Cyclin G2 inhibits epithelial-to-mesenchymal transition by disrupting Wnt/β-catenin signaling
Epithelial ovarian cancer (EOC) has the highest mortality rate among gynecological malignancies owing to poor screening methods, non-specific symptoms and limited knowledge of the cellular targets that contribute to the disease. Cyclin G2 is an unconventional cyclin that acts to oppose cell cycle pr...
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| Veröffentlicht in: | Oncogene 2016-09, Vol.35 (36), p.4816-4827 |
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| creator | Bernaudo, S Salem, M Qi, X Zhou, W Zhang, C Yang, W Rosman, D Deng, Z Ye, G Yang, B Vanderhyden, B Wu, Z Peng, C |
| description | Epithelial ovarian cancer (EOC) has the highest mortality rate among gynecological malignancies owing to poor screening methods, non-specific symptoms and limited knowledge of the cellular targets that contribute to the disease. Cyclin G2 is an unconventional cyclin that acts to oppose cell cycle progression. Dysregulation of the cyclin G2 gene (
CCNG2
) in a variety of human cancers has been reported; however, the role of cyclin G2 in tumorigenesis remains unclear. In this study, we investigated the function of cyclin G2 in EOC.
In vitro
and
in vivo
studies using several EOC-derived tumor cell lines revealed that cyclin G2 inhibited cell proliferation, migration, invasion and spheroid formation, as well as tumor formation and invasion. By interrogating cDNA microarray data sets, we found that
CCGN2
mRNA is reduced in several large cohorts of human ovarian carcinoma when compared with normal ovarian surface epithelium or borderline tumors of the ovary. Mechanistically, cyclin G2 was found to suppress epithelial-to-mesenchymal transition (EMT), as demonstrated by the differential regulation of various EMT genes, such as Snail, Slug, vimentin and E-cadherin. Moreover, cyclin G2 potently suppressed the Wnt/β-catenin signaling pathway by downregulating key Wnt components, namely LRP6, DVL2 and β-catenin, which could be linked to inhibition of EMT. Taken together, our novel findings demonstrate that cyclin G2 has potent tumor-suppressive effects in EOCs by inhibiting EMT through attenuating Wnt/β-catenin signaling. |
| doi_str_mv | 10.1038/onc.2016.15 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5024152</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1827889343</sourcerecordid><originalsourceid>FETCH-LOGICAL-c451t-682f9cc6442df7fb91c51fd4d6c88ffbbaad0299b242015b23576ec41da6e2c03</originalsourceid><addsrcrecordid>eNptkctKxDAUhoMoOl5W7qVLQTsmaZI2G0EGHQXBjeLOkKZpJ9ImY5IK81o-iM9kZFQUXJ3F-fjO5QfgEMEpgkV15qyaYojYFNENMEGkZDmlnGyCCeQU5hwXeAfshvAMISw5xNtgB7OqZBiyCXiarVRvbDbHmbELU5sYMr00caF7I_s8unzQQVu1WA2yz6KXNphonM3qVdaY4MdlNLbLHm08e3_LlYzaJlswnZVJ2-2DrVb2QR981T3wcHV5P7vOb-_mN7OL21wRimLOKtxypRghuGnLtuZIUdQ2pGGqqtq2rqVsIOa8xiRdSmtc0JJpRVAjmcYKFnvgfO1djvWgG6VtWrUXS28G6VfCSSP-dqxZiM69CgoxQRQnwfGXwLuXUYcoBhOU7ntptRuDQBUuq4oXpEjoyRpV3oXgdfszBkHxmYhIiYjPRASiiT76vdkP-x1BAk7XQEgt22kvnt3o0_vCv74PxKGZWA</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1827889343</pqid></control><display><type>article</type><title>Cyclin G2 inhibits epithelial-to-mesenchymal transition by disrupting Wnt/β-catenin signaling</title><source>MEDLINE</source><source>Nature</source><source>Springer Nature - Complete Springer Journals</source><creator>Bernaudo, S ; Salem, M ; Qi, X ; Zhou, W ; Zhang, C ; Yang, W ; Rosman, D ; Deng, Z ; Ye, G ; Yang, B ; Vanderhyden, B ; Wu, Z ; Peng, C</creator><creatorcontrib>Bernaudo, S ; Salem, M ; Qi, X ; Zhou, W ; Zhang, C ; Yang, W ; Rosman, D ; Deng, Z ; Ye, G ; Yang, B ; Vanderhyden, B ; Wu, Z ; Peng, C</creatorcontrib><description>Epithelial ovarian cancer (EOC) has the highest mortality rate among gynecological malignancies owing to poor screening methods, non-specific symptoms and limited knowledge of the cellular targets that contribute to the disease. Cyclin G2 is an unconventional cyclin that acts to oppose cell cycle progression. Dysregulation of the cyclin G2 gene (
CCNG2
) in a variety of human cancers has been reported; however, the role of cyclin G2 in tumorigenesis remains unclear. In this study, we investigated the function of cyclin G2 in EOC.
