ZEB2 promotes vasculogenic mimicry by TGF-β1 induced epithelial-to-mesenchymal transition in hepatocellular carcinoma
Zinc finger E-box binding homeobox 2 (ZEB2), an epithelial–mesenchymal transition (EMT) regulator, has been involved in invasion and metastasis of human tumor. Although EMT may be involved in vasculogenic mimicry (VM) formation, no reports describing the relation between ZEB2 and VM are available. W...
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| Veröffentlicht in: | Experimental and molecular pathology 2015-06, Vol.98 (3), p.352-359 |
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| creator | Yang, Zhihong Sun, Baocun Li, Yanlei Zhao, Xiulan Zhao, Xueming Gu, Qiang An, Jindan Dong, Xueyi Liu, Fang Wang, Yong |
| description | Zinc finger E-box binding homeobox 2 (ZEB2), an epithelial–mesenchymal transition (EMT) regulator, has been involved in invasion and metastasis of human tumor. Although EMT may be involved in vasculogenic mimicry (VM) formation, no reports describing the relation between ZEB2 and VM are available. We hypothesize that ZEB2 may promote VM formation in hepatocellular carcinoma (HCC).
Paraffin-embedded tumor tissue samples from 92 patients were immunostained with anti-ZEB2 antibody. We found that the ZEB2 nuclear expression was significantly associated with VM formation and metastasis. Patients with VM and ZEB2 nuclear expression had a shorter survival period than those without expression. In vitro, ZEB2 overexpression significantly enhanced cell motility, invasiveness, and VM formation of HepG2 cells. ZEB2 upregulation also increased VE-cadherin, Flt-1, and Flk-1 expression and activated MMPs. ZEB2 knockdown inhibited cell motility, invasiveness, and VM formation in Bel7402 cells. ZEB2 knockdown also decreased VE-cadherin, Flt-1, and Flk-1 expression and MMP activity. In addition, EMT in HepG2 cells was induced by TGF-β1 treatment, and the kinetics of expression of EMT markers and regulators were assessed by Western blot analysis. The expression of ZEB2 increased significantly, and VM formation was promoted.
ZEB2 can promote VM formation through the EMT pathway. Our findings may represent a novel therapeutic target in HCC.
•ZEB2 nuclear expression was associated with VM formation and metastasis in human hepatocellular carcinoma samples.•ZEB2 overexpression enhanced cell motility, invasiveness, and VM formation of hepatocellular carcinoma cells.•Knockdown of ZEB2 reduced tumor cell migration, invasion, VM formation, and endothelium related markers expression.•Epithelial–mesenchymal transition in hepatocellular carcinoma cells was induced by TGF-β1 treatment.•ZEB2 can promote VM formation through the EMT pathway. |
| doi_str_mv | 10.1016/j.yexmp.2015.03.030 |
| format | Article |
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Paraffin-embedded tumor tissue samples from 92 patients were immunostained with anti-ZEB2 antibody. We found that the ZEB2 nuclear expression was significantly associated with VM formation and metastasis. Patients with VM and ZEB2 nuclear expression had a shorter survival period than those without expression. In vitro, ZEB2 overexpression significantly enhanced cell motility, invasiveness, and VM formation of HepG2 cells. ZEB2 upregulation also increased VE-cadherin, Flt-1, and Flk-1 expression and activated MMPs. ZEB2 knockdown inhibited cell motility, invasiveness, and VM formation in Bel7402 cells. ZEB2 knockdown also decreased VE-cadherin, Flt-1, and Flk-1 expression and MMP activity. In addition, EMT in HepG2 cells was induced by TGF-β1 treatment, and the kinetics of expression of EMT markers and regulators were assessed by Western blot analysis. The expression of ZEB2 increased significantly, and VM formation was promoted.
ZEB2 can promote VM formation through the EMT pathway. Our findings may represent a novel therapeutic target in HCC.
