Inheritable and precise large genomic deletions of non-coding RNA genes in zebrafish using TALENs
Transcription activator-like effector nucleases (TALENs) have so far been applied to disrupt protein-coding genes which constitute only 2-3% of the genome in animals. The majority (70-90%) of the animal genome is actually transcribed as non-coding RNAs (ncRNAs), yet the lack of efficient tools to kn...
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| creator | Liu, Yun Luo, Daji Zhao, Hui Zhu, Zuoyan Hu, Wei Cheng, Christopher H K |
| description | Transcription activator-like effector nucleases (TALENs) have so far been applied to disrupt protein-coding genes which constitute only 2-3% of the genome in animals. The majority (70-90%) of the animal genome is actually transcribed as non-coding RNAs (ncRNAs), yet the lack of efficient tools to knockout ncRNA genes hinders studies on their in vivo functions. Here we have developed novel strategies using TALENs to achieve precise and inheritable large genomic deletions and knockout of ncRNA genes in zebrafish. We have demonstrated that individual miRNA genes could be disrupted using one pair of TALENs, whereas large microRNA (miRNA) gene clusters and long non-coding RNA (lncRNA) genes could be precisely deleted using two pairs of TALENs. We have generated large genomic deletions of two miRNA clusters (the 1.2 kb miR-17-92 cluster and the 79.8 kb miR-430 cluster) and one long non-coding RNA (lncRNA) gene (the 9.0 kb malat1), and the deletions are transmitted through the germline. Taken together, our results establish TALENs as a robust tool to engineer large genomic deletions and knockout of ncRNA genes, thus opening up new avenues in the application of TALENs to study the genome in vivo. |
| doi_str_mv | 10.1371/journal.pone.0076387 |
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The majority (70-90%) of the animal genome is actually transcribed as non-coding RNAs (ncRNAs), yet the lack of efficient tools to knockout ncRNA genes hinders studies on their in vivo functions. Here we have developed novel strategies using TALENs to achieve precise and inheritable large genomic deletions and knockout of ncRNA genes in zebrafish. We have demonstrated that individual miRNA genes could be disrupted using one pair of TALENs, whereas large microRNA (miRNA) gene clusters and long non-coding RNA (lncRNA) genes could be precisely deleted using two pairs of TALENs. We have generated large genomic deletions of two miRNA clusters (the 1.2 kb miR-17-92 cluster and the 79.8 kb miR-430 cluster) and one long non-coding RNA (lncRNA) gene (the 9.0 kb malat1), and the deletions are transmitted through the germline. Taken together, our results establish TALENs as a robust tool to engineer large genomic deletions and knockout of ncRNA genes, thus opening up new avenues in the application of TALENs to study the genome in vivo.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0076387</identifier><identifier>PMID: 24130773</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Base Sequence ; Biotechnology ; Cloning ; Clusters ; Danio rerio ; Deoxyribonucleases - metabolism ; Deoxyribonucleic acid ; DNA ; DNA binding proteins ; Freshwater ecology ; Gene clusters ; Gene expression ; Gene Knockout Techniques ; Genes ; Genetic Engineering - methods ; Genetic research ; Genomes ; Genomics ; Germ Cells - metabolism ; In vivo methods and tests ; Laboratories ; MicroRNA ; MicroRNAs ; MicroRNAs - genetics ; miRNA ; Morphogenesis ; Multigene Family - genetics ; Mutation ; Non-coding RNA ; Nuclease ; Nucleases ; Plasmids ; Proteins ; Ribonucleic acid ; RNA ; RNA, Untranslated - genetics ; Transcription ; Transcription activator-like effector nucleases ; Zebrafish ; Zebrafish - genetics</subject><ispartof>PloS one, 2013-10, Vol.8 (10), p.e76387-e76387</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-f08677a2148e2470aca91d01ba14e7e79a6ca2fa2618fd95a3695bdc1bb028193</citedby><cites>FETCH-LOGICAL-c758t-f08677a2148e2470aca91d01ba14e7e79a6ca2fa2618fd95a3695bdc1bb028193</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/PMC3794983/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3794983/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24130773$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Gong, Zhiyuan</contributor><creatorcontrib>Liu, Yun</creatorcontrib><creatorcontrib>Luo, Daji</creatorcontrib><creatorcontrib>Zhao, Hui</creatorcontrib><creatorcontrib>Zhu, Zuoyan</creatorcontrib><creatorcontrib>Hu, Wei</creatorcontrib><creatorcontrib>Cheng, Christopher H K</creatorcontrib><title>Inheritable and precise large genomic deletions of non-coding RNA genes in zebrafish using TALENs</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Transcription activator-like effector nucleases (TALENs) have so far been applied to disrupt protein-coding genes which constitute only 2-3% of the genome in animals. The majority (70-90%) of the animal genome is actually transcribed as non-coding RNAs (ncRNAs), yet the lack of efficient tools to knockout ncRNA genes hinders studies on their in vivo functions. Here we have developed novel strategies using TALENs to achieve precise and inheritable large genomic deletions and knockout of ncRNA genes in zebrafish. We have demonstrated that individual miRNA genes could be disrupted using one pair of TALENs, whereas large microRNA (miRNA) gene clusters and long non-coding RNA (lncRNA) genes could be precisely deleted using two pairs of TALENs. We have generated large genomic deletions of two miRNA clusters (the 1.2 kb miR-17-92 cluster and the 79.8 kb miR-430 cluster) and one long non-coding RNA (lncRNA) gene (the 9.0 kb malat1), and the deletions are transmitted through the germline. Taken together, our results establish TALENs as a robust tool to engineer large genomic deletions and knockout of ncRNA genes, thus opening up new avenues in the application of TALENs to study the genome in vivo.</description><subject>Animals</subject><subject>Base Sequence</subject><subject>Biotechnology</subject><subject>Cloning</subject><subject>Clusters</subject><subject>Danio rerio</subject><subject>Deoxyribonucleases - metabolism</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA binding proteins</subject><subject>Freshwater ecology</subject><subject>Gene clusters</subject><subject>Gene expression</subject><subject>Gene Knockout Techniques</subject><subject>Genes</subject><subject>Genetic Engineering - methods</subject><subject>Genetic research</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Germ Cells - metabolism</subject><subject>In vivo methods and tests</subject><subject>Laboratories</subject><subject>MicroRNA</subject><subject>MicroRNAs</subject><subject>MicroRNAs - genetics</subject><subject>miRNA</subject><subject>Morphogenesis</subject><subject>Multigene Family - genetics</subject><subject>Mutation</subject><subject>Non-coding RNA</subject><subject>Nuclease</subject><subject>Nucleases</subject><subject>Plasmids</subject><subject>Proteins</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Untranslated - genetics</subject><subject>Transcription</subject><subject>Transcription activator-like effector nucleases</subject><subject>Zebrafish</subject><subject>Zebrafish - genetics</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk1FrFDEQxxdRbK1-A9EFQfThzmSTS3ZfhKNUPThaqNXXkM1O9lJyyZnsivrpzd5ty630QQJJSH7zn8xkJsteYjTHhOMPt74PTtr5zjuYI8QZKfmj7BRXpJixApHHR_uT7FmMtwgtSMnY0-ykoJggzslpJlduA8F0sraQS9fkuwDKRMitDC3kLTi_NSpvwEJnvIu517nzbqZ8Y1ybX18uBwZiblz-B-ogtYmbvI_D5c1yfXEZn2dPtLQRXozrWfbt08XN-ZfZ-urz6ny5nim-KLuZRiXjXBaYllBQjqSSFW4QriWmwIFXkilZaFkwXOqmWkjCqkXdKFzXqChTpGfZ64PuzvooxuxEgSnFRYkoYolYHYjGy1uxC2Yrw2_hpRH7Ax9aIUNnlAXBmSpUmgAhTHXBao0bihkieqFTogdvH0dvfb2FRoHrgrQT0emNMxvR-p-C8IpWJUkC70aB4H_0EDuxNVGBtdKB7_fvJlVV0pIm9M0_6MPRjVQrUwDGaZ_8qkFULClPHheJTdT8ASqNBtI_p1LSJp1PDN5PDBLTwa-ulX2MYvX1-v_Zq-9T9u0RuwFpu030tt9X2RSkB1AFH2MAfZ9kjMTQCXfZEEMniLETktmr4w-6N7orffIXeysB1Q</recordid><startdate>20131010</startdate><enddate>20131010</enddate><creator>Liu, Yun</creator><creator>Luo, Daji</creator><creator>Zhao, Hui</creator><creator>Zhu, Zuoyan</creator><creator>Hu, Wei</creator><creator>Cheng, Christopher