A Novel Wilms Tumor 1 (WT1) Target Gene Negatively Regulates the WNT Signaling Pathway
Mammalian kidney development requires the functions of the Wilms tumor gene WT1 and the WNT/β-catenin signaling pathway. Recent studies have shown that WT1 negatively regulates WNT/β-catenin signaling, but the molecular mechanisms by which WT1 inhibits WNT/β-catenin signaling are not completely unde...
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| creator | Kim, Myoung Shin Yoon, Seung Kew Bollig, Frank Kitagaki, Jirouta Hur, Wonhee Whye, Nathan J. Wu, Yun-Ping Rivera, Miguel N. Park, Jik Young Kim, Ho-Shik Malik, Karim Bell, Daphne W. Englert, Christoph Perantoni, Alan O. Lee, Sean Bong |
| description | Mammalian kidney development requires the functions of the Wilms tumor gene WT1 and the WNT/β-catenin signaling pathway. Recent studies have shown that WT1 negatively regulates WNT/β-catenin signaling, but the molecular mechanisms by which WT1 inhibits WNT/β-catenin signaling are not completely understood. In this study, we identified a gene, CXXC5, which we have renamed WID (WT1-induced Inhibitor of Dishevelled), as a novel WT1 transcriptional target that negatively regulates WNT/β-catenin signaling. WT1 activates WID transcription through the upstream enhancer region. In the developing kidney, Wid and Wt1 are coexpressed in podocytes of maturing nephrons. Structure-function analysis demonstrated that WID interacts with Dishevelled via its C-terminal CXXC zinc finger and Dishevelled binding domains and potently inhibits WNT/β-catenin signaling in vitro and in vivo. WID is evolutionarily conserved, and ablation of wid in zebrafish embryos with antisense morpholino oligonucleotides perturbs embryonic kidney development. Taken together, our results demonstrate that the WT1 negatively regulates WNT/β-catenin pathway via its target gene WID and further suggest a role for WID in nephrogenesis. |
| doi_str_mv | 10.1074/jbc.M109.094334 |
| format | Article |
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Recent studies have shown that WT1 negatively regulates WNT/β-catenin signaling, but the molecular mechanisms by which WT1 inhibits WNT/β-catenin signaling are not completely understood. In this study, we identified a gene, CXXC5, which we have renamed WID (WT1-induced Inhibitor of Dishevelled), as a novel WT1 transcriptional target that negatively regulates WNT/β-catenin signaling. WT1 activates WID transcription through the upstream enhancer region. In the developing kidney, Wid and Wt1 are coexpressed in podocytes of maturing nephrons. Structure-function analysis demonstrated that WID interacts with Dishevelled via its C-terminal CXXC zinc finger and Dishevelled binding domains and potently inhibits WNT/β-catenin signaling in vitro and in vivo. WID is evolutionarily conserved, and ablation of wid in zebrafish embryos with antisense morpholino oligonucleotides perturbs embryonic kidney development. Taken together, our results demonstrate that the WT1 negatively regulates WNT/β-catenin pathway via its target gene WID and further suggest a role for WID in nephrogenesis.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.M109.094334</identifier><identifier>PMID: 20220130</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adaptor Proteins, Signal Transducing - genetics ; Adaptor Proteins, Signal Transducing - metabolism ; Animals ; Axin Protein ; beta Catenin - genetics ; beta Catenin - metabolism ; Carrier Proteins - genetics ; Carrier Proteins - metabolism ; Chromatin Immunoprecipitation ; Danio rerio ; Developmental Biology ; Dishevelled Proteins ; DNA-Binding Proteins ; Down-Regulation ; Embryo, Nonmammalian - cytology ; Embryo, Nonmammalian - metabolism ; Gene Expression ; Gene Expression Regulation, Neoplastic ; Humans ; Immunoblotting ; Immunoglobulin G - immunology ; Immunoprecipitation ; Kidney ; Kidney - cytology ; Kidney - metabolism ; Luciferases - metabolism ; Mice ; NIH 3T3 Cells ; Phosphoproteins - genetics ; Phosphoproteins - metabolism ; Promoter Regions, Genetic ; Rabbits ; Repressor Proteins - genetics ; Repressor Proteins - metabolism ; Reverse Transcriptase Polymerase Chain Reaction ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; RNA, Small Interfering - pharmacology ; Signal Transduction ; Transcription Factors ; Transcription Target Genes ; Tumor Suppressor ; Wnt Pathway ; Wnt Proteins - genetics ; Wnt Proteins - metabolism ; WT1 Proteins - genetics ; WT1 Proteins - metabolism ; Zebrafish</subject><ispartof>The Journal of biological chemistry, 2010-05, Vol.285 (19), p.14585-14593</ispartof><rights>2010 © 2010 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.