•ZEB2 nuclear expression was associated with VM formation and metastasis in human hepatocellular carcinoma samples.•ZEB2 overexpression enhanced cell motility, invasiveness, and VM formation of hepatocellular carcinoma cells.•Knockdown of ZEB2 reduced tumor cell migration, invasion, VM formation, and endothelium related markers expression.•Epithelial–mesenchymal transition in hepatocellular carcinoma cells was induced by TGF-β1 treatment.•ZEB2 can promote VM formation through the EMT pathway.</description><identifier>ISSN: 0014-4800</identifier><identifier>EISSN: 1096-0945</identifier><identifier>DOI: 10.1016/j.yexmp.2015.03.030</identifier><identifier>PMID: 25818166</identifier><language>eng</language><publisher>Netherlands: Elsevier Inc</publisher><subject>Adult ; Antigens, CD - genetics ; Antigens, CD - metabolism ; Cadherins - genetics ; Cadherins - metabolism ; Carcinoma, Hepatocellular - metabolism ; Carcinoma, Hepatocellular - pathology ; Epithelial-Mesenchymal Transition ; Female ; Hep G2 Cells ; Hepatocellular carcinoma ; Homeodomain Proteins - genetics ; Homeodomain Proteins - metabolism ; Humans ; Liver Neoplasms - metabolism ; Liver Neoplasms - pathology ; Male ; Matrix Metalloproteinases - genetics ; Matrix Metalloproteinases - metabolism ; Middle Aged ; Neovascularization, Pathologic - metabolism ; Neovascularization, Pathologic - pathology ; Repressor Proteins - genetics ; Repressor Proteins - metabolism ; TGF-β1 ; Transforming Growth Factor beta1 - pharmacology ; Vascular Endothelial Growth Factor Receptor-1 - genetics ; Vascular Endothelial Growth Factor Receptor-1 - metabolism ; Vascular Endothelial Growth Factor Receptor-2 - genetics ; Vascular Endothelial Growth Factor Receptor-2 - metabolism ; Vasculogenic mimicry ; Zinc Finger E-box Binding Homeobox 2</subject><ispartof>Experimental and molecular pathology, 2015-06, Vol.98 (3), p.352-359</ispartof><rights>2015 Elsevier Inc.</rights><rights>Copyright © 2015 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c274t-8f623324ba33968694f2f6028ba27a1b41c8236aeb71383098f92810608d7d983</citedby><cites>FETCH-LOGICAL-c274t-8f623324ba33968694f2f6028ba27a1b41c8236aeb71383098f92810608d7d983</cites><orcidid>0000-0002-4392-8728</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.yexmp.2015.03.030$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,45974</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25818166$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Zhihong</creatorcontrib><creatorcontrib>Sun, Baocun</creatorcontrib><creatorcontrib>Li, Yanlei</creatorcontrib><creatorcontrib>Zhao, Xiulan</creatorcontrib><creatorcontrib>Zhao, Xueming</creatorcontrib><creatorcontrib>Gu, Qiang</creatorcontrib><creatorcontrib>An, Jindan</creatorcontrib><creatorcontrib>Dong, Xueyi</creatorcontrib><creatorcontrib>Liu, Fang</creatorcontrib><creatorcontrib>Wang, Yong</creatorcontrib><title>ZEB2 promotes vasculogenic mimicry by TGF-β1 induced epithelial-to-mesenchymal transition in hepatocellular carcinoma</title><title>Experimental and molecular pathology</title><addtitle>Exp Mol Pathol</addtitle><description>Zinc finger E-box binding homeobox 2 (ZEB2), an epithelial–mesenchymal transition (EMT) regulator, has been involved in invasion and metastasis of human tumor. Although EMT may be involved in vasculogenic mimicry (VM) formation, no reports describing the relation between ZEB2 and VM are available. We hypothesize that ZEB2 may promote VM formation in hepatocellular carcinoma (HCC).