H K</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>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20131010</creationdate><title>Inheritable and precise large genomic deletions of non-coding RNA genes in zebrafish using TALENs</title><author>Liu, Yun ; Luo, Daji ; Zhao, Hui ; Zhu, Zuoyan ; Hu, Wei ; Cheng, Christopher H K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-f08677a2148e2470aca91d01ba14e7e79a6ca2fa2618fd95a3695bdc1bb028193</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Base Sequence</topic><topic>Biotechnology</topic><topic>Cloning</topic><topic>Clusters</topic><topic>Danio rerio</topic><topic>Deoxyribonucleases - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Yun</au><au>Luo, Daji</au><au>Zhao, Hui</au><au>Zhu, Zuoyan</au><au>Hu, Wei</au><au>Cheng, Christopher H K</au><au>Gong, Zhiyuan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Inheritable and precise large genomic deletions of non-coding RNA genes in zebrafish using TALENs</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-10-10</date><risdate>2013</risdate><volume>8</volume><issue>10</issue><spage>e76387</spage><epage>e76387</epage><pages>e76387-e76387</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Transcription activator-like effector nucleases (TALENs) have so far been applied to disrupt protein-coding genes which constitute only 2-3% of the genome in animals. The majority (70-90%) of the animal genome is actually transcribed as non-coding RNAs (ncRNAs), yet the lack of efficient tools to knockout ncRNA genes hinders studies on their in vivo functions. Here we have developed novel strategies using TALENs to achieve precise and inheritable large genomic deletions and knockout of ncRNA genes in zebrafish. We have demonstrated that individual miRNA genes could be disrupted using one pair of TALENs, whereas large microRNA (miRNA) gene clusters and long non-coding RNA (lncRNA) genes could be precisely deleted using two pairs of TALENs. We have generated large genomic deletions of two miRNA clusters (the 1.2 kb miR-17-92 cluster and the 79.8 kb miR-430 cluster) and one long non-coding RNA (lncRNA) gene (the 9.0 kb malat1), and the deletions are transmitted through the germline. Taken together, our results establish TALENs as a robust tool to engineer large genomic deletions and knockout of ncRNA genes, thus opening up new avenues in the application of TALENs to study the genome in vivo.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24130773</pmid><doi>10.1371/journal.pone.0076387</doi><tpages>e76387</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Animals Base Sequence Biotechnology Cloning Clusters Danio rerio Deoxyribonucleases - metabolism Deoxyribonucleic acid DNA DNA binding proteins Freshwater ecology Gene clusters Gene expression Gene Knockout Techniques Genes Genetic Engineering - methods Genetic research Genomes Genomics Germ Cells - metabolism In vivo methods and tests Laboratories MicroRNA MicroRNAs MicroRNAs - genetics miRNA Morphogenesis Multigene Family - genetics Mutation Non-coding RNA Nuclease Nucleases Plasmids Proteins Ribonucleic acid RNA RNA, Untranslated - genetics Transcription Transcription activator-like effector nucleases Zebrafish Zebrafish - genetics |
| title | Inheritable and precise large genomic deletions of non-coding RNA genes in zebrafish using TALENs |
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