p75 neurotrophin receptor expression is a characteristic of the mitotically quiescent cancer stem cell population present in esophageal squamous cell carcinoma
Mitotically quiescent cancer stem cells (CSC) are hypothesized to exhibit a more aggressive phenotype involving greater therapeutic resistance and metastasis. The aim of our study was to develop a method for identifying quiescent CSC in esophageal squamous cell carcinoma (ESCC) based on their expres...
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| Veröffentlicht in: | International journal of oncology 2016-05, Vol.48 (5), p.1943-1954 |
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| creator | YAMAGUCHI, TETSUJI OKUMURA, TOMOYUKI HIRANO, KATSUHISA WATANABE, TORU NAGATA, TAKUYA SHIMADA, YUTAKA TSUKADA, KAZUHIRO |
| description | Mitotically quiescent cancer stem cells (CSC) are hypothesized to exhibit a more aggressive phenotype involving greater therapeutic resistance and metastasis. The aim of our study was to develop a method for identifying quiescent CSC in esophageal squamous cell carcinoma (ESCC) based on their expression of the p75 neurotrophin receptor (p75NTR) and other proposed CSC markers, such as CD44 and CD90. Double immunostaining of surgical ESCC specimens revealed that the mean Ki-67-labeling index of the p75NTR-positive cells was significantly lower than that of the p75NTR-negative cells. Real-time PCR analysis of sorted fractions of ESCC cell lines (KYSE cells) revealed that stem cell-related genes (Nanog, p63 and Bmi-1) and epithelial-mesenchymal transition (EMT)-related genes (N-cadherin and fibronectin) were expressed at significantly higher levels in the p75NTR-positive fractions than in the CD44-positive or CD90-positive fractions. In addition, the p75NTR-positive fractions exhibited significantly higher colony formation in vitro, significantly enhanced tumor formation in mice, and significantly greater chemoresistance against cisplatin (CDDP) than the CD44-positive or CD90-positive fractions. Furthermore, in both the cultured cells and those from the mouse xenograft tumors, the p75NTR-positive/CD44-negative and p75NTR-positive/CD90-negative KYSE cell fractions contained significantly higher proportions of mitotically quiescent cells. These results suggest that the mitotically quiescent CSC population in ESCC can be identified and isolated based on their p75NTR expression, providing researchers with a novel diagnostic and therapeutic target. |
| doi_str_mv | 10.3892/ijo.2016.3432 |
| format | Article |
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The aim of our study was to develop a method for identifying quiescent CSC in esophageal squamous cell carcinoma (ESCC) based on their expression of the p75 neurotrophin receptor (p75NTR) and other proposed CSC markers, such as CD44 and CD90. Double immunostaining of surgical ESCC specimens revealed that the mean Ki-67-labeling index of the p75NTR-positive cells was significantly lower than that of the p75NTR-negative cells. Real-time PCR analysis of sorted fractions of ESCC cell lines (KYSE cells) revealed that stem cell-related genes (Nanog, p63 and Bmi-1) and epithelial-mesenchymal transition (EMT)-related genes (N-cadherin and fibronectin) were expressed at significantly higher levels in the p75NTR-positive fractions than in the CD44-positive or CD90-positive fractions. In addition, the p75NTR-positive fractions exhibited significantly higher colony formation in vitro, significantly enhanced tumor formation in mice, and significantly greater chemoresistance against cisplatin (CDDP) than the CD44-positive or CD90-positive fractions. Furthermore, in both the cultured cells and those from the mouse xenograft tumors, the p75NTR-positive/CD44-negative and p75NTR-positive/CD90-negative KYSE cell fractions contained significantly higher proportions of mitotically quiescent cells. These results suggest that the mitotically quiescent CSC population in ESCC can be identified and isolated based on their p75NTR expression, providing researchers with a novel diagnostic and therapeutic target.