Paraffin-embedded tumor tissue samples from 92 patients were immunostained with anti-ZEB2 antibody. We found that the ZEB2 nuclear expression was significantly associated with VM formation and metastasis. Patients with VM and ZEB2 nuclear expression had a shorter survival period than those without expression. In vitro, ZEB2 overexpression significantly enhanced cell motility, invasiveness, and VM formation of HepG2 cells. ZEB2 upregulation also increased VE-cadherin, Flt-1, and Flk-1 expression and activated MMPs. ZEB2 knockdown inhibited cell motility, invasiveness, and VM formation in Bel7402 cells. ZEB2 knockdown also decreased VE-cadherin, Flt-1, and Flk-1 expression and MMP activity. In addition, EMT in HepG2 cells was induced by TGF-β1 treatment, and the kinetics of expression of EMT markers and regulators were assessed by Western blot analysis. The expression of ZEB2 increased significantly, and VM formation was promoted.
ZEB2 can promote VM formation through the EMT pathway. Our findings may represent a novel therapeutic target in HCC.
•ZEB2 nuclear expression was associated with VM formation and metastasis in human hepatocellular carcinoma samples.•ZEB2 overexpression enhanced cell motility, invasiveness, and VM formation of hepatocellular carcinoma cells.•Knockdown of ZEB2 reduced tumor cell migration, invasion, VM formation, and endothelium related markers expression.•Epithelial–mesenchymal transition in hepatocellular carcinoma cells was induced by TGF-β1 treatment.•ZEB2 can promote VM formation through the EMT pathway.</description><subject>Adult</subject><subject>Antigens, CD - genetics</subject><subject>Antigens, CD - metabolism</subject><subject>Cadherins - genetics</subject><subject>Cadherins - metabolism</subject><subject>Carcinoma, Hepatocellular - metabolism</subject><subject>Carcinoma, Hepatocellular - pathology</subject><subject>Epithelial-Mesenchymal Transition</subject><subject>Female</subject><subject>Hep G2 Cells</subject><subject>Hepatocellular carcinoma</subject><subject>Homeodomain Proteins - genetics</subject><subject>Homeodomain Proteins - metabolism</subject><subject>Humans</subject><subject>Liver Neoplasms - metabolism</subject><subject>Liver Neoplasms - pathology</subject><subject>Male</subject><subject>Matrix Metalloproteinases - genetics</subject><subject>Matrix Metalloproteinases - metabolism</subject><subject>Middle Aged</subject><subject>Neovascularization, Pathologic - metabolism</subject><subject>Neovascularization, Pathologic - pathology</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><subject>TGF-β1</subject><subject>Transforming Growth Factor beta1 - pharmacology</subject><subject>Vascular Endothelial Growth Factor Receptor-1 - genetics</subject><subject>Vascular Endothelial Growth Factor Receptor-1 - metabolism</subject><subject>Vascular Endothelial Growth Factor Receptor-2 - genetics</subject><subject>Vascular Endothelial Growth Factor Receptor-2 - metabolism</subject><subject>Vasculogenic mimicry</subject><subject>Zinc Finger E-box Binding Homeobox 2</subject><issn>0014-4800</issn><issn>1096-0945</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kM9u1DAQhy0EokvhCZCQj1yyzNiJ1zlwgKotSJW4lAsXy3EmrFdxHOxk1bwWD8IzkWULR6SR5vLNn9_H2GuELQKqd4ftQg9h3ArAagtyLXjCNgi1KqAuq6dsA4BlUWqAC_Yi5wMA1IDiObsQlUaNSm3Y8dv1R8HHFEOcKPOjzW7u43cavOPBB-_SwpuF39_eFL9-IvdDOztqOY1-2lPvbV9MsQiUaXD7JdieT8kO2U8-DivM9zTaKTrq-7m3iTubnB9isC_Zs872mV499kv29eb6_upTcffl9vPVh7vCiV05FbpTQkpRNlbKWmlVl53oFAjdWLGz2JTotJDKUrNDqSXUuquFRlCg211ba3nJ3p73rgl_zJQnE3w-vWMHinM2qDQKhVWFKyrPqEsx50SdGZMPNi0GwZyEm4P5I9ychBuQa8E69ebxwNwEav_N_DW8Au_PAK0xj56Syc6vtqj1idxk2uj_e-A3s9OT3A</recordid><startdate>201506</startdate><enddate>201506</enddate><creator>Yang, Zhihong</creator><creator>Sun, Baocun</creator><creator>Li, Yanlei</creator><creator>Zhao, Xiulan</creator><creator>Zhao, Xueming</creator><creator>Gu, Qiang</creator><creator>An, Jindan</creator><creator>Dong, Xueyi</creator><creator>Liu, Fang</creator><creator>Wang, Yong</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-4392-8728</orcidid></search><sort><creationdate>201506</creationdate><title>ZEB2 