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Antitumor effects of interleukin-6 (IL-6)/interleukin-6 receptor (IL-6R) signaling pathway inhibition in clear cell carcinoma of the ovary
Among epithelial ovarian cancers, clear cell carcinoma of the ovary (CCC) has unique clinical and molecular characteristics that include chemoresistance resulting in poor prognosis. It was shown that CCC recently was characterized by specific upregulation of the IL‐6/IL‐6R‐signal transducer and acti...
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| Published in: | Molecular carcinogenesis 2016-05, Vol.55 (5), p.832-841 |
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| container_title | Molecular carcinogenesis |
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| creator | Yanaihara, Nozomu Hirata, Yukihiro Yamaguchi, Noriko Noguchi, Yukiko Saito, Misato Nagata, Chie Takakura, Satoshi Yamada, Kyosuke Okamoto, Aikou |
| description | Among epithelial ovarian cancers, clear cell carcinoma of the ovary (CCC) has unique clinical and molecular characteristics that include chemoresistance resulting in poor prognosis. It was shown that CCC recently was characterized by specific upregulation of the IL‐6/IL‐6R‐signal transducer and activator of transcription 3 (Stat3) signaling pathway. In this study, we aim to clarify whether IL‐6/IL‐6R mediated signaling pathway could have clinical relations with CCC and to evaluate inhibitory effects of the pathway on CCC carcinogenesis. A total of 84 CCC cases collected from primary surgical specimens were evaluated by the immunohistochemical analysis for IL‐6R and phosphorylated Stat3 (pStat3), and we found that high IL‐6R expression correlated with poor patient survival both by the univariate and multivariate analyses, suggesting that IL‐6/IL‐6R signaling pathway could be implicated in the progression of CCC. We further investigated the effects of IL‐6/IL‐6R mediated signaling pathway inhibition either by IL‐6R small interfering RNA (siRNA) approach or humanized anti‐human IL‐6R antibody (tocilizumab) in CCC. Inhibition of endogenous IL‐6R including tocilizumab in CCC cells did reduce cell invasion ability and restored their response to cytotoxic reagent. These data suggest that IL‐6/IL‐6R signaling pathway could act on CCC cells to enhance invasion and chemoresistance and, therefore, targeting IL‐6/IL‐6R mediated signaling pathway could be a promising therapeutic strategy for CCC. © 2015 Wiley Periodicals, Inc. |
| doi_str_mv | 10.1002/mc.22325 |
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It was shown that CCC recently was characterized by specific upregulation of the IL‐6/IL‐6R‐signal transducer and activator of transcription 3 (Stat3) signaling pathway. In this study, we aim to clarify whether IL‐6/IL‐6R mediated signaling pathway could have clinical relations with CCC and to evaluate inhibitory effects of the pathway on CCC carcinogenesis. A total of 84 CCC cases collected from primary surgical specimens were evaluated by the immunohistochemical analysis for IL‐6R and phosphorylated Stat3 (pStat3), and we found that high IL‐6R expression correlated with poor patient survival both by the univariate and multivariate analyses, suggesting that IL‐6/IL‐6R signaling pathway could be implicated in the progression of CCC. We further investigated the effects of IL‐6/IL‐6R mediated signaling pathway inhibition either by IL‐6R small interfering RNA (siRNA) approach or humanized anti‐human IL‐6R antibody (tocilizumab) in CCC. Inhibition of endogenous IL‐6R including tocilizumab in CCC cells did reduce cell invasion ability and restored their response to cytotoxic reagent. These data suggest that IL‐6/IL‐6R signaling pathway could act on CCC cells to enhance invasion and chemoresistance and, therefore, targeting IL‐6/IL‐6R mediated signaling pathway could be a promising therapeutic strategy for CCC. © 2015 Wiley Periodicals, Inc.