Systematic analysis of transcription start sites in avian development
Cap Analysis of Gene Expression (CAGE) in combination with single-molecule sequencing technology allows precision mapping of transcription start sites (TSSs) and genome-wide capture of promoter activities in differentiated and steady state cell populations. Much less is known about whether TSS profi...
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| creator | Lizio, Marina Deviatiiarov, Ruslan Nagai, Hiroki Galan, Laura Arner, Erik Itoh, Masayoshi Lassmann, Timo Kasukawa, Takeya Hasegawa, Akira Ros, Marian A Hayashizaki, Yoshihide Carninci, Piero Forrest, Alistair R R Kawaji, Hideya Gusev, Oleg Sheng, Guojun |
| description | Cap Analysis of Gene Expression (CAGE) in combination with single-molecule sequencing technology allows precision mapping of transcription start sites (TSSs) and genome-wide capture of promoter activities in differentiated and steady state cell populations. Much less is known about whether TSS profiling can characterize diverse and non-steady state cell populations, such as the approximately 400 transitory and heterogeneous cell types that arise during ontogeny of vertebrate animals. To gain such insight, we used the chick model and performed CAGE-based TSS analysis on embryonic samples covering the full 3-week developmental period. In total, 31,863 robust TSS peaks (>1 tag per million [TPM]) were mapped to the latest chicken genome assembly, of which 34% to 46% were active in any given developmental stage. ZENBU, a web-based, open-source platform, was used for interactive data exploration. TSSs of genes critical for lineage differentiation could be precisely mapped and their activities tracked throughout development, suggesting that non-steady state and heterogeneous cell populations are amenable to CAGE-based transcriptional analysis. Our study also uncovered a large set of extremely stable housekeeping TSSs and many novel stage-specific ones. We furthermore demonstrated that TSS mapping could expedite motif-based promoter analysis for regulatory modules associated with stage-specific and housekeeping genes. Finally, using Brachyury as an example, we provide evidence that precise TSS mapping in combination with Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR)-on technology enables us, for the first time, to efficiently target endogenous avian genes for transcriptional activation. Taken together, our results represent the first report of genome-wide TSS mapping in birds and the first systematic developmental TSS analysis in any amniote species (birds and mammals). By facilitating promoter-based molecular analysis and genetic manipulation, our work also underscores the value of avian models in unravelling the complex regulatory mechanism of cell lineage specification during amniote development. |
| doi_str_mv | 10.1371/journal.pbio.2002887 |
| format | Article |
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Much less is known about whether TSS profiling can characterize diverse and non-steady state cell populations, such as the approximately 400 transitory and heterogeneous cell types that arise during ontogeny of vertebrate animals. To gain such insight, we used the chick model and performed CAGE-based TSS analysis on embryonic samples covering the full 3-week developmental period. In total, 31,863 robust TSS peaks (>1 tag per million [TPM]) were mapped to the latest chicken genome assembly, of which 34% to 46% were active in any given developmental stage. ZENBU, a web-based, open-source platform, was used for interactive data exploration. TSSs of genes critical for lineage differentiation could be precisely mapped and their activities tracked throughout development, suggesting that non-steady state and heterogeneous cell populations are amenable to CAGE-based transcriptional analysis. Our study also uncovered a large set of extremely stable housekeeping TSSs and many novel stage-specific ones. We furthermore demonstrated that TSS mapping could expedite motif-based promoter analysis for regulatory modules associated with stage-specific and housekeeping genes. Finally, using Brachyury as an example, we provide evidence that precise TSS mapping in combination with Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR)-on technology enables us, for the first time, to efficiently target endogenous avian genes for transcriptional activation. Taken together, our results represent the first report of genome-wide TSS mapping in birds and the first systematic developmental TSS analysis in any amniote species (birds and mammals). By facilitating promoter-based molecular analysis and genetic manipulation, our work also underscores the value of avian models in unravelling the complex regulatory mechanism of cell lineage specification during amniote development.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.2002887</identifier><identifier>PMID: 28873399</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Bioinformatics ; Biological Evolution ; Biology and Life Sciences ; Birds ; Cages ; Cell lineage ; Chick Embryo ; Clustered Regularly Interspaced Short Palindromic Repeats ; CRISPR ; Deoxyribonucleic acid ; Developmental biology ; Developmental stages ; DNA ; DNA methylation ; DNA sequencing ; Embryonic Development ; Exploration ; Gene expression ; Gene mapping ; Gene sequencing ; Genes ; Genetic engineering ; Genetic transcription ; Genome-Wide Association Study ; Genomes ; Life sciences ; Mammals ; Mapping ; Medical research ; Methods ; Methods and Resources ; Nucleotide sequencing ; Observations ; Ontogeny ; Populations ; Preventive medicine ; Regulatory mechanisms (biology) ; Research and Analysis Methods ; Software ; Steady state ; Supervision ; Technology ; Transcription activation ; Transcription factors ; Transcription Initiation Site</subject><ispartof>PLoS biology, 2017-09, Vol.15 (9), p.e2002887-e2002887</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Public Library of Science. 