</description><identifier>ISSN: 1019-6439</identifier><identifier>EISSN: 1791-2423</identifier><identifier>DOI: 10.3892/ijo.2016.3432</identifier><identifier>PMID: 26984177</identifier><language>eng</language><publisher>Greece: D.A. Spandidos</publisher><subject>Aged ; Animals ; Cancer ; Cancer cells ; cancer stem cell ; Carcinoma, Squamous Cell - metabolism ; Carcinoma, Squamous Cell - pathology ; Care and treatment ; CD271 ; CD44 ; CD90 ; Cell cycle ; Cell Line, Tumor ; Cell receptors ; Cisplatin - pharmacology ; Cloning ; Development and progression ; Drug Resistance, Neoplasm ; Epithelial-Mesenchymal Transition ; Esophageal cancer ; Esophageal Neoplasms - metabolism ; Esophageal Neoplasms - pathology ; Esophageal Squamous Cell Carcinoma ; Esophagus ; Female ; Gene expression ; Gene Expression Regulation, Neoplastic ; Genetic aspects ; Humans ; Identification and classification ; Immunoglobulins ; Innovations ; Male ; Medical research ; Mice ; Middle Aged ; Mitosis ; Molecular targeted therapy ; Neoplasm Transplantation ; Neoplastic Stem Cells - metabolism ; Neoplastic Stem Cells - pathology ; Nerve Tissue Proteins - metabolism ; p75NTR ; Patients ; Polymerase chain reaction ; Properties ; Receptors, Nerve Growth Factor - metabolism ; Squamous cell carcinoma ; Stem cells ; Studies ; Tissue Array Analysis - methods</subject><ispartof>International journal of oncology, 2016-05, Vol.48 (5), p.1943-1954</ispartof><rights>Copyright © 2016, Spandidos Publications</rights><rights>COPYRIGHT 2016 Spandidos Publications</rights><rights>Copyright Spandidos Publications UK Ltd. 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c556t-ab88d3f0ce4d8d0315ca9f1c874e598f3e1ce4fc697e5a22f437f8bc709856253</citedby><cites>FETCH-LOGICAL-c556t-ab88d3f0ce4d8d0315ca9f1c874e598f3e1ce4fc697e5a22f437f8bc709856253</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,5556,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26984177$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>YAMAGUCHI, TETSUJI</creatorcontrib><creatorcontrib>OKUMURA, TOMOYUKI</creatorcontrib><creatorcontrib>HIRANO, KATSUHISA</creatorcontrib><creatorcontrib>WATANABE, TORU</creatorcontrib><creatorcontrib>NAGATA, TAKUYA</creatorcontrib><creatorcontrib>SHIMADA, YUTAKA</creatorcontrib><creatorcontrib>TSUKADA, KAZUHIRO</creatorcontrib><title>p75 neurotrophin receptor expression is a characteristic of the mitotically quiescent cancer stem cell population present in esophageal squamous cell carcinoma</title><title>International journal of oncology</title><addtitle>Int J Oncol</addtitle><description>Mitotically quiescent cancer stem cells (CSC) are hypothesized to exhibit a more aggressive phenotype involving greater therapeutic resistance and metastasis. The aim of our study was to develop a method for identifying quiescent CSC in esophageal squamous cell carcinoma (ESCC) based on their expression of the p75 neurotrophin receptor (p75NTR) and other proposed CSC markers, such as CD44 and CD90. Double immunostaining of surgical ESCC specimens revealed that the mean Ki-67-labeling index of the p75NTR-positive cells was significantly lower than that of the p75NTR-negative cells. Real-time PCR analysis of sorted fractions of ESCC cell lines (KYSE cells) revealed that stem cell-related genes (Nanog, p63 and Bmi-1) and epithelial-mesenchymal transition (EMT)-related genes (N-cadherin and fibronectin) were expressed at significantly higher levels in the p75NTR-positive fractions than in the CD44-positive or CD90-positive fractions. In addition, the p75NTR-positive fractions exhibited significantly higher colony formation in vitro, significantly enhanced tumor formation in mice, and significantly greater chemoresistance against cisplatin (CDDP) than the CD44-positive or CD90-positive fractions. Furthermore, in both the cultured cells and those from the mouse xenograft tumors, the p75NTR-positive/CD44-negative and p75NTR-positive/CD90-negative KYSE cell fractions contained significantly higher proportions of mitotically quiescent cells. These results suggest that the mitotically quiescent CSC population in ESCC can be identified and isolated based on their p75NTR expression, providing researchers with a novel diagnostic and therapeutic target.</description><subject>Aged</subject><subject>Animals</subject><subject>Cancer</subject><subject>Cancer cells</subject><subject>cancer stem cell</subject><subject>Carcinoma, Squamous Cell - metabolism</subject><subject>Carcinoma, Squamous Cell - pathology</subject><subject>Care and treatment</subject><subject>CD271</subject><subject>CD44</subject><subject>CD90</subject><subject>Cell cycle</subject><subject>Cell Line, Tumor</subject><subject>Cell receptors</subject><subject>Cisplatin - pharmacology</subject><subject>Cloning</subject><subject>Development and progression</subject><subject>Drug Resistance, Neoplasm</subject><subject>Epithelial-Mesenchymal Transition</subject><subject>Esophageal cancer</subject><subject>Esophageal Neoplasms - metabolism</subject><subject>Esophageal Neoplasms - pathology</subject><subject>Esophageal Squamous Cell