Glutaminase 2 stabilizes Dicer to repress Snail and metastasis in hepatocellular carcinoma cells
Abstract Glutaminolysis that catabolizes glutamine to glutamate plays a critical role in cancer progression. Glutaminase 2 (GLS2) has been reported as a tumor suppressor. Recent studies implied that GLS2 may display its multifunction besides classical metabolic feature by different localizations and...
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| Veröffentlicht in: | Cancer letters 2016-12, Vol.383 (2), p.282-294 |
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| creator | Kuo, Tsang-Chih Chen, Chi-Kuan Hua, Kuo-Ti Yu, Pei Lee, Wei-Jiunn Chen, Min-Wei Jeng, Yung-Ming Chien, Ming-Hsien Kuo, Kuang-Tai Hsiao, Michael Kuo, Min-Liang |
| description | Abstract Glutaminolysis that catabolizes glutamine to glutamate plays a critical role in cancer progression. Glutaminase 2 (GLS2) has been reported as a tumor suppressor. Recent studies implied that GLS2 may display its multifunction besides classical metabolic feature by different localizations and potential protein binding domains. Here, we showed that GLS2 expression correlates inversely with stage, vascular invasion, tumor size and poor prognosis in human hepatocellular carcinoma (HCC) tissues. We found that GLS2 significantly represses cell migration, invasion and metastasis of HCC through downregulation of Snail in vitro and in vivo . Moreover, our results demonstrated that GLS2 interacts with Dicer and stabilizes Dicer protein to facilitate miR-34a maturation and subsequently represses Snail expression in a glutaminase activity independent manner. Our findings indicate that non-glutaminolysis function of GLS2 inhibits migration and invasion of HCC cells by repressing the epithelial–mesenchymal transition via the Dicer-miR-34a-Snail axis. |
| doi_str_mv | 10.1016/j.canlet.2016.10.012 |
| format | Article |
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Glutaminase 2 (GLS2) has been reported as a tumor suppressor. Recent studies implied that GLS2 may display its multifunction besides classical metabolic feature by different localizations and potential protein binding domains. Here, we showed that GLS2 expression correlates inversely with stage, vascular invasion, tumor size and poor prognosis in human hepatocellular carcinoma (HCC) tissues. We found that GLS2 significantly represses cell migration, invasion and metastasis of HCC through downregulation of Snail in vitro and in vivo . Moreover, our results demonstrated that GLS2 interacts with Dicer and stabilizes Dicer protein to facilitate miR-34a maturation and subsequently represses Snail expression in a glutaminase activity independent manner. Our findings indicate that non-glutaminolysis function of GLS2 inhibits migration and invasion of HCC cells by repressing the epithelial–mesenchymal transition via the Dicer-miR-34a-Snail axis.</description><identifier>ISSN: 0304-3835</identifier><identifier>EISSN: 1872-7980</identifier><identifier>DOI: 10.1016/j.canlet.2016.10.012</identifier><identifier>PMID: 27725225</identifier><language>eng</language><publisher>Ireland: Elsevier B.V</publisher><subject>Animals ; Biosynthesis ; Carcinoma, Hepatocellular - enzymology ; Carcinoma, Hepatocellular - genetics ; Carcinoma, Hepatocellular - mortality ; Carcinoma, Hepatocellular - secondary ; Cell growth ; Cell migration ; Cell Movement ; DEAD-box RNA Helicases - genetics ; DEAD-box RNA Helicases - metabolism ; Dicer ; Dicer