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: Lizio M, Deviatiiarov R, Nagai H, Galan L, Arner E, Itoh M, et al. (2017) Systematic analysis of transcription start sites in avian development. PLoS Biol15(9): e2002887. https://doi.org/10.1371/journal.pbio.2002887</rights><rights>2017 Lizio et al 2017 Lizio et al</rights><rights>2017 Public Library of Science. 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: Lizio M, Deviatiiarov R, Nagai H, Galan L, Arner E, Itoh M, et al. (2017) Systematic analysis of transcription start sites in avian development. PLoS Biol15(9): e2002887. https://doi.org/10.1371/journal.pbio.2002887</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c761t-707d222bd59253f3c4702a74fcd1460e3a6325536f5e4a665efe07d10e2f5fa33</citedby><cites>FETCH-LOGICAL-c761t-707d222bd59253f3c4702a74fcd1460e3a6325536f5e4a665efe07d10e2f5fa33</cites><orcidid>0000-0001-6759-3785</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5600399/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5600399/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28873399$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Briscoe, James</contributor><creatorcontrib>Lizio, Marina</creatorcontrib><creatorcontrib>Deviatiiarov, Ruslan</creatorcontrib><creatorcontrib>Nagai, Hiroki</creatorcontrib><creatorcontrib>Galan, Laura</creatorcontrib><creatorcontrib>Arner, Erik</creatorcontrib><creatorcontrib>Itoh, Masayoshi</creatorcontrib><creatorcontrib>Lassmann, Timo</creatorcontrib><creatorcontrib>Kasukawa, Takeya</creatorcontrib><creatorcontrib>Hasegawa, Akira</creatorcontrib><creatorcontrib>Ros, Marian A</creatorcontrib><creatorcontrib>Hayashizaki, Yoshihide</creatorcontrib><creatorcontrib>Carninci, Piero</creatorcontrib><creatorcontrib>Forrest, Alistair R R</creatorcontrib><creatorcontrib>Kawaji, Hideya</creatorcontrib><creatorcontrib>Gusev, Oleg</creatorcontrib><creatorcontrib>Sheng, Guojun</creatorcontrib><title>Systematic analysis of transcription start sites in avian development</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>Cap Analysis of Gene Expression (CAGE) in combination with single-molecule sequencing technology allows precision mapping of transcription start sites (TSSs) and genome-wide capture of promoter activities in differentiated and steady state cell populations. Much less is known about whether TSS profiling can characterize diverse and non-steady state cell populations, such as the approximately 400 transitory and heterogeneous cell types that arise during ontogeny of vertebrate animals. To gain such insight, we used the chick model and performed CAGE-based TSS analysis on embryonic samples covering the full 3-week developmental period. In total, 31,863 robust TSS peaks (>1 tag per million [TPM]) were mapped to the latest chicken genome assembly, of which 34% to 46% were active in any given developmental stage. ZENBU, a web-based, open-source platform, was used for interactive data exploration. TSSs of genes critical for lineage differentiation could be precisely mapped and their activities tracked throughout development, suggesting that non-steady state and heterogeneous cell populations are amenable to CAGE-based transcriptional analysis. Our study also uncovered a large set of extremely stable housekeeping TSSs and many novel stage-specific ones. We furthermore demonstrated that TSS mapping could expedite motif-based promoter analysis for regulatory modules associated with stage-specific and housekeeping genes. Finally, using Brachyury as an example, we provide evidence that precise TSS mapping in combination with Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR)-on technology enables us, for the first time, to efficiently target endogenous avian genes for transcriptional activation. Taken together, our results represent the first report of genome-wide TSS mapping in birds and the first systematic developmental TSS analysis in any amniote species (birds and mammals). By facilitating promoter-based molecular analysis and genetic manipulation, our work also underscores the value of avian models in unravelling the complex regulatory mechanism of cell lineage specification during amniote development.</description><subject>Animals</subject><subject>Bioinformatics</subject><subject>Biological Evolution</subject><subject>Biology and Life Sciences</subject><subject>Birds</subject><subject>Cages</subject><subject>Cell lineage</subject><subject>Chick Embryo</subject><subject>Clustered Regularly Interspaced Short Palindromic Repeats</subject><subject>CRISPR</subject><subject>Deoxyribonucleic acid</subject><subject>Developmental biology</subject><subject>Developmental stages</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>DNA sequencing</subject><subject>Embryonic Development</subject><subject>Exploration</subject><subject>Gene expression</subject><subject>Gene mapping</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genetic engineering</subject><subject>Genetic transcription</subject><subject>Genome-Wide Association Study</subject><subject>Genomes</subject><subject>Life sciences</subject><subject>Mammals</subject><subject>Mapping</subject><subject>Medical research</subject><subject>Methods</subject><subject>Methods and Resources</subject><subject>Nucleotide sequencing</subject><subject>Observations</subject><subject>Ontogeny</subject><subject>Populations</subject><subject>Preventive medicine</subject><subject>Regulatory mechanisms (biology)</subject><subject>Research