</description><identifier>ISSN: 0899-1987</identifier><identifier>EISSN: 1098-2744</identifier><identifier>DOI: 10.1002/mc.22325</identifier><identifier>PMID: 25856562</identifier><language>eng</language><publisher>United States: Blackwell Publishing Ltd</publisher><subject>Adenocarcinoma, Clear Cell - genetics ; Adenocarcinoma, Clear Cell - metabolism ; Adenocarcinoma, Clear Cell - pathology ; Antibodies, Monoclonal, Humanized - pharmacology ; Antineoplastic Agents - pharmacology ; Antitumor activity ; Carcinogenesis ; Cell Line, Tumor ; Cell Movement - drug effects ; Cell Proliferation - drug effects ; Cell Survival - drug effects ; Chemoresistance ; Chemotherapy ; clear cell carcinoma of the ovary ; Cytokines ; Cytotoxicity ; Drug resistance ; Female ; Gene Expression Regulation, Neoplastic - drug effects ; Humans ; IL-6 ; IL-6R ; Inhibition ; Interleukin 6 ; Interleukin-6 - genetics ; Interleukin-6 - metabolism ; Kinases ; Medical prognosis ; Ovarian cancer ; Ovarian Neoplasms - genetics ; Ovarian Neoplasms - metabolism ; Ovarian Neoplasms - pathology ; Phosphorylation - drug effects ; Prognosis ; Receptors, Interleukin-6 - genetics ; Receptors, Interleukin-6 - metabolism ; Signal transduction ; Signal Transduction - drug effects ; siRNA ; Stat3 ; Stat3 protein ; STAT3 Transcription Factor - metabolism ; tocilizumab ; Transcription ; Tumors</subject><ispartof>Molecular carcinogenesis, 2016-05, Vol.55 (5), p.832-841</ispartof><rights>2015 Wiley Periodicals, Inc.</rights><rights>2016 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4485-35af5f93ecf43f66f20a028c13eb9c85ffbc4f2a2f14dd1e400aa1bb9f84f4753</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fmc.22325$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fmc.22325$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,786,790,27957,27958,50923,51032</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25856562$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yanaihara, Nozomu</creatorcontrib><creatorcontrib>Hirata, Yukihiro</creatorcontrib><creatorcontrib>Yamaguchi, Noriko</creatorcontrib><creatorcontrib>Noguchi, Yukiko</creatorcontrib><creatorcontrib>Saito, Misato</creatorcontrib><creatorcontrib>Nagata, Chie</creatorcontrib><creatorcontrib>Takakura, Satoshi</creatorcontrib><creatorcontrib>Yamada, Kyosuke</creatorcontrib><creatorcontrib>Okamoto, Aikou</creatorcontrib><title>Antitumor effects of interleukin-6 (IL-6)/interleukin-6 receptor (IL-6R) signaling pathway inhibition in clear cell carcinoma of the ovary</title><title>Molecular carcinogenesis</title><addtitle>Mol. Carcinog</addtitle><description>Among epithelial ovarian cancers, clear cell carcinoma of the ovary (CCC) has unique clinical and molecular characteristics that include chemoresistance resulting in poor prognosis. It was shown that CCC recently was characterized by specific upregulation of the IL‐6/IL‐6R‐signal transducer and activator of transcription 3 (Stat3) signaling pathway. In this study, we aim to clarify whether IL‐6/IL‐6R mediated signaling pathway could have clinical relations with CCC and to evaluate inhibitory effects