</rights><rights>2010 by The American Society for Biochemistry and Molecular Biology, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c544t-8056c93168b3514ccad47106f9c66f92ee654eddf7ff68b752d628b82d9734c3</citedby><cites>FETCH-LOGICAL-c544t-8056c93168b3514ccad47106f9c66f92ee654eddf7ff68b752d628b82d9734c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2863207/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2863207/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27923,27924,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20220130$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kim, Myoung Shin</creatorcontrib><creatorcontrib>Yoon, Seung Kew</creatorcontrib><creatorcontrib>Bollig, Frank</creatorcontrib><creatorcontrib>Kitagaki, Jirouta</creatorcontrib><creatorcontrib>Hur, Wonhee</creatorcontrib><creatorcontrib>Whye, Nathan J.</creatorcontrib><creatorcontrib>Wu, Yun-Ping</creatorcontrib><creatorcontrib>Rivera, Miguel N.</creatorcontrib><creatorcontrib>Park, Jik Young</creatorcontrib><creatorcontrib>Kim, Ho-Shik</creatorcontrib><creatorcontrib>Malik, Karim</creatorcontrib><creatorcontrib>Bell, Daphne W.</creatorcontrib><creatorcontrib>Englert, Christoph</creatorcontrib><creatorcontrib>Perantoni, Alan O.</creatorcontrib><creatorcontrib>Lee, Sean Bong</creatorcontrib><title>A Novel Wilms Tumor 1 (WT1) Target Gene Negatively Regulates the WNT Signaling Pathway</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>Mammalian kidney development requires the functions of the Wilms tumor gene WT1 and the WNT/β-catenin signaling pathway. Recent studies have shown that WT1 negatively regulates WNT/β-catenin signaling, but the molecular mechanisms by which WT1 inhibits WNT/β-catenin signaling are not completely understood. In this study, we identified a gene, CXXC5, which we have renamed WID (WT1-induced Inhibitor of Dishevelled), as a novel WT1 transcriptional target that negatively regulates WNT/β-catenin signaling. WT1 activates WID transcription through the upstream enhancer region. In the developing kidney, Wid and Wt1 are coexpressed in podocytes of maturing nephrons. Structure-function analysis demonstrated that WID interacts with Dishevelled via its C-terminal CXXC zinc finger and Dishevelled binding domains and potently inhibits WNT/β-catenin signaling in vitro and in vivo. WID is evolutionarily conserved, and ablation of wid in zebrafish embryos with antisense morpholino oligonucleotides perturbs embryonic kidney development. Taken together, our results demonstrate that the WT1 negatively regulates WNT/β-catenin pathway via its target gene WID and further suggest a role for WID in nephrogenesis.</description><subject>Adaptor Proteins, Signal Transducing - genetics</subject><subject>Adaptor Proteins, Signal Transducing - metabolism</subject><subject>Animals</subject><subject>Axin Protein</subject><subject>beta Catenin - genetics</subject><subject>beta Catenin - metabolism</subject><subject>Carrier Proteins - genetics</subject><subject>Carrier Proteins - metabolism</subject><subject>Chromatin Immunoprecipitation</subject><subject>Danio rerio</subject><subject>Developmental Biology</subject><subject>Dishevelled Proteins</subject><subject>DNA-Binding Proteins</subject><subject>Down-Regulation</subject><subject>Embryo, Nonmammalian - cytology</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Gene Expression</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Humans</subject><subject>Immunoblotting</subject><subject>Immunoglobulin G - immunology</subject><subject>Immunoprecipitation</subject><subject>Kidney</subject><subject>Kidney - cytology</subject><subject>Kidney - metabolism</subject><subject>Luciferases - metabolism</subject><subject>Mice</subject><subject>NIH 3T3 Cells</subject><subject>Phosphoproteins - genetics</subject><subject>Phosphoproteins - metabolism</subject><subject>Promoter Regions, Genetic</subject><subject>Rabbits</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>RNA, Small Interfering - pharmacology</subject><subject>Signal Transduction</subject><subject>Transcription Factors</subject><subject>Transcription Target Genes</subject><subject>Tumor Suppressor</subject><subject>Wnt Pathway</subject><subject>Wnt Proteins - genetics</subject><subject>Wnt Proteins - metabolism</subject><subject>WT1 Proteins - genetics</subject><subject>WT1 Proteins - metabolism</subject><subject>Zebrafish</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtv1DAURi0EotPCmh14R1lk6leceINUVVCQyoBoYNhZHucm4yqPYjuD5t_jIaWCBRJe2It7_N1rH4SeUbKkpBBnNxu7_ECJWhIlOBcP0IKSkmc8p98eogUhjGaK5eUROg7hhqQlFH2MjhhhjFBOFujrOV6NO-jw2nV9wNXUjx5TfLqu6CtcGd9CxJcwAF5Ba6JL5B5_hnbqTISA4xbwelXha9cOpnNDiz-ZuP1h9k_Qo8Z0AZ7enSeoevumuniXXX28fH9xfpXZXIiYlSSXVnEqy00aWVhralFQIhtlZdoYgMwF1HVTNE1iipzVkpWbktWq4MLyE_R6jr2dNj3UFoboTadvveuN3-vROP13ZXBb3Y47zUrJGSlSwMu7AD9-nyBE3btgoevMAOMUdCGEpLli_0FyzgoliwN5NpPWjyF4aO7noUQfrOlkTR-s6dlauvH8z2fc8781JeDFDDRm1Kb1Lugv179KtOQiVzQRaiYg_fbOgdfBOhgs1M6Djboe3T_b_wQ6i649</recordid><startdate>20100507</startdate><enddate>20100507</enddate><creator>Kim, Myoung Shin</creator><creator>Yoon, Seung Kew</creator><creator>Bollig, Frank</creator><creator>Kitagaki, Jirouta</creator><creator>Hur, Wonhee</creator><creator>Whye, Nathan J.</creator><creator>Wu, Yun-Ping</creator><creator>Rivera, Miguel N.</creator><creator>Park, Jik Young</creator><creator>Kim, Ho-Shik</creator><creator>Malik, Karim</creator><creator>Bell, Daphne W.</creator><creator>Englert, Christoph</creator><creator>Perantoni, Alan O.</creator><creator>Lee, Sean Bong</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</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>7X8</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>20100507</creationdate><title>A Novel Wilms Tumor 1 (WT1) Target Gene Negatively Regulates the WNT Signaling Pathway</title><author>Kim, Myoung Shin ; Yoon, Seung Kew ; Bollig, Frank ; Kitagaki, Jirouta ; Hur, Wonhee ; Whye, Nathan J. ; Wu, Yun-Ping ; Rivera, Miguel N. ; Park, Jik Young ; Kim, Ho-Shik ; Malik, Karim ; Bell, Daphne W. ; Englert, Christoph ; Perantoni, Alan O. ; Lee, Sean Bong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c544t-8056c93168b3514ccad47106f9c66f92ee654eddf7ff68b752d628b82d9734c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Adaptor Proteins, Signal Transducing - genetics</topic><topic>Adaptor Proteins, Signal Transducing - metabolism</topic><topic>Animals</topic><topic>Axin Protein</topic><topic>beta Catenin - genetics</topic><topic>beta Catenin - metabolism</topic><topic>Carrier Proteins - genetics</topic><topic>Carrier Proteins - metabolism</topic><topic>Chromatin Immunoprecipitation</topic><topic>Danio rerio</topic><topic>Developmental Biology</topic><topic>Dishevelled Proteins</topic><topic>DNA-Binding Proteins</topic><topic>Down-Regulation</topic><topic>Embryo, Nonmammalian - cytology</topic><topic>Embryo, Nonmammalian - metabolism</topic><topic>Gene Expression</topic><topic>Gene Expression Regulation, Neoplastic</topic><topic>Humans</topic><topic>Immunoblotting</topic><topic>Immunoglobulin G - immunology</topic><topic>Immunoprecipitation</topic><topic>Kidney</topic><topic>Kidney - cytology</topic><topic>Kidney - metabolism</topic><topic>Luciferases - metabolism</topic><topic>Mice</topic><topic>NIH 3T3 Cells</topic><topic>Phosphoproteins - genetics</topic><topic>Phosphoproteins - metabolism</topic><topic>Promoter Regions, Genetic</topic><topic>Rabbits</topic><topic>Repressor Proteins - genetics</topic><topic>Repressor Proteins - metabolism</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>RNA, Small Interfering - pharmacology</topic><topic>Signal Transduction</topic><topic>Transcription Factors</topic><topic>Transcription Target Genes</topic><topic>Tumor Suppressor</topic><topic>Wnt Pathway</topic><topic>Wnt Proteins - genetics</topic><topic>Wnt Proteins - metabolism</topic><topic>WT1 Proteins - genetics</topic><topic>WT1 Proteins - metabolism</topic><topic>Zebrafish</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kim, Myoung Shin</creatorcontrib><creatorcontrib>Yoon, Seung Kew</creatorcontrib><creatorcontrib>Bollig, Frank</creatorcontrib><creatorcontrib>Kitagaki, Jirouta</creatorcontrib><creatorcontrib>Hur, Wonhee</creatorcontrib><creatorcontrib>Whye, Nathan J.