protein ; Down-Regulation ; Enzymes ; Epithelial-Mesenchymal Transition ; Female ; Gene expression ; Gene Expression Regulation, Neoplastic ; Glutaminase ; Glutaminase - genetics ; Glutaminase - metabolism ; Glutaminase 2 ; Glutamine ; HEK293 Cells ; Hematology, Oncology and Palliative Medicine ; Hep G2 Cells ; Hepatocellular carcinoma ; Hepatocellular carcinoma cells ; Humans ; Kaplan-Meier Estimate ; Liver cancer ; Liver Neoplasms - enzymology ; Liver Neoplasms - genetics ; Liver Neoplasms - mortality ; Liver Neoplasms - pathology ; Male ; Medical prognosis ; Mesenchyme ; Metabolism ; Metastases ; Metastasis ; Mice, Inbred NOD ; Mice, SCID ; MicroRNAs - genetics ; MicroRNAs - metabolism ; Motility ; Neoplasm Invasiveness ; Neoplasm Staging ; Protein Stability ; Proteins ; R&D ; Research & development ; Ribonuclease III - genetics ; Ribonuclease III - metabolism ; RNA Interference ; Roles ; Signal Transduction ; Snail ; Snail Family Transcription Factors - genetics ; Snail Family Transcription Factors - metabolism ; Time Factors ; Transfection ; Tumor Burden ; Tumor suppressor genes</subject><ispartof>Cancer letters, 2016-12, Vol.383 (2), p.282-294</ispartof><rights>Elsevier Ireland Ltd</rights><rights>2016 Elsevier Ireland Ltd</rights><rights>Copyright © 2016 Elsevier Ireland Ltd. All rights reserved.</rights><rights>Copyright Elsevier Limited Dec 28, 2016</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c548t-de835520c65c9a27fe77544ae23bf7f259efaf105c286079862db57be24c01ab3</citedby><cites>FETCH-LOGICAL-c548t-de835520c65c9a27fe77544ae23bf7f259efaf105c286079862db57be24c01ab3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0304383516306243$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27725225$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kuo, Tsang-Chih</creatorcontrib><creatorcontrib>Chen, Chi-Kuan</creatorcontrib><creatorcontrib>Hua, Kuo-Ti</creatorcontrib><creatorcontrib>Yu, Pei</creatorcontrib><creatorcontrib>Lee, Wei-Jiunn</creatorcontrib><creatorcontrib>Chen, Min-Wei</creatorcontrib><creatorcontrib>Jeng, Yung-Ming</creatorcontrib><creatorcontrib>Chien, Ming-Hsien</creatorcontrib><creatorcontrib>Kuo, Kuang-Tai</creatorcontrib><creatorcontrib>Hsiao, Michael</creatorcontrib><creatorcontrib>Kuo, Min-Liang</creatorcontrib><title>Glutaminase 2 stabilizes Dicer to repress Snail and metastasis in hepatocellular carcinoma cells</title><title>Cancer letters</title><addtitle>Cancer Lett</addtitle><description>Abstract Glutaminolysis that catabolizes glutamine to glutamate plays a critical role in cancer progression. Glutaminase 2 (GLS2) has been reported as a tumor suppressor. Recent studies implied that GLS2 may display its multifunction besides classical metabolic feature by different localizations and potential protein binding domains. Here, we showed that GLS2 expression correlates inversely with stage, vascular invasion, tumor size and poor prognosis in human hepatocellular carcinoma (HCC) tissues. We found that GLS2 significantly represses cell migration, invasion and metastasis of HCC through downregulation of Snail in vitro and in vivo . Moreover, our results demonstrated that GLS2 interacts with Dicer and stabilizes Dicer protein to facilitate miR-34a maturation and subsequently represses Snail expression in a glutaminase activity independent manner. Our findings indicate that non-glutaminolysis function of GLS2 inhibits migration and invasion of HCC cells by repressing the epithelial–mesenchymal transition via the Dicer-miR-34a-Snail axis.