Carcinoma</subject><subject>Esophagus</subject><subject>Female</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Genetic aspects</subject><subject>Humans</subject><subject>Identification and classification</subject><subject>Immunoglobulins</subject><subject>Innovations</subject><subject>Male</subject><subject>Medical research</subject><subject>Mice</subject><subject>Middle Aged</subject><subject>Mitosis</subject><subject>Molecular targeted therapy</subject><subject>Neoplasm Transplantation</subject><subject>Neoplastic Stem Cells - metabolism</subject><subject>Neoplastic Stem Cells - pathology</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>p75NTR</subject><subject>Patients</subject><subject>Polymerase chain reaction</subject><subject>Properties</subject><subject>Receptors, Nerve Growth Factor - metabolism</subject><subject>Squamous cell carcinoma</subject><subject>Stem cells</subject><subject>Studies</subject><subject>Tissue Array Analysis - methods</subject><issn>1019-6439</issn><issn>1791-2423</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNptkk1rFTEUhgdRbK0u3UpAsKu55nMmWZaiVSi40XXIzZx0cplJ5iYZsL_Gv2qGW6sFySJfz3kPefM2zVuCd0wq-tEf4o5i0u0YZ_RZc056RVrKKXte15iotuNMnTWvcj5gTIXA5GVzRjslOen78-bX0gsUYE2xpLiMPqAEFpYSE4KfS4KcfQzIZ2SQHU0ytkDyuXiLokNlBDT7EuvWTNM9Oq4esoVQkDXBQkK5wIwsTBNa4rJOpmxim-rG1F6Qa09zB2ZC-biaOa75hFuTrA9xNq-bF85MGd48zBfNj8-fvl9_aW-_3Xy9vrptrRBdac1eyoE5bIEPcsCMCGuUI1b2HISSjgGpV852qgdhKHWc9U7ubY-VFB0V7KJ5f9JdUjyukIs-xDWF2lITxSjDSlDyl7ozE2gfXHXN2Nlnq6941ZGqo6xSu_9QdQwwexsDOF_PnxR8-KdgrHaUMcdp3ezKT8H2BNoUc07g9JL8bNK9JlhvcdA1DnqLg97iUPl3D69a9zMMj_Sf_6_A5QnIiwmDH2J-ZKpSy2WLRUsUZ-w3nP6_mg</recordid><startdate>20160501</startdate><enddate>20160501</enddate><creator>YAMAGUCHI, TETSUJI</creator><creator>OKUMURA, TOMOYUKI</creator><creator>HIRANO, KATSUHISA</creator><creator>WATANABE, TORU</creator><creator>NAGATA, TAKUYA</creator><creator>SHIMADA, YUTAKA</creator><creator>TSUKADA, KAZUHIRO</creator><general>D.A. Spandidos</general><general>Spandidos Publications</general><general>Spandidos Publications UK Ltd</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>3V.</scope><scope>7RV</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AN0</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>KB0</scope><scope>M0S</scope><scope>M1P</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope></search><sort><creationdate>20160501</creationdate><title>p75 neurotrophin receptor expression is a characteristic of the mitotically quiescent cancer stem cell population present in esophageal squamous cell carcinoma</title><author>YAMAGUCHI, TETSUJI ; OKUMURA, TOMOYUKI ; HIRANO, KATSUHISA ; WATANABE, TORU ; NAGATA, TAKUYA ; SHIMADA, YUTAKA ; TSUKADA, KAZUHIRO</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c556t-ab88d3f0ce4d8d0315ca9f1c874e598f3e1ce4fc697e5a22f437f8bc709856253</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Aged</topic><topic>Animals</topic><topic>Cancer</topic><topic>Cancer cells</topic><topic>cancer stem cell</topic><topic>Carcinoma, Squamous Cell - metabolism</topic><topic>Carcinoma, Squamous Cell - pathology</topic><topic>Care and treatment</topic><topic>CD271</topic><topic>CD44</topic><topic>CD90</topic><topic>Cell cycle</topic><topic>Cell Line, Tumor</topic><topic>Cell receptors</topic><topic>Cisplatin - pharmacology</topic><topic>Cloning</topic><topic>Development and progression</topic><topic>Drug Resistance, Neoplasm</topic><topic>Epithelial-Mesenchymal Transition</topic><topic>Esophageal cancer</topic><topic>Esophageal Neoplasms - metabolism</topic><topic>Esophageal Neoplasms - pathology</topic><topic>Esophageal Squamous Cell Carcinoma</topic><topic>Esophagus</topic><topic>Female</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Neoplastic</topic><topic>Genetic aspects</topic><topic>Humans</topic><topic>Identification and classification</topic><topic>Immunoglobulins</topic><topic>Innovations</topic><topic>Male</topic><topic>Medical research</topic><topic>Mice</topic><topic>Middle Aged</topic><topic>Mitosis</topic><topic>Molecular targeted therapy</topic><topic>Neoplasm Transplantation</topic><topic>Neoplastic Stem Cells - metabolism</topic><topic>Neoplastic Stem Cells - pathology</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>p75NTR</topic><topic>Patients</topic><topic>Polymerase chain reaction</topic><topic>Properties</topic><topic>Receptors, Nerve Growth Factor - metabolism</topic><topic>Squamous cell carcinoma</topic><topic>Stem cells</topic><topic>Studies</topic><topic>Tissue Array Analysis - methods</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>YAMAGUCHI, TETSUJI</creatorcontrib><creatorcontrib>OKUMURA, TOMOYUKI</creatorcontrib><creatorcontrib>HIRANO, KATSUHISA</creatorcontrib><creatorcontrib>WATANABE, TORU</creatorcontrib><creatorcontrib>NAGATA, TAKUYA</creatorcontrib><creatorcontrib>SHIMADA, YUTAKA</creatorcontrib><creatorcontrib>TSUKADA, KAZUHIRO</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Nursing & Allied Health Database</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>British Nursing Database</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Nursing & Allied Health Premium</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><jtitle>International journal of oncology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>YAMAGUCHI, TETSUJI</au><au>OKUMURA, TOMOYUKI</au><au>HIRANO, KATSUHISA</au><au>WATANABE, TORU</au><au>NAGATA, TAKUYA</au><au>SHIMADA, YUTAKA</au><au>TSUKADA, KAZUHIRO</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>p75 neurotrophin receptor expression is a characteristic of the mitotically quiescent cancer stem cell population present in esophageal squamous cell carcinoma</atitle><jtitle>International journal of oncology</jtitle><addtitle>Int J Oncol</addtitle><date>2016-05-01</date><risdate>2016</risdate><volume>48</volume><issue>5</issue><spage>1943</spage><epage>1954</epage><pages>1943-1954</pages><issn>1019-6439</issn><eissn>1791-2423</eissn><abstract>Mitotically quiescent cancer stem cells (CSC) are hypothesized to exhibit a more aggressive phenotype involving greater therapeutic resistance and metastasis. The aim of our study was to develop a method for identifying quiescent CSC in esophageal squamous cell carcinoma (ESCC) based on their expression of the p75 neurotrophin receptor (p75NTR) and other proposed CSC markers, such as CD44 and CD90. Double immunostaining of surgical ESCC specimens revealed that the mean Ki-67-labeling index of the p75NTR-positive cells was significantly lower than that of the p75NTR-negative cells. Real-time PCR analysis of sorted fractions of ESCC cell lines (KYSE cells) revealed that stem cell-related genes (Nanog, p63 and Bmi-1) and epithelial-mesenchymal transition (EMT)-related genes (N-cadherin and fibronectin) were expressed at significantly higher levels in the p75NTR-positive fractions than in the CD44-positive or CD90-positive fractions. In addition, the p75NTR-positive fractions exhibited significantly higher colony formation in vitro, significantly enhanced tumor formation in mice, and significantly greater chemoresistance against cisplatin (CDDP) than the CD44-positive or CD90-positive fractions. Furthermore, in both the cultured cells and those from the mouse xenograft tumors, the p75NTR-positive/CD44-negative and p75NTR-positive/CD90-negative KYSE cell fractions contained significantly higher proportions of mitotically quiescent cells. These results suggest that the mitotically quiescent CSC population in ESCC can be identified and isolated based on their p75NTR expression, providing researchers with a novel diagnostic and therapeutic target.</abstract><cop>Greece</cop><pub>D.A. Spandidos</pub><pmid>26984177</pmid><doi>10.3892/ijo.2016.3432</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1019-6439 |
| ispartof | International journal of oncology, 2016-05, Vol.48 (5), p.1943-1954 |
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| source | Spandidos Publications Journals; MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection |
| subjects | Aged Animals Cancer Cancer cells cancer stem cell Carcinoma, Squamous Cell - metabolism Carcinoma, Squamous Cell - pathology Care and treatment CD271 CD44 CD90 Cell cycle Cell Line, Tumor Cell receptors Cisplatin - pharmacology Cloning Development and progression Drug Resistance, Neoplasm Epithelial-Mesenchymal Transition Esophageal cancer Esophageal Neoplasms - metabolism Esophageal Neoplasms - pathology Esophageal Squamous Cell Carcinoma Esophagus Female Gene expression Gene Expression Regulation, Neoplastic Genetic aspects Humans Identification and classification Immunoglobulins Innovations Male Medical research Mice Middle Aged Mitosis Molecular targeted therapy Neoplasm Transplantation Neoplastic Stem Cells - metabolism Neoplastic Stem Cells - pathology Nerve Tissue Proteins - metabolism p75NTR Patients Polymerase chain reaction Properties Receptors, Nerve Growth Factor - metabolism Squamous cell carcinoma Stem cells Studies Tissue Array Analysis - methods |
| title | p75 neurotrophin receptor expression is a characteristic of the mitotically quiescent cancer stem cell population present in esophageal squamous cell carcinoma |
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