of the pathway on CCC carcinogenesis. A total of 84 CCC cases collected from primary surgical specimens were evaluated by the immunohistochemical analysis for IL‐6R and phosphorylated Stat3 (pStat3), and we found that high IL‐6R expression correlated with poor patient survival both by the univariate and multivariate analyses, suggesting that IL‐6/IL‐6R signaling pathway could be implicated in the progression of CCC. We further investigated the effects of IL‐6/IL‐6R mediated signaling pathway inhibition either by IL‐6R small interfering RNA (siRNA) approach or humanized anti‐human IL‐6R antibody (tocilizumab) in CCC. Inhibition of endogenous IL‐6R including tocilizumab in CCC cells did reduce cell invasion ability and restored their response to cytotoxic reagent. These data suggest that IL‐6/IL‐6R signaling pathway could act on CCC cells to enhance invasion and chemoresistance and, therefore, targeting IL‐6/IL‐6R mediated signaling pathway could be a promising therapeutic strategy for CCC. © 2015 Wiley Periodicals, Inc.</description><subject>Adenocarcinoma, Clear Cell - genetics</subject><subject>Adenocarcinoma, Clear Cell - metabolism</subject><subject>Adenocarcinoma, Clear Cell - pathology</subject><subject>Antibodies, Monoclonal, Humanized - pharmacology</subject><subject>Antineoplastic Agents - pharmacology</subject><subject>Antitumor activity</subject><subject>Carcinogenesis</subject><subject>Cell Line, Tumor</subject><subject>Cell Movement - drug effects</subject><subject>Cell Proliferation - drug effects</subject><subject>Cell Survival - drug effects</subject><subject>Chemoresistance</subject><subject>Chemotherapy</subject><subject>clear cell carcinoma of the ovary</subject><subject>Cytokines</subject><subject>Cytotoxicity</subject><subject>Drug resistance</subject><subject>Female</subject><subject>Gene Expression Regulation, Neoplastic - drug effects</subject><subject>Humans</subject><subject>IL-6</subject><subject>IL-6R</subject><subject>Inhibition</subject><subject>Interleukin 6</subject><subject>Interleukin-6 - genetics</subject><subject>Interleukin-6 - metabolism</subject><subject>Kinases</subject><subject>Medical prognosis</subject><subject>Ovarian cancer</subject><subject>Ovarian Neoplasms - genetics</subject><subject>Ovarian Neoplasms - metabolism</subject><subject>Ovarian Neoplasms - pathology</subject><subject>Phosphorylation - drug effects</subject><subject>Prognosis</subject><subject>Receptors, Interleukin-6 - genetics</subject><subject>Receptors, Interleukin-6 - metabolism</subject><subject>Signal transduction</subject><subject>Signal Transduction - drug effects</subject><subject>siRNA</subject><subject>Stat3</subject><subject>Stat3 protein</subject><subject>STAT3 Transcription Factor - metabolism</subject><subject>tocilizumab</subject><subject>Transcription</subject><subject>Tumors</subject><issn>0899-1987</issn><issn>1098-2744</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><recordid>eNp9kctO3DAUhq2qqAy0Ek-ALHVTFgHbsWN7iaJ2uEypWlGxtBzPMWPIZeo4wLwCT00YKIgNq3N0_u_cEdqhZJ8Swg4at89YzsQHNKFEq4xJzj-iCVFaZ1QruYm2-v6KEEqlIJ_QJhNKFKJgE3R_2KaQhqaLGLwHl3rceRzaBLGG4Tq0WYG_Hc-yYu_gbTCCg2Ua09bqnz3ch8vW1qG9xEubFrd2NVZZhCqk0LWji10NNmIHdY2djS60XWMfe6UF4O7GxtVntOFt3cOXZ7uN_v74fl4eZbNf0-PycJY5zpXIcmG98DoH53nui8IzYglTjuZQaaeE95XjnlnmKZ_PKXBCrKVVpb3inkuRb6OvT3WXsfs3QJ_MVTfEcfbeUKUFpUJr-S4lFSFEaspGaveZGqoG5mYZQzOuYv4feASyJ-A21LB60Skxj48zjTPrx5mf5dq-8qFPcPfC23htCplLYS7Opqa8KI5-l6fn5iR_ALMOmIA</recordid><startdate>201605</startdate><enddate>201605</enddate><creator>Yanaihara, Nozomu</creator><creator>Hirata, Yukihiro</creator><creator>Yamaguchi, Noriko</creator><creator>Noguchi, Yukiko</creator><creator>Saito, Misato</creator><creator>Nagata, Chie</creator><creator>Takakura, Satoshi</creator><creator>Yamada, Kyosuke</creator><creator>Okamoto, Aikou</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7TM</scope><scope>7TO</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>RC3</scope></search><sort><creationdate>201605</creationdate><title>Antitumor