</description><subject>Animals</subject><subject>Biosynthesis</subject><subject>Carcinoma, Hepatocellular - enzymology</subject><subject>Carcinoma, Hepatocellular - genetics</subject><subject>Carcinoma, Hepatocellular - mortality</subject><subject>Carcinoma, Hepatocellular - secondary</subject><subject>Cell growth</subject><subject>Cell migration</subject><subject>Cell Movement</subject><subject>DEAD-box RNA Helicases - genetics</subject><subject>DEAD-box RNA Helicases - metabolism</subject><subject>Dicer</subject><subject>Dicer protein</subject><subject>Down-Regulation</subject><subject>Enzymes</subject><subject>Epithelial-Mesenchymal Transition</subject><subject>Female</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Glutaminase</subject><subject>Glutaminase - genetics</subject><subject>Glutaminase - metabolism</subject><subject>Glutaminase 2</subject><subject>Glutamine</subject><subject>HEK293 Cells</subject><subject>Hematology, Oncology and Palliative Medicine</subject><subject>Hep G2 Cells</subject><subject>Hepatocellular carcinoma</subject><subject>Hepatocellular carcinoma cells</subject><subject>Humans</subject><subject>Kaplan-Meier Estimate</subject><subject>Liver cancer</subject><subject>Liver Neoplasms - enzymology</subject><subject>Liver Neoplasms - genetics</subject><subject>Liver Neoplasms - mortality</subject><subject>Liver Neoplasms - pathology</subject><subject>Male</subject><subject>Medical prognosis</subject><subject>Mesenchyme</subject><subject>Metabolism</subject><subject>Metastases</subject><subject>Metastasis</subject><subject>Mice, Inbred NOD</subject><subject>Mice, SCID</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - metabolism</subject><subject>Motility</subject><subject>Neoplasm Invasiveness</subject><subject>Neoplasm Staging</subject><subject>Protein Stability</subject><subject>Proteins</subject><subject>R&D</subject><subject>Research & development</subject><subject>Ribonuclease III - genetics</subject><subject>Ribonuclease III - metabolism</subject><subject>RNA Interference</subject><subject>Roles</subject><subject>Signal Transduction</subject><subject>Snail</subject><subject>Snail Family Transcription Factors - genetics</subject><subject>Snail Family Transcription Factors - metabolism</subject><subject>Time Factors</subject><subject>Transfection</subject><subject>Tumor Burden</subject><subject>Tumor suppressor genes</subject><issn>0304-3835</issn><issn>1872-7980</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk2LFDEQhoMo7rj6D0QCXrzMmM9Oz0WQXV2FBQ-r51idrsaM6fSY6hbWX2-aWRX24ilU8VTlrXqLsedS7KSQzevDLkBOOO9UjWpqJ6R6wDaydWrr9q14yDZCC7PVrbZn7AnRQQhhjbOP2ZlyTlml7IZ9vUrLDGPMQMgVpxm6mOIvJH4ZAxY-T7zgsSARv8kQE4fc8xFnqCRF4jHzb3iEeQqY0pKg8AAlxDyNwNcUPWWPBkiEz-7ec_bl_bvPFx-215-uPl68vd4Ga9p522OVaZUIjQ17UG5A56wxgEp3gxuU3eMAgxQ2qLYRdb5G9Z11HSoThIROn7NXp77HMv1YkGY_RloVQMZpIS9b7bQ0jW0r-vIeepiWkqu6ldJ7I9qmqZQ5UaFMRAUHfyxxhHLrpfCrA_7gTw741YE1Wx2oZS_umi_diP3foj8rr8CbE4B1Gz8jFk8hYg7Yx4Jh9v0U__fD_QYhxRwDpO94i_RvFk_KC3-zXsF6BLLRolFG69--M62V</recordid><startdate>20161228</startdate><enddate>20161228</enddate><creator>Kuo, Tsang-Chih</creator><creator>Chen, Chi-Kuan</creator><creator>Hua, Kuo-Ti</creator><creator>Yu, Pei</creator><creator>Lee, Wei-Jiunn</creator><creator>Chen, Min-Wei</creator><creator>Jeng, Yung-Ming</creator><creator>Chien, Ming-Hsien</creator><creator>Kuo, Kuang-Tai</creator><creator>Hsiao, Michael</creator><creator>Kuo, Min-Liang</creator><general>Elsevier B.V</general><general>Elsevier Limited</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>7TO</scope><scope>7U9</scope><scope>H94</scope><scope>K9.