</creatorcontrib><creatorcontrib>Wu, Yun-Ping</creatorcontrib><creatorcontrib>Rivera, Miguel N.</creatorcontrib><creatorcontrib>Park, Jik Young</creatorcontrib><creatorcontrib>Kim, Ho-Shik</creatorcontrib><creatorcontrib>Malik, Karim</creatorcontrib><creatorcontrib>Bell, Daphne W.</creatorcontrib><creatorcontrib>Englert, Christoph</creatorcontrib><creatorcontrib>Perantoni, Alan O.</creatorcontrib><creatorcontrib>Lee, Sean Bong</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</collection><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><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kim, Myoung Shin</au><au>Yoon, Seung Kew</au><au>Bollig, Frank</au><au>Kitagaki, Jirouta</au><au>Hur, Wonhee</au><au>Whye, Nathan J.</au><au>Wu, Yun-Ping</au><au>Rivera, Miguel N.</au><au>Park, Jik Young</au><au>Kim, Ho-Shik</au><au>Malik, Karim</au><au>Bell, Daphne W.</au><au>Englert, Christoph</au><au>Perantoni, Alan O.</au><au>Lee, Sean Bong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Novel Wilms Tumor 1 (WT1) Target Gene Negatively Regulates the WNT Signaling Pathway</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2010-05-07</date><risdate>2010</risdate><volume>285</volume><issue>19</issue><spage>14585</spage><epage>14593</epage><pages>14585-14593</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>Mammalian kidney development requires the functions of the Wilms tumor gene WT1 and the WNT/β-catenin signaling pathway. Recent studies have shown that WT1 negatively regulates WNT/β-catenin signaling, but the molecular mechanisms by which WT1 inhibits WNT/β-catenin signaling are not completely understood. In this study, we identified a gene, CXXC5, which we have renamed WID (WT1-induced Inhibitor of Dishevelled), as a novel WT1 transcriptional target that negatively regulates WNT/β-catenin signaling. WT1 activates WID transcription through the upstream enhancer region. In the developing kidney, Wid and Wt1 are coexpressed in podocytes of maturing nephrons. Structure-function analysis demonstrated that WID interacts with Dishevelled via its C-terminal CXXC zinc finger and Dishevelled binding domains and potently inhibits WNT/β-catenin signaling in vitro and in vivo. WID is evolutionarily conserved, and ablation of wid in zebrafish embryos with antisense morpholino oligonucleotides perturbs embryonic kidney development. Taken together, our results demonstrate that the WT1 negatively regulates WNT/β-catenin pathway via its target gene WID and further suggest a role for WID in nephrogenesis.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>20220130</pmid><doi>10.1074/jbc.M109.094334</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Adaptor Proteins, Signal Transducing - genetics Adaptor Proteins, Signal Transducing - metabolism Animals Axin Protein beta Catenin - genetics beta Catenin - metabolism Carrier Proteins - genetics Carrier Proteins - metabolism Chromatin Immunoprecipitation Danio rerio Developmental Biology Dishevelled Proteins DNA-Binding Proteins Down-Regulation Embryo, Nonmammalian - cytology Embryo, Nonmammalian - metabolism Gene Expression Gene Expression Regulation, Neoplastic Humans Immunoblotting Immunoglobulin G - immunology Immunoprecipitation Kidney Kidney - cytology Kidney - metabolism Luciferases - metabolism Mice NIH 3T3 Cells Phosphoproteins - genetics Phosphoproteins - metabolism Promoter Regions, Genetic Rabbits Repressor Proteins - genetics Repressor Proteins - metabolism Reverse Transcriptase Polymerase Chain Reaction RNA, Messenger - genetics RNA, Messenger - metabolism RNA, Small Interfering - pharmacology Signal Transduction Transcription Factors Transcription Target Genes Tumor Suppressor Wnt Pathway Wnt Proteins - genetics Wnt Proteins - metabolism WT1 Proteins - genetics WT1 Proteins - metabolism Zebrafish |
| title | A Novel Wilms Tumor 1 (WT1) Target Gene Negatively Regulates the WNT Signaling Pathway |
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