Pax6 regulates gene expression in the vertebrate lens through miR-204
During development, tissue-specific transcription factors regulate both protein-coding and non-coding genes to control differentiation. Recent studies have established a dual role for the transcription factor Pax6 as both an activator and repressor of gene expression in the eye, central nervous syst...
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| creator | Shaham, Ohad Gueta, Karen Mor, Eyal Oren-Giladi, Pazit Grinberg, Dina Xie, Qing Cvekl, Ales Shomron, Noam Davis, Noa Keydar-Prizant, Maya Raviv, Shaul Pasmanik-Chor, Metsada Bell, Rachel E Levy, Carmit Avellino, Raffaella Banfi, Sandro Conte, Ivan Ashery-Padan, Ruth |
| description | During development, tissue-specific transcription factors regulate both protein-coding and non-coding genes to control differentiation. Recent studies have established a dual role for the transcription factor Pax6 as both an activator and repressor of gene expression in the eye, central nervous system, and pancreas. However, the molecular mechanism underlying the inhibitory activity of Pax6 is not fully understood. Here, we reveal that Trpm3 and the intronic microRNA gene miR-204 are co-regulated by Pax6 during eye development. miR-204 is probably the best known microRNA to function as a negative modulator of gene expression during eye development in vertebrates. Analysis of genes altered in mouse Pax6 mutants during lens development revealed significant over-representation of miR-204 targets among the genes up-regulated in the Pax6 mutant lens. A number of new targets of miR-204 were revealed, among them Sox11, a member of the SoxC family of pro-neuronal transcription factors, and an important regulator of eye development. Expression of Trpm/miR-204 and a few of its targets are also Pax6-dependent in medaka fish eyes. Collectively, this study identifies a novel evolutionarily conserved mechanism by which Pax6 controls the down-regulation of multiple genes through direct up-regulation of miR-204. |
| doi_str_mv | 10.1371/journal.pgen.1003357 |
| format | Article |
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Recent studies have established a dual role for the transcription factor Pax6 as both an activator and repressor of gene expression in the eye, central nervous system, and pancreas. However, the molecular mechanism underlying the inhibitory activity of Pax6 is not fully understood. Here, we reveal that Trpm3 and the intronic microRNA gene miR-204 are co-regulated by Pax6 during eye development. miR-204 is probably the best known microRNA to function as a negative modulator of gene expression during eye development in vertebrates. Analysis of genes altered in mouse Pax6 mutants during lens development revealed significant over-representation of miR-204 targets among the genes up-regulated in the Pax6 mutant lens. A number of new targets of miR-204 were revealed, among them Sox11, a member of the SoxC family of pro-neuronal transcription factors, and an important regulator of eye development. Expression of Trpm/miR-204 and a few of its targets are also Pax6-dependent in medaka fish eyes. Collectively, this study identifies a novel evolutionarily conserved mechanism by which Pax6 controls the down-regulation of multiple genes through direct up-regulation of miR-204.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1003357</identifier><identifier>PMID: 23516376</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animal development ; Animals ; Binding Sites ; Biology ; Cell culture ; Cell Differentiation - genetics ; Crystallins - genetics ; Crystallins - metabolism ; Evolution, Molecular ; Experiments ; Eye - growth & development ; Eye - metabolism ; Eye Proteins - genetics ; Eye Proteins - metabolism ; Gene expression ; Gene Expression Regulation ; Gene Expression Regulation, Developmental ; Genetic aspects ; Genomics ; Homeodomain Proteins - genetics ; Homeodomain Proteins - metabolism ; Mice ; MicroRNA ; MicroRNAs - genetics ; MicroRNAs - metabolism ; Mutation ; Paired Box Transcription Factors - genetics ; Paired Box Transcription Factors - metabolism ; Pancreas ; PAX6 Transcription Factor ; Properties ; Proteins ; Repressor Proteins - genetics ; Repressor Proteins - metabolism ; Science ; SOXC Transcription Factors - metabolism ; Testing ; Transcription factors ; TRPM Cation Channels - genetics ; TRPM Cation Channels - metabolism ; Vertebrates - genetics ; Vertebrates - metabolism</subject><ispartof>PLoS genetics, 2013-03, Vol.9 (3), p.e1003357-e1003357</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Shaham et al 2013 Shaham et al</rights><rights>2013 Shaham et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Shaham O, Gueta K, Mor E, Oren-Giladi P, Grinberg D, et al. (2013) Pax6 Regulates Gene Expression in the Vertebrate Lens through miR-204. PLoS Genet 9(3): e1003357. doi:10.1371/journal.pgen.1003357</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c698t-55ace16d3142a1a308e6d9f79c8be85d5239c402b6236f3aedc6ff4d86719a7f3</citedby><cites>FETCH-LOGICAL-c698t-55ace16d3142a1a308e6d9f79c8be85d5239c402b6236f3aedc6ff4d86719a7f3</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/PMC3597499/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3597499/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23516376$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shaham, Ohad</creatorcontrib><creatorcontrib>Gueta, Karen</creatorcontrib><creatorcontrib>Mor, Eyal</creatorcontrib><creatorcontrib>Oren-Giladi, Pazit</creatorcontrib><creatorcontrib>Grinberg, Dina</creatorcontrib><creatorcontrib>Xie, Qing</creatorcontrib><creatorcontrib>Cvekl, Ales</creatorcontrib><creatorcontrib>Shomron, Noam</creatorcontrib><creatorcontrib>Davis, Noa</creatorcontrib><creatorcontrib>Keydar-Prizant, Maya</creatorcontrib><creatorcontrib>Raviv, Shaul</creatorcontrib><creatorcontrib>Pasmanik-Chor, Metsada</creatorcontrib><creatorcontrib>Bell, Rachel E</creatorcontrib><creatorcontrib>Levy, Carmit</creatorcontrib><creatorcontrib>Avellino, Raffaella</creatorcontrib><creatorcontrib>Banfi, Sandro</creatorcontrib><creatorcontrib>Conte, Ivan</creatorcontrib><creatorcontrib>Ashery-Padan, Ruth</creatorcontrib><title>Pax6 regulates gene expression in the vertebrate lens through miR-204</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>During development, tissue-specific transcription factors regulate both protein-coding and non-coding genes to control differentiation. Recent studies have established a dual role for the transcription factor Pax6 as both an activator and repressor of gene expression in the eye, central nervous system, and pancreas. However, the molecular mechanism underlying the inhibitory activity of Pax6 is not fully understood. Here, we reveal that Trpm3 and the intronic microRNA gene miR-204 are co-regulated by Pax6 during eye development. miR-204 is probably the best known microRNA to function as a negative modulator of gene expression during eye development in vertebrates. Analysis of genes altered in mouse Pax6 mutants during lens development revealed significant over-representation of miR-204 targets among the genes up-regulated in the Pax6 mutant lens. A number of new targets of miR-204 were revealed, among them Sox11, a member of the SoxC family of pro-neuronal transcription factors, and an important regulator of eye development. Expression of Trpm/miR-204 and a few of its targets are also Pax6-dependent in medaka fish eyes. Collectively, this study identifies a novel evolutionarily conserved mechanism by which Pax6 controls the down-regulation of multiple genes through direct up-regulation of miR-204.</description><subject>Animal development</subject><subject>Animals</subject><subject>Binding Sites</subject><subject>Biology</subject><subject>Cell culture</subject><subject>Cell Differentiation - genetics</subject><subject>Crystallins - genetics</subject><subject>Crystallins - metabolism</subject><subject>Evolution, Molecular</subject><subject>Experiments</subject><subject>Eye - growth & development</subject><subject>Eye - metabolism</subject><subject>Eye Proteins - genetics</subject><subject>Eye Proteins - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Regulation</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genetic aspects</subject><subject>Genomics</subject><subject>Homeodomain Proteins - genetics</subject><subject>Homeodomain Proteins - metabolism</subject><subject>Mice</subject><subject>MicroRNA</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - metabolism</subject><subject>Mutation</subject><subject>Paired Box Transcription Factors - genetics</subject><subject>Paired Box Transcription Factors - metabolism</subject><subject>Pancreas</subject><subject>PAX6 Transcription Factor</subject><subject>Properties</subject><subject>Proteins</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><subject>Science</subject><subject>SOXC Transcription Factors - metabolism</subject><subject>Testing</subject><subject>Transcription factors</subject><subject>TRPM Cation Channels - genetics</subject><subject>TRPM Cation Channels - metabolism</subject><subject>Vertebrates - genetics</subject><subject>Vertebrates - metabolism</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVkl1rFDEUhgdRbF39B6IDgujFrpPvyY1QSqsLxUr9uA2ZmTOzWbKTNcmU9d83607LDnih5CLh5HnfHHLeLHuJigUiAn1Yu8H32i62HfQLVBSEMPEoO0WMkbmgBX18dD7JnoWwTgwrpXianWDCECeCn2YXX_WO5x66weoIIU9mkMNu6yEE4_rc9HlcQX4LPkLlE5Jb6EOqeTd0q3xjbua4oM-zJ622AV6M-yz7cXnx_fzz_Or60_L87Gpec1nGOWO6BsQbgijWSJOiBN7IVsi6rKBkDcNE1rTAFceEt0RDU_O2pU3JBZJatGSWvT74bq0LavyBoBDBQvAkxIlYHojG6bXaerPR_rdy2qg_Bec7pX00tQVVtRwjAhxJ3lAtywo3vOFUkAIxwihJXh_H14Zqk3qBPnptJ6bTm96sVOduFWFSUCmTwbvRwLtfA4SoNibUYK3uwQ37vpFEJeGYJvTNAe10as30rUuO9R5XZwRzVjCRxjfLFn-h0mpgY2rXQ2tSfSJ4PxEkJsIudnoIQS2_3fwH--Xf2eufU_btEbsCbeMqODvElK8wBekBrL0LwUP78NWoUPvM309c7TOvxswn2avjMT2I7kNO7gDI7_lB</recordid><startdate>20130301</startdate><enddate>20130301</enddate><creator>Shaham, Ohad</creator><creator>Gueta, Karen</creator><creator>Mor, Eyal</creator><creator>Oren-Giladi, Pazit</creator><creator>Grinberg, Dina</creator><creator>Xie, Qing</creator><creator>Cvekl, Ales</creator><creator>Shomron, Noam</creator><creator>Davis, Noa</creator><creator>Keydar-Prizant, Maya</creator><creator>Raviv, Shaul</creator><creator>Pasmanik-Chor, Metsada</creator><creator>Bell, Rachel E</creator><creator>Levy, Carmit</creator><creator>Avellino, Raffaella</creator><creator>Banfi, Sandro</creator><creator>Conte, Ivan</creator><creator>Ashery-Padan, Ruth</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130301</creationdate><title>Pax6 regulates gene expression in the vertebrate lens through miR-204</title><author>Shaham, Ohad ; Gueta, Karen ; Mor, Eyal ; Oren-Giladi, Pazit ; Grinberg, Dina ; Xie, Qing ; Cvekl, Ales ; Shomron, Noam ; Davis, Noa ; Keydar-Prizant, Maya ; Raviv, Shaul ; Pasmanik-Chor, Metsada ; Bell, Rachel E ; Levy, Carmit ; Avellino, Raffaella ; Banfi, Sandro ; Conte, Ivan ; Ashery-Padan, Ruth</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c698t-55ace16d3142a1a308e6d9f79c8be85d5239c402b6236f3aedc6ff4d86719a7f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animal development</topic><topic>Animals</topic><topic>Binding Sites</topic><topic>Biology</topic><topic>Cell culture</topic><topic>Cell Differentiation - genetics</topic><topic>Crystallins - genetics</topic><topic>Crystallins - metabolism</topic><topic>Evolution, Molecular</topic><topic>Experiments</topic><topic>Eye - growth & development</topic><topic>Eye - metabolism</topic><topic>Eye Proteins - genetics</topic><topic>Eye Proteins - metabolism</topic><topic>Gene expression</topic><topic>Gene Expression Regulation</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Genetic aspects</topic><topic>Genomics</topic><topic>Homeodomain Proteins - genetics</topic><topic>Homeodomain Proteins - metabolism</topic><topic>Mice</topic><topic>MicroRNA</topic><topic>MicroRNAs - genetics</topic><topic>MicroRNAs - metabolism</topic><topic>Mutation</topic><topic>Paired Box Transcription Factors - genetics</topic><topic>Paired Box Transcription Factors - metabolism</topic><topic>Pancreas</topic><topic>PAX6 Transcription Factor</topic><topic>Properties</topic><topic>Proteins</topic><topic>Repressor Proteins - genetics</topic><topic>Repressor Proteins - metabolism</topic><topic>Science</topic><topic>SOXC Transcription Factors - metabolism</topic><topic>Testing</topic><topic>Transcription factors</topic><topic>TRPM Cation Channels - genetics</topic><topic>TRPM Cation Channels - metabolism</topic><topic>Vertebrates - genetics</topic><topic>Vertebrates - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shaham, Ohad</creatorcontrib><creatorcontrib>Gueta, Karen</creatorcontrib><creatorcontrib>Mor, Eyal</creatorcontrib><creatorcontrib>Oren-Giladi, Pazit</creatorcontrib><creatorcontrib>Grinberg, Dina</creatorcontrib><creatorcontrib>Xie, Qing</creatorcontrib><creatorcontrib>Cvekl, Ales</creatorcontrib><creatorcontrib>Shomron, Noam</creatorcontrib><creatorcontrib>Davis, Noa</creatorcontrib><creatorcontrib>Keydar-Prizant, Maya</creatorcontrib><creatorcontrib>Raviv, Shaul</creatorcontrib><creatorcontrib>Pasmanik-Chor, Metsada</creatorcontrib><creatorcontrib>Bell, Rachel E</creatorcontrib><creatorcontrib>Levy, Carmit</creatorcontrib><creatorcontrib>Avellino, Raffaella</creatorcontrib><creatorcontrib>Banfi, Sandro</creatorcontrib><creatorcontrib>Conte, Ivan</creatorcontrib><creatorcontrib>Ashery-Padan, Ruth</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shaham, Ohad</au><au>Gueta, Karen</au><au>Mor, Eyal</au><au>Oren-Giladi, Pazit</au><au>Grinberg, Dina</au><au>Xie, Qing</au><au>Cvekl, Ales</au><au>Shomron, Noam</au><au>Davis, Noa</au><au>Keydar-Prizant, Maya</au><au>Raviv, Shaul</au><au>Pasmanik-Chor, Metsada</au><au>Bell, Rachel E</au><au>Levy, Carmit</au><au>Avellino, Raffaella</au><au>Banfi, Sandro</au><au>Conte, Ivan</au><au>Ashery-Padan, Ruth</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pax6 regulates gene expression in the vertebrate lens through miR-204</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2013-03-01</date><risdate>2013</risdate><volume>9</volume><issue>3</issue><spage>e1003357</spage><epage>e1003357</epage><pages>e1003357-e1003357</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>During development, tissue-specific transcription factors regulate both protein-coding and non-coding genes to control differentiation. Recent studies have established a dual role for the transcription factor Pax6 as both an activator and repressor of gene expression in the eye, central nervous system, and pancreas. However, the molecular mechanism underlying the inhibitory activity of Pax6 is not fully understood. Here, we reveal that Trpm3 and the intronic microRNA gene miR-204 are co-regulated by Pax6 during eye development. miR-204 is probably the best known microRNA to function as a negative modulator of gene expression during eye development in vertebrates. Analysis of genes altered in mouse Pax6 mutants during lens development revealed significant over-representation of miR-204 targets among the genes up-regulated in the Pax6 mutant lens. A number of new targets of miR-204 were revealed, among them Sox11, a member of the SoxC family of pro-neuronal transcription factors, and an important regulator of eye development. Expression of Trpm/miR-204 and a few of its targets are also Pax6-dependent in medaka fish eyes. Collectively, this study identifies a novel evolutionarily conserved mechanism by which Pax6 controls the down-regulation of multiple genes through direct up-regulation of miR-204.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23516376</pmid><doi>10.1371/journal.pgen.1003357</doi><oa>free_for_read</oa></addata></record> |
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| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | Animal development Animals Binding Sites Biology Cell culture Cell Differentiation - genetics Crystallins - genetics Crystallins - metabolism Evolution, Molecular Experiments Eye - growth & development Eye - metabolism Eye Proteins - genetics Eye Proteins - metabolism Gene expression Gene Expression Regulation Gene Expression Regulation, Developmental Genetic aspects Genomics Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Mice MicroRNA MicroRNAs - genetics MicroRNAs - metabolism Mutation Paired Box Transcription Factors - genetics Paired Box Transcription Factors - metabolism Pancreas PAX6 Transcription Factor Properties Proteins Repressor Proteins - genetics Repressor Proteins - metabolism Science SOXC Transcription Factors - metabolism Testing Transcription factors TRPM Cation Channels - genetics TRPM Cation Channels - metabolism Vertebrates - genetics Vertebrates - metabolism |
| title | Pax6 regulates gene expression in the vertebrate lens through miR-204 |
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