</scope><scope>NAPCQ</scope></search><sort><creationdate>20161228</creationdate><title>Glutaminase 2 stabilizes Dicer to repress Snail and metastasis in hepatocellular carcinoma cells</title><author>Kuo, Tsang-Chih ; Chen, Chi-Kuan ; Hua, Kuo-Ti ; Yu, Pei ; Lee, Wei-Jiunn ; Chen, Min-Wei ; Jeng, Yung-Ming ; Chien, Ming-Hsien ; Kuo, Kuang-Tai ; Hsiao, Michael ; Kuo, Min-Liang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c548t-de835520c65c9a27fe77544ae23bf7f259efaf105c286079862db57be24c01ab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Biosynthesis</topic><topic>Carcinoma, Hepatocellular - enzymology</topic><topic>Carcinoma, Hepatocellular - genetics</topic><topic>Carcinoma, Hepatocellular - mortality</topic><topic>Carcinoma, Hepatocellular - secondary</topic><topic>Cell growth</topic><topic>Cell migration</topic><topic>Cell Movement</topic><topic>DEAD-box RNA Helicases - genetics</topic><topic>DEAD-box RNA Helicases - metabolism</topic><topic>Dicer</topic><topic>Dicer protein</topic><topic>Down-Regulation</topic><topic>Enzymes</topic><topic>Epithelial-Mesenchymal Transition</topic><topic>Female</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Neoplastic</topic><topic>Glutaminase</topic><topic>Glutaminase - genetics</topic><topic>Glutaminase - metabolism</topic><topic>Glutaminase 2</topic><topic>Glutamine</topic><topic>HEK293 Cells</topic><topic>Hematology, Oncology and Palliative Medicine</topic><topic>Hep G2 Cells</topic><topic>Hepatocellular carcinoma</topic><topic>Hepatocellular carcinoma cells</topic><topic>Humans</topic><topic>Kaplan-Meier Estimate</topic><topic>Liver cancer</topic><topic>Liver Neoplasms - enzymology</topic><topic>Liver Neoplasms - genetics</topic><topic>Liver Neoplasms - mortality</topic><topic>Liver Neoplasms - pathology</topic><topic>Male</topic><topic>Medical prognosis</topic><topic>Mesenchyme</topic><topic>Metabolism</topic><topic>Metastases</topic><topic>Metastasis</topic><topic>Mice, Inbred NOD</topic><topic>Mice, SCID</topic><topic>MicroRNAs - genetics</topic><topic>MicroRNAs - metabolism</topic><topic>Motility</topic><topic>Neoplasm Invasiveness</topic><topic>Neoplasm Staging</topic><topic>Protein Stability</topic><topic>Proteins</topic><topic>R&D</topic><topic>Research & development</topic><topic>Ribonuclease III - genetics</topic><topic>Ribonuclease III - metabolism</topic><topic>RNA Interference</topic><topic>Roles</topic><topic>Signal Transduction</topic><topic>Snail</topic><topic>Snail Family Transcription Factors - genetics</topic><topic>Snail Family Transcription Factors - metabolism</topic><topic>Time Factors</topic><topic>Transfection</topic><topic>Tumor Burden</topic><topic>Tumor suppressor genes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kuo, Tsang-Chih</creatorcontrib><creatorcontrib>Chen, Chi-Kuan</creatorcontrib><creatorcontrib>Hua, Kuo-Ti</creatorcontrib><creatorcontrib>Yu, Pei</creatorcontrib><creatorcontrib>Lee, Wei-Jiunn</creatorcontrib><creatorcontrib>Chen, Min-Wei</creatorcontrib><creatorcontrib>Jeng, Yung-Ming</creatorcontrib><creatorcontrib>Chien, Ming-Hsien</creatorcontrib><creatorcontrib>Kuo, Kuang-Tai</creatorcontrib><creatorcontrib>Hsiao, Michael</creatorcontrib><creatorcontrib>Kuo, Min-Liang</creatorcontrib><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>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><jtitle>Cancer