and Analysis Methods</subject><subject>Software</subject><subject>Steady state</subject><subject>Supervision</subject><subject>Technology</subject><subject>Transcription activation</subject><subject>Transcription factors</subject><subject>Transcription Initiation 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analysis of transcription start sites in avian development</title><author>Lizio, Marina ; Deviatiiarov, Ruslan ; Nagai, Hiroki ; Galan, Laura ; Arner, Erik ; Itoh, Masayoshi ; Lassmann, Timo ; Kasukawa, Takeya ; Hasegawa, Akira ; Ros, Marian A ; Hayashizaki, Yoshihide ; Carninci, Piero ; Forrest, Alistair R R ; Kawaji, Hideya ; Gusev, Oleg ; Sheng, Guojun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c761t-707d222bd59253f3c4702a74fcd1460e3a6325536f5e4a665efe07d10e2f5fa33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Bioinformatics</topic><topic>Biological Evolution</topic><topic>Biology and Life Sciences</topic><topic>Birds</topic><topic>Cages</topic><topic>Cell lineage</topic><topic>Chick Embryo</topic><topic>Clustered Regularly Interspaced Short Palindromic Repeats</topic><topic>CRISPR</topic><topic>Deoxyribonucleic 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Guojun</au><au>Briscoe, James</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Systematic analysis of transcription start sites in avian development</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2017-09-05</date><risdate>2017</risdate><volume>15</volume><issue>9</issue><spage>e2002887</spage><epage>e2002887</epage><pages>e2002887-e2002887</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>Cap Analysis of Gene Expression (CAGE) in combination with single-molecule sequencing technology allows precision mapping of transcription start sites (TSSs) and genome-wide capture of promoter activities in differentiated and steady state cell populations. Much less is known about whether TSS profiling can characterize diverse and non-steady state cell populations, such as the approximately 400 transitory and heterogeneous cell types that arise during ontogeny of vertebrate animals. To gain such insight, we used the chick model and performed CAGE-based TSS analysis on embryonic samples covering the full 3-week developmental period. In total, 31,863 robust TSS peaks (>1 tag per million [TPM]) were mapped to the latest chicken genome assembly, of which 34% to 46% were active in any given developmental stage. ZENBU, a web-based, open-source platform, was used for interactive data exploration. TSSs of genes critical for lineage differentiation could be precisely mapped and their activities tracked throughout development, suggesting that non-steady state and heterogeneous cell populations are amenable to CAGE-based transcriptional analysis. Our study also uncovered a large set of extremely stable housekeeping TSSs and many novel stage-specific ones. We furthermore demonstrated that TSS mapping could expedite motif-based promoter analysis for regulatory modules associated with stage-specific and housekeeping genes. Finally, using Brachyury as an example, we provide evidence that precise TSS mapping in combination with Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR)-on technology enables us, for the first time, to efficiently target endogenous avian genes for transcriptional activation. Taken together, our results represent the first report of genome-wide TSS mapping in birds and the first systematic developmental TSS analysis in any amniote species (birds and mammals). By facilitating promoter-based molecular analysis and genetic manipulation, our work also underscores the value of avian models in unravelling the complex regulatory mechanism of cell lineage specification during amniote development.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28873399</pmid><doi>10.1371/journal.pbio.2002887</doi><orcidid>https://orcid.org/0000-0001-6759-3785</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1545-7885 |
| ispartof | PLoS biology, 2017-09, Vol.15 (9), p.e2002887-e2002887 |
| issn | 1545-7885 1544-9173 1545-7885 |
| language | eng |
| recordid | cdi_plos_journals_1951453941 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Animals Bioinformatics Biological Evolution Biology and Life Sciences Birds Cages Cell lineage Chick Embryo Clustered Regularly Interspaced Short Palindromic Repeats CRISPR Deoxyribonucleic acid Developmental biology Developmental stages DNA DNA methylation DNA sequencing Embryonic Development Exploration Gene expression Gene mapping Gene sequencing Genes Genetic engineering Genetic transcription Genome-Wide Association Study Genomes Life sciences Mammals Mapping Medical research Methods Methods and Resources Nucleotide sequencing Observations Ontogeny Populations Preventive medicine Regulatory mechanisms (biology) Research and Analysis Methods Software Steady state Supervision Technology Transcription activation Transcription factors Transcription Initiation Site |
| title | Systematic analysis of transcription start sites in avian development |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-28T23%3A42%3A43IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Systematic%20analysis%20of%20transcription%20start%20sites%20in%20avian%20development&rft.jtitle=PLoS%20biology&rft.au=Lizio,%20Marina&rft.date=2017-09-05&rft.volume=15&rft.issue=9&rft.spage=e2002887&rft.epage=e2002887&rft.pages=e2002887-e2002887&rft.issn=1545-7885&rft.eissn=1545-7885&rft_id=info:doi/10.1371/journal.pbio.2002887&rft_dat=%3Cgale_plos_%3EA507385045%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1951453941&rft_id=info:pmid/28873399&rft_galeid=A507385045&rft_doaj_id=oai_doaj_org_article_0228b3fecd784d699da9ea289bdbf602&rfr_iscdi=true |