In vitro
and
in vivo
studies using several EOC-derived tumor cell lines revealed that cyclin G2 inhibited cell proliferation, migration, invasion and spheroid formation, as well as tumor formation and invasion. By interrogating cDNA microarray data sets, we found that
CCGN2
mRNA is reduced in several large cohorts of human ovarian carcinoma when compared with normal ovarian surface epithelium or borderline tumors of the ovary. Mechanistically, cyclin G2 was found to suppress epithelial-to-mesenchymal transition (EMT), as demonstrated by the differential regulation of various EMT genes, such as Snail, Slug, vimentin and E-cadherin. Moreover, cyclin G2 potently suppressed the Wnt/β-catenin signaling pathway by downregulating key Wnt components, namely LRP6, DVL2 and β-catenin, which could be linked to inhibition of EMT. Taken together, our novel findings demonstrate that cyclin G2 has potent tumor-suppressive effects in EOCs by inhibiting EMT through attenuating Wnt/β-catenin signaling.</description><identifier>ISSN: 0950-9232</identifier><identifier>EISSN: 1476-5594</identifier><identifier>DOI: 10.1038/onc.2016.15</identifier><identifier>PMID: 26876206</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/95 ; 14/19 ; 14/34 ; 38/109 ; 38/77 ; 38/89 ; 631/67/1517/1709 ; 82/80 ; Antigens, CD ; Apoptosis ; beta Catenin - antagonists & inhibitors ; beta Catenin - genetics ; Cadherins - genetics ; Carcinogenesis - genetics ; Carcinoma, Ovarian Epithelial ; Cell Biology ; Cell Movement - genetics ; Cell Proliferation - genetics ; Cyclin G2 - genetics ; Dishevelled Proteins - antagonists & inhibitors ; Dishevelled Proteins - genetics ; Epithelial-Mesenchymal Transition - genetics ; Female ; Human Genetics ; Humans ; Internal Medicine ; Low Density Lipoprotein Receptor-Related Protein-6 - antagonists & inhibitors ; Low Density Lipoprotein Receptor-Related Protein-6 - genetics ; Medicine ; Medicine & Public Health ; Neoplasm Invasiveness - genetics ; Neoplasms, Glandular and Epithelial - genetics ; Neoplasms, Glandular and Epithelial - pathology ; Oncology ; Original ; original-article ; Ovarian Neoplasms - genetics ; Ovarian Neoplasms - pathology ; Wnt Signaling Pathway - genetics</subject><ispartof>Oncogene, 2016-09, Vol.35 (36), p.4816-4827</ispartof><rights>The Author(s) 2016</rights><rights>Copyright © 2016 Macmillan Publishers Limited 2016 Macmillan Publishers Limited</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c451t-682f9cc6442df7fb91c51fd4d6c88ffbbaad0299b242015b23576ec41da6e2c03</citedby><cites>FETCH-LOGICAL-c451t-682f9cc6442df7fb91c51fd4d6c88ffbbaad0299b242015b23576ec41da6e2c03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/onc.2016.15$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/onc.2016.15$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,778,782,883,27907,27908,41471,42540,51302</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26876206$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bernaudo, S</creatorcontrib><creatorcontrib>Salem, M</creatorcontrib><creatorcontrib>Qi, X</creatorcontrib><creatorcontrib>Zhou, W</creatorcontrib><creatorcontrib>Zhang, C</creatorcontrib><creatorcontrib>Yang, W</creatorcontrib><creatorcontrib>Rosman, D</creatorcontrib><creatorcontrib>Deng, Z</creatorcontrib><creatorcontrib>Ye, G</creatorcontrib><creatorcontrib>Yang, B</creatorcontrib><creatorcontrib>Vanderhyden, B</creatorcontrib><creatorcontrib>Wu, Z</creatorcontrib><creatorcontrib>Peng, C</creatorcontrib><title>Cyclin G2 