letters</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kuo, Tsang-Chih</au><au>Chen, Chi-Kuan</au><au>Hua, Kuo-Ti</au><au>Yu, Pei</au><au>Lee, Wei-Jiunn</au><au>Chen, Min-Wei</au><au>Jeng, Yung-Ming</au><au>Chien, Ming-Hsien</au><au>Kuo, Kuang-Tai</au><au>Hsiao, Michael</au><au>Kuo, Min-Liang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Glutaminase 2 stabilizes Dicer to repress Snail and metastasis in hepatocellular carcinoma cells</atitle><jtitle>Cancer letters</jtitle><addtitle>Cancer Lett</addtitle><date>2016-12-28</date><risdate>2016</risdate><volume>383</volume><issue>2</issue><spage>282</spage><epage>294</epage><pages>282-294</pages><issn>0304-3835</issn><eissn>1872-7980</eissn><abstract>Abstract Glutaminolysis that catabolizes glutamine to glutamate plays a critical role in cancer progression. Glutaminase 2 (GLS2) has been reported as a tumor suppressor. Recent studies implied that GLS2 may display its multifunction besides classical metabolic feature by different localizations and potential protein binding domains. Here, we showed that GLS2 expression correlates inversely with stage, vascular invasion, tumor size and poor prognosis in human hepatocellular carcinoma (HCC) tissues. We found that GLS2 significantly represses cell migration, invasion and metastasis of HCC through downregulation of Snail in vitro and in vivo . Moreover, our results demonstrated that GLS2 interacts with Dicer and stabilizes Dicer protein to facilitate miR-34a maturation and subsequently represses Snail expression in a glutaminase activity independent manner. Our findings indicate that non-glutaminolysis function of GLS2 inhibits migration and invasion of HCC cells by repressing the epithelial–mesenchymal transition via the Dicer-miR-34a-Snail axis.</abstract><cop>Ireland</cop><pub>Elsevier B.V</pub><pmid>27725225</pmid><doi>10.1016/j.canlet.2016.10.012</doi><tpages>13</tpages></addata></record> |
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| subjects | Animals Biosynthesis Carcinoma, Hepatocellular - enzymology Carcinoma, Hepatocellular - genetics Carcinoma, Hepatocellular - mortality Carcinoma, Hepatocellular - secondary Cell growth Cell migration Cell Movement DEAD-box RNA Helicases - genetics DEAD-box RNA Helicases - metabolism Dicer Dicer protein Down-Regulation Enzymes Epithelial-Mesenchymal Transition Female Gene expression Gene Expression Regulation, Neoplastic Glutaminase Glutaminase - genetics Glutaminase - metabolism Glutaminase 2 Glutamine HEK293 Cells Hematology, Oncology and Palliative Medicine Hep G2 Cells Hepatocellular carcinoma Hepatocellular carcinoma cells Humans Kaplan-Meier Estimate Liver cancer Liver Neoplasms - enzymology Liver Neoplasms - genetics Liver Neoplasms - mortality Liver Neoplasms - pathology Male Medical prognosis Mesenchyme Metabolism Metastases Metastasis Mice, Inbred NOD Mice, SCID MicroRNAs - genetics MicroRNAs - metabolism Motility Neoplasm Invasiveness Neoplasm Staging Protein Stability Proteins R&D Research & development Ribonuclease III - genetics Ribonuclease III - metabolism RNA Interference Roles Signal Transduction Snail Snail Family Transcription Factors - genetics Snail Family Transcription Factors - metabolism Time Factors Transfection Tumor Burden Tumor suppressor genes |
| title | Glutaminase 2 stabilizes Dicer to repress Snail and metastasis in hepatocellular carcinoma cells |
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