promotes vasculogenic mimicry by TGF-β1 induced epithelial-to-mesenchymal transition in hepatocellular carcinoma</title><author>Yang, Zhihong ; Sun, Baocun ; Li, Yanlei ; Zhao, Xiulan ; Zhao, Xueming ; Gu, Qiang ; An, Jindan ; Dong, Xueyi ; Liu, Fang ; Wang, Yong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c274t-8f623324ba33968694f2f6028ba27a1b41c8236aeb71383098f92810608d7d983</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Adult</topic><topic>Antigens, CD - genetics</topic><topic>Antigens, CD - metabolism</topic><topic>Cadherins - genetics</topic><topic>Cadherins - metabolism</topic><topic>Carcinoma, Hepatocellular - metabolism</topic><topic>Carcinoma, Hepatocellular - pathology</topic><topic>Epithelial-Mesenchymal Transition</topic><topic>Female</topic><topic>Hep G2 Cells</topic><topic>Hepatocellular carcinoma</topic><topic>Homeodomain Proteins - genetics</topic><topic>Homeodomain Proteins - metabolism</topic><topic>Humans</topic><topic>Liver Neoplasms - metabolism</topic><topic>Liver Neoplasms - pathology</topic><topic>Male</topic><topic>Matrix Metalloproteinases - genetics</topic><topic>Matrix Metalloproteinases - metabolism</topic><topic>Middle Aged</topic><topic>Neovascularization, Pathologic - metabolism</topic><topic>Neovascularization, Pathologic - pathology</topic><topic>Repressor Proteins - genetics</topic><topic>Repressor Proteins - metabolism</topic><topic>TGF-β1</topic><topic>Transforming Growth Factor beta1 - pharmacology</topic><topic>Vascular Endothelial Growth Factor Receptor-1 - genetics</topic><topic>Vascular Endothelial Growth Factor Receptor-1 - metabolism</topic><topic>Vascular Endothelial Growth Factor Receptor-2 - genetics</topic><topic>Vascular Endothelial Growth Factor Receptor-2 - metabolism</topic><topic>Vasculogenic mimicry</topic><topic>Zinc Finger E-box Binding Homeobox 2</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Zhihong</creatorcontrib><creatorcontrib>Sun, Baocun</creatorcontrib><creatorcontrib>Li, Yanlei</creatorcontrib><creatorcontrib>Zhao, Xiulan</creatorcontrib><creatorcontrib>Zhao, Xueming</creatorcontrib><creatorcontrib>Gu, Qiang</creatorcontrib><creatorcontrib>An, Jindan</creatorcontrib><creatorcontrib>Dong, Xueyi</creatorcontrib><creatorcontrib>Liu, Fang</creatorcontrib><creatorcontrib>Wang, Yong</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Experimental and molecular pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Zhihong</au><au>Sun, Baocun</au><au>Li, Yanlei</au><au>Zhao, Xiulan</au><au>Zhao, Xueming</au><au>Gu, Qiang</au><au>An, Jindan</au><au>Dong, Xueyi</au><au>Liu, Fang</au><au>Wang, Yong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>ZEB2 promotes vasculogenic mimicry by TGF-β1 induced epithelial-to-mesenchymal transition in hepatocellular carcinoma</atitle><jtitle>Experimental and molecular pathology</jtitle><addtitle>Exp Mol Pathol</addtitle><date>2015-06</date><risdate>2015</risdate><volume>98</volume><issue>3</issue><spage>352</spage><epage>359</epage><pages>352-359</pages><issn>0014-4800</issn><eissn>1096-0945</eissn><abstract>Zinc finger E-box binding homeobox 2 (ZEB2), an epithelial–mesenchymal transition (EMT) regulator, has been involved in invasion and metastasis of human tumor. Although EMT may be involved in vasculogenic mimicry (VM) formation, no reports describing the relation between ZEB2 and VM are available. We hypothesize that ZEB2 may promote VM formation in hepatocellular carcinoma (HCC).