effects of interleukin-6 (IL-6)/interleukin-6 receptor (IL-6R) signaling pathway inhibition in clear cell carcinoma of the ovary</title><author>Yanaihara, Nozomu ; Hirata, Yukihiro ; Yamaguchi, Noriko ; Noguchi, Yukiko ; Saito, Misato ; Nagata, Chie ; Takakura, Satoshi ; Yamada, Kyosuke ; Okamoto, Aikou</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4485-35af5f93ecf43f66f20a028c13eb9c85ffbc4f2a2f14dd1e400aa1bb9f84f4753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adenocarcinoma, Clear Cell - genetics</topic><topic>Adenocarcinoma, Clear Cell - metabolism</topic><topic>Adenocarcinoma, Clear Cell - pathology</topic><topic>Antibodies, Monoclonal, Humanized - pharmacology</topic><topic>Antineoplastic Agents - pharmacology</topic><topic>Antitumor activity</topic><topic>Carcinogenesis</topic><topic>Cell Line, Tumor</topic><topic>Cell Movement - drug effects</topic><topic>Cell Proliferation - drug effects</topic><topic>Cell Survival - drug effects</topic><topic>Chemoresistance</topic><topic>Chemotherapy</topic><topic>clear cell carcinoma of the ovary</topic><topic>Cytokines</topic><topic>Cytotoxicity</topic><topic>Drug resistance</topic><topic>Female</topic><topic>Gene Expression Regulation, Neoplastic - drug effects</topic><topic>Humans</topic><topic>IL-6</topic><topic>IL-6R</topic><topic>Inhibition</topic><topic>Interleukin 6</topic><topic>Interleukin-6 - genetics</topic><topic>Interleukin-6 - metabolism</topic><topic>Kinases</topic><topic>Medical prognosis</topic><topic>Ovarian cancer</topic><topic>Ovarian Neoplasms - genetics</topic><topic>Ovarian Neoplasms - metabolism</topic><topic>Ovarian Neoplasms - pathology</topic><topic>Phosphorylation - drug effects</topic><topic>Prognosis</topic><topic>Receptors, Interleukin-6 - genetics</topic><topic>Receptors, Interleukin-6 - metabolism</topic><topic>Signal transduction</topic><topic>Signal Transduction - drug effects</topic><topic>siRNA</topic><topic>Stat3</topic><topic>Stat3 protein</topic><topic>STAT3 Transcription Factor - metabolism</topic><topic>tocilizumab</topic><topic>Transcription</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yanaihara, Nozomu</creatorcontrib><creatorcontrib>Hirata, Yukihiro</creatorcontrib><creatorcontrib>Yamaguchi, Noriko</creatorcontrib><creatorcontrib>Noguchi, Yukiko</creatorcontrib><creatorcontrib>Saito, Misato</creatorcontrib><creatorcontrib>Nagata, Chie</creatorcontrib><creatorcontrib>Takakura, Satoshi</creatorcontrib><creatorcontrib>Yamada, Kyosuke</creatorcontrib><creatorcontrib>Okamoto, Aikou</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>Molecular carcinogenesis</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yanaihara, Nozomu</au><au>Hirata, Yukihiro</au><au>Yamaguchi, Noriko</au><au>Noguchi, Yukiko</au><au>Saito, Misato</au><au>Nagata, Chie</au><au>Takakura, Satoshi</au><au>Yamada, Kyosuke</au><au>Okamoto, Aikou</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Antitumor effects of interleukin-6 (IL-6)/interleukin-6 receptor (IL-6R) signaling pathway