inhibits epithelial-to-mesenchymal transition by disrupting Wnt/β-catenin signaling</title><title>Oncogene</title><addtitle>Oncogene</addtitle><addtitle>Oncogene</addtitle><description>Epithelial ovarian cancer (EOC) has the highest mortality rate among gynecological malignancies owing to poor screening methods, non-specific symptoms and limited knowledge of the cellular targets that contribute to the disease. Cyclin G2 is an unconventional cyclin that acts to oppose cell cycle progression. Dysregulation of the cyclin G2 gene (
CCNG2
) in a variety of human cancers has been reported; however, the role of cyclin G2 in tumorigenesis remains unclear. In this study, we investigated the function of cyclin G2 in EOC.
In vitro
and
in vivo
studies using several EOC-derived tumor cell lines revealed that cyclin G2 inhibited cell proliferation, migration, invasion and spheroid formation, as well as tumor formation and invasion. By interrogating cDNA microarray data sets, we found that
CCGN2
mRNA is reduced in several large cohorts of human ovarian carcinoma when compared with normal ovarian surface epithelium or borderline tumors of the ovary. Mechanistically, cyclin G2 was found to suppress epithelial-to-mesenchymal transition (EMT), as demonstrated by the differential regulation of various EMT genes, such as Snail, Slug, vimentin and E-cadherin. Moreover, cyclin G2 potently suppressed the Wnt/β-catenin signaling pathway by downregulating key Wnt components, namely LRP6, DVL2 and β-catenin, which could be linked to inhibition of EMT. Taken together, our novel findings demonstrate that cyclin G2 has potent tumor-suppressive effects in EOCs by inhibiting EMT through attenuating Wnt/β-catenin signaling.</description><subject>13/95</subject><subject>14/19</subject><subject>14/34</subject><subject>38/109</subject><subject>38/77</subject><subject>38/89</subject><subject>631/67/1517/1709</subject><subject>82/80</subject><subject>Antigens, CD</subject><subject>Apoptosis</subject><subject>beta Catenin - antagonists & inhibitors</subject><subject>beta Catenin - genetics</subject><subject>Cadherins - genetics</subject><subject>Carcinogenesis - genetics</subject><subject>Carcinoma, Ovarian Epithelial</subject><subject>Cell Biology</subject><subject>Cell Movement - genetics</subject><subject>Cell Proliferation - genetics</subject><subject>Cyclin G2 - genetics</subject><subject>Dishevelled Proteins - antagonists & inhibitors</subject><subject>Dishevelled Proteins - genetics</subject><subject>Epithelial-Mesenchymal Transition - genetics</subject><subject>Female</subject><subject>Human Genetics</subject><subject>Humans</subject><subject>Internal Medicine</subject><subject>Low Density Lipoprotein Receptor-Related Protein-6 - antagonists & inhibitors</subject><subject>Low Density Lipoprotein Receptor-Related Protein-6 - genetics</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Neoplasm Invasiveness - genetics</subject><subject>Neoplasms, Glandular and Epithelial - genetics</subject><subject>Neoplasms, Glandular and Epithelial - pathology</subject><subject>Oncology</subject><subject>Original</subject><subject>original-article</subject><subject>Ovarian Neoplasms - genetics</subject><subject>Ovarian Neoplasms - pathology</subject><subject>Wnt Signaling Pathway - genetics</subject><issn>0950-9232</issn><issn>1476-5594</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><recordid>eNptkctKxDAUhoMoOl5W7qVLQTsmaZI2G0EGHQXBjeLOkKZpJ9ImY5IK81o-iM9kZFQUXJ3F-fjO5QfgEMEpgkV15qyaYojYFNENMEGkZDmlnGyCCeQU5hwXeAfshvAMISw5xNtgB7OqZBiyCXiarVRvbDbHmbELU5sYMr00caF7I_s8unzQQVu1WA2yz6KXNphonM3qVdaY4MdlNLbLHm08e3_LlYzaJlswnZVJ2-2DrVb2QR981T3wcHV5P7vOb-_mN7OL21wRimLOKtxypRghuGnLtuZIUdQ2pGGqqtq2rqVsIOa8xiRdSmtc0JJpRVAjmcYKFnvgfO1djvWgG6VtWrUXS28G6VfCSSP-dqxZiM69CgoxQRQnwfGXwLuXUYcoBhOU7ntptRuDQBUuq4oXpEjoyRpV3oXgdfszBkHxmYhIiYjPRASiiT76vdkP-x1BAk7XQEgt22kvnt3o0_vCv74PxKGZWA</recordid><startdate>20160908</startdate><enddate>20160908</enddate><creator>Bernaudo, S</creator><creator>Salem, M</creator><creator>Qi, X</creator><creator>Zhou, W</creator><creator>Zhang, C</creator><creator>Yang, W</creator><creator>Rosman, D</creator><creator>Deng, Z</creator><creator>Ye, G</creator><creator>Yang, B</creator><creator>Vanderhyden, B</creator><creator>Wu, Z</creator><creator>Peng, C</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><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>7TO</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>20160908</creationdate><title>Cyclin G2 inhibits epithelial-to-mesenchymal transition by disrupting Wnt/β-catenin signaling</title><author>Bernaudo, S ; Salem, M ; Qi, X ; Zhou, W ; Zhang, C ; Yang, W ; Rosman, D ; Deng, Z ; Ye, G ; Yang, B ; Vanderhyden, B ; Wu, Z ; Peng, C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c451t-682f9cc6442df7fb91c51fd4d6c88ffbbaad0299b242015b23576ec41da6e2c03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>13/95</topic><topic>14/19</topic><topic>14/34</topic><topic>38/109</topic><topic>38/77</topic><topic>38/89</topic><topic>631/67/1517/1709</topic><topic>82/80</topic><topic>Antigens, CD</topic><topic>Apoptosis</topic><topic>beta Catenin - antagonists & inhibitors</topic><topic>beta Catenin - genetics</topic><topic>Cadherins - genetics</topic><topic>Carcinogenesis - genetics</topic><topic>Carcinoma, Ovarian Epithelial</topic><topic>Cell Biology</topic><topic>Cell Movement - genetics</topic><topic>Cell Proliferation - genetics</topic><topic>Cyclin G2 - genetics</topic><topic>Dishevelled Proteins - antagonists & inhibitors</topic><topic>Dishevelled Proteins - genetics</topic><topic>Epithelial-Mesenchymal Transition - genetics</topic><topic>Female</topic><topic>Human Genetics</topic><topic>Humans</topic><topic>Internal Medicine</topic><topic>Low Density Lipoprotein Receptor-Related Protein-6 - antagonists & inhibitors</topic><topic>Low Density Lipoprotein Receptor-Related Protein-6 - genetics</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Neoplasm Invasiveness - genetics</topic><topic>Neoplasms, Glandular and Epithelial - genetics</topic><topic>Neoplasms, Glandular and Epithelial - pathology</topic><topic>Oncology</topic><topic>Original</topic><topic>original-article</topic><topic>Ovarian Neoplasms - genetics</topic><topic>Ovarian Neoplasms - pathology</topic><topic>Wnt Signaling Pathway - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bernaudo, S</creatorcontrib><creatorcontrib>Salem, M</creatorcontrib><creatorcontrib>Qi, X</creatorcontrib><creatorcontrib>Zhou, W</creatorcontrib><creatorcontrib>Zhang, C</creatorcontrib><creatorcontrib>Yang, W</creatorcontrib><creatorcontrib>Rosman, D</creatorcontrib><creatorcontrib>Deng, Z</creatorcontrib><creatorcontrib>Ye, G</creatorcontrib><creatorcontrib>Yang, B</creatorcontrib><creatorcontrib>Vanderhyden, B</creatorcontrib><creatorcontrib>Wu, Z</creatorcontrib><creatorcontrib>Peng, C</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</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><collection>PubMed Central (Full Participant titles)</collection><jtitle>Oncogene</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bernaudo, S</au><au>Salem, M</au><au>Qi, X</au><au>Zhou, W</au><au>Zhang, C</au><au>Yang, W</au><au>Rosman, D</au><au>Deng, Z</au><au>Ye, G</au><au>Yang, B</au><au>Vanderhyden, B</au><au>Wu, Z</au><au>Peng, C</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cyclin G2 inhibits epithelial-to-mesenchymal transition by disrupting Wnt/β-catenin signaling</atitle><jtitle>Oncogene</jtitle><stitle>Oncogene</stitle><addtitle>Oncogene</addtitle><date>2016-09-08</date><risdate>2016</risdate><volume>35</volume><issue>36</issue><spage>4816</spage><epage>4827</epage><pages>4816-4827</pages><issn>0950-9232</issn><eissn>1476-5594</eissn><abstract>Epithelial ovarian cancer (EOC) has the highest mortality rate among gynecological malignancies owing to poor screening methods, non-specific symptoms and limited knowledge of the cellular targets that contribute to the disease. Cyclin G2 is an unconventional cyclin that acts to oppose cell cycle progression. Dysregulation of the cyclin G2 gene (
CCNG2
) in a variety of human cancers has been reported; however, the role of cyclin G2 in tumorigenesis remains unclear. In this study, we investigated the function of cyclin G2 in EOC.
In vitro
and
in vivo
studies using several EOC-derived tumor cell lines revealed that cyclin G2 inhibited cell proliferation, migration, invasion and spheroid formation, as well as tumor formation and invasion. By interrogating cDNA microarray data sets, we found that
CCGN2
mRNA is reduced in several large cohorts of human ovarian carcinoma when compared with normal ovarian surface epithelium or borderline tumors of the ovary. Mechanistically, cyclin G2 was found to suppress epithelial-to-mesenchymal transition (EMT), as demonstrated by the differential regulation of various EMT genes, such as Snail, Slug, vimentin and E-cadherin. Moreover, cyclin G2 potently suppressed the Wnt/β-catenin signaling pathway by downregulating key Wnt components, namely LRP6, DVL2 and β-catenin, which could be linked to inhibition of EMT. Taken together, our novel findings demonstrate that cyclin G2 has potent tumor-suppressive effects in EOCs by inhibiting EMT through attenuating Wnt/β-catenin signaling.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>26876206</pmid><doi>10.1038/onc.2016.15</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 13/95 14/19 14/34 38/109 38/77 38/89 631/67/1517/1709 82/80 Antigens, CD Apoptosis beta Catenin - antagonists & inhibitors beta Catenin - genetics Cadherins - genetics Carcinogenesis - genetics Carcinoma, Ovarian Epithelial Cell Biology Cell Movement - genetics Cell Proliferation - genetics Cyclin G2 - genetics Dishevelled Proteins - antagonists & inhibitors Dishevelled Proteins - genetics Epithelial-Mesenchymal Transition - genetics Female Human Genetics Humans Internal Medicine Low Density Lipoprotein Receptor-Related Protein-6 - antagonists & inhibitors Low Density Lipoprotein Receptor-Related Protein-6 - genetics Medicine Medicine & Public Health Neoplasm Invasiveness - genetics Neoplasms, Glandular and Epithelial - genetics Neoplasms, Glandular and Epithelial - pathology Oncology Original original-article Ovarian Neoplasms - genetics Ovarian Neoplasms - pathology Wnt Signaling Pathway - genetics |
| title | Cyclin G2 inhibits epithelial-to-mesenchymal transition by disrupting Wnt/β-catenin signaling |
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