Paraffin-embedded tumor tissue samples from 92 patients were immunostained with anti-ZEB2 antibody. We found that the ZEB2 nuclear expression was significantly associated with VM formation and metastasis. Patients with VM and ZEB2 nuclear expression had a shorter survival period than those without expression. In vitro, ZEB2 overexpression significantly enhanced cell motility, invasiveness, and VM formation of HepG2 cells. ZEB2 upregulation also increased VE-cadherin, Flt-1, and Flk-1 expression and activated MMPs. ZEB2 knockdown inhibited cell motility, invasiveness, and VM formation in Bel7402 cells. ZEB2 knockdown also decreased VE-cadherin, Flt-1, and Flk-1 expression and MMP activity. In addition, EMT in HepG2 cells was induced by TGF-β1 treatment, and the kinetics of expression of EMT markers and regulators were assessed by Western blot analysis. The expression of ZEB2 increased significantly, and VM formation was promoted.
ZEB2 can promote VM formation through the EMT pathway. Our findings may represent a novel therapeutic target in HCC.
•ZEB2 nuclear expression was associated with VM formation and metastasis in human hepatocellular carcinoma samples.•ZEB2 overexpression enhanced cell motility, invasiveness, and VM formation of hepatocellular carcinoma cells.•Knockdown of ZEB2 reduced tumor cell migration, invasion, VM formation, and endothelium related markers expression.•Epithelial–mesenchymal transition in hepatocellular carcinoma cells was induced by TGF-β1 treatment.•ZEB2 can promote VM formation through the EMT pathway.</abstract><cop>Netherlands</cop><pub>Elsevier Inc</pub><pmid>25818166</pmid><doi>10.1016/j.yexmp.2015.03.030</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-4392-8728</orcidid></addata></record> |
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| ispartof | Experimental and molecular pathology, 2015-06, Vol.98 (3), p.352-359 |
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| subjects | Adult Antigens, CD - genetics Antigens, CD - metabolism Cadherins - genetics Cadherins - metabolism Carcinoma, Hepatocellular - metabolism Carcinoma, Hepatocellular - pathology Epithelial-Mesenchymal Transition Female Hep G2 Cells Hepatocellular carcinoma Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Humans Liver Neoplasms - metabolism Liver Neoplasms - pathology Male Matrix Metalloproteinases - genetics Matrix Metalloproteinases - metabolism Middle Aged Neovascularization, Pathologic - metabolism Neovascularization, Pathologic - pathology Repressor Proteins - genetics Repressor Proteins - metabolism TGF-β1 Transforming Growth Factor beta1 - pharmacology Vascular Endothelial Growth Factor Receptor-1 - genetics Vascular Endothelial Growth Factor Receptor-1 - metabolism Vascular Endothelial Growth Factor Receptor-2 - genetics Vascular Endothelial Growth Factor Receptor-2 - metabolism Vasculogenic mimicry Zinc Finger E-box Binding Homeobox 2 |
| title | ZEB2 promotes vasculogenic mimicry by TGF-β1 induced epithelial-to-mesenchymal transition in hepatocellular carcinoma |
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