SYT-SSX2 interfere with repression of E-cadherin by snail and slug: A potential mechanism for aberrant mesenchymal to epithelial transition in human synovial sarcoma","volume":"66","author":"Saito","year":"2006","journal-title":"Cancer Res"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/14\/10\/20768\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T21:49:54Z","timestamp":1760219394000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/14\/10\/20768"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,10,16]]},"references-count":78,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2013,10]]}},"alternative-id":["ijms141020768"],"URL":"https:\/\/doi.org\/10.3390\/ijms141020768","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,10,16]]}}}