inhibition in clear cell carcinoma of the ovary</atitle><jtitle>Molecular carcinogenesis</jtitle><addtitle>Mol. Carcinog</addtitle><date>2016-05</date><risdate>2016</risdate><volume>55</volume><issue>5</issue><spage>832</spage><epage>841</epage><pages>832-841</pages><issn>0899-1987</issn><eissn>1098-2744</eissn><notes>JSPS KAKENHI - No. 25462615; No. 25462616</notes><notes>istex:F75C81380120200C842670F58C8073E3B57046B3</notes><notes>ark:/67375/WNG-CW6HQCKT-J</notes><notes>ArticleID:MC22325</notes><notes>The Jikei University Research Fund</notes><abstract>Among epithelial ovarian cancers, clear cell carcinoma of the ovary (CCC) has unique clinical and molecular characteristics that include chemoresistance resulting in poor prognosis. It was shown that CCC recently was characterized by specific upregulation of the IL‐6/IL‐6R‐signal transducer and activator of transcription 3 (Stat3) signaling pathway. In this study, we aim to clarify whether IL‐6/IL‐6R mediated signaling pathway could have clinical relations with CCC and to evaluate inhibitory effects of the pathway on CCC carcinogenesis. A total of 84 CCC cases collected from primary surgical specimens were evaluated by the immunohistochemical analysis for IL‐6R and phosphorylated Stat3 (pStat3), and we found that high IL‐6R expression correlated with poor patient survival both by the univariate and multivariate analyses, suggesting that IL‐6/IL‐6R signaling pathway could be implicated in the progression of CCC. We further investigated the effects of IL‐6/IL‐6R mediated signaling pathway inhibition either by IL‐6R small interfering RNA (siRNA) approach or humanized anti‐human IL‐6R antibody (tocilizumab) in CCC. Inhibition of endogenous IL‐6R including tocilizumab in CCC cells did reduce cell invasion ability and restored their response to cytotoxic reagent. These data suggest that IL‐6/IL‐6R signaling pathway could act on CCC cells to enhance invasion and chemoresistance and, therefore, targeting IL‐6/IL‐6R mediated signaling pathway could be a promising therapeutic strategy for CCC. © 2015 Wiley Periodicals, Inc.</abstract><cop>United States</cop><pub>Blackwell Publishing Ltd</pub><pmid>25856562</pmid><doi>10.1002/mc.22325</doi><tpages>10</tpages></addata></record> |
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| subjects | Adenocarcinoma, Clear Cell - genetics Adenocarcinoma, Clear Cell - metabolism Adenocarcinoma, Clear Cell - pathology Antibodies, Monoclonal, Humanized - pharmacology Antineoplastic Agents - pharmacology Antitumor activity Carcinogenesis Cell Line, Tumor Cell Movement - drug effects Cell Proliferation - drug effects Cell Survival - drug effects Chemoresistance Chemotherapy clear cell carcinoma of the ovary Cytokines Cytotoxicity Drug resistance Female Gene Expression Regulation, Neoplastic - drug effects Humans IL-6 IL-6R Inhibition Interleukin 6 Interleukin-6 - genetics Interleukin-6 - metabolism Kinases Medical prognosis Ovarian cancer Ovarian Neoplasms - genetics Ovarian Neoplasms - metabolism Ovarian Neoplasms - pathology Phosphorylation - drug effects Prognosis Receptors, Interleukin-6 - genetics Receptors, Interleukin-6 - metabolism Signal transduction Signal Transduction - drug effects siRNA Stat3 Stat3 protein STAT3 Transcription Factor - metabolism tocilizumab Transcription Tumors |
| title | Antitumor effects of interleukin-6 (IL-6)/interleukin-6 receptor (IL-6R) signaling pathway inhibition in clear cell carcinoma of the ovary |
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