Identification of estrogen target genes during zebrafish embryonic development through transcriptomic analysis
Estrogen signaling is important for vertebrate embryonic development. Here we have used zebrafish (Danio rerio) as a vertebrate model to analyze estrogen signaling during development. Zebrafish embryos were exposed to 1 µM 17β-estradiol (E2) or vehicle from 3 hours to 4 days post fertilization (dpf)...
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| description | Estrogen signaling is important for vertebrate embryonic development. Here we have used zebrafish (Danio rerio) as a vertebrate model to analyze estrogen signaling during development. Zebrafish embryos were exposed to 1 µM 17β-estradiol (E2) or vehicle from 3 hours to 4 days post fertilization (dpf), harvested at 1, 2, 3 and 4 dpf, and subjected to RNA extraction for transcriptome analysis using microarrays. Differentially expressed genes by E2-treatment were analyzed with hierarchical clustering followed by biological process and tissue enrichment analysis. Markedly distinct sets of genes were up and down-regulated by E2 at the four different time points. Among these genes, only the well-known estrogenic marker vtg1 was co-regulated at all time points. Despite this, the biological functional categories targeted by E2 were relatively similar throughout zebrafish development. According to knowledge-based tissue enrichment, estrogen responsive genes were clustered mainly in the liver, pancreas and brain. This was in line with the developmental dynamics of estrogen-target tissues that were visualized using transgenic zebrafish containing estrogen responsive elements driving the expression of GFP (Tg(5xERE:GFP)). Finally, the identified embryonic estrogen-responsive genes were compared to already published estrogen-responsive genes identified in male adult zebrafish (Gene Expression Omnibus database). The expressions of a few genes were co-regulated by E2 in both embryonic and adult zebrafish. These could potentially be used as estrogenic biomarkers for exposure to estrogens or estrogenic endocrine disruptors in zebrafish. In conclusion, our data suggests that estrogen effects on early embryonic zebrafish development are stage- and tissue- specific. |
| doi_str_mv | 10.1371/journal.pone.0079020 |
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Here we have used zebrafish (Danio rerio) as a vertebrate model to analyze estrogen signaling during development. Zebrafish embryos were exposed to 1 µM 17β-estradiol (E2) or vehicle from 3 hours to 4 days post fertilization (dpf), harvested at 1, 2, 3 and 4 dpf, and subjected to RNA extraction for transcriptome analysis using microarrays. Differentially expressed genes by E2-treatment were analyzed with hierarchical clustering followed by biological process and tissue enrichment analysis. Markedly distinct sets of genes were up and down-regulated by E2 at the four different time points. Among these genes, only the well-known estrogenic marker vtg1 was co-regulated at all time points. Despite this, the biological functional categories targeted by E2 were relatively similar throughout zebrafish development. According to knowledge-based tissue enrichment, estrogen responsive genes were clustered mainly in the liver, pancreas and brain. This was in line with the developmental dynamics of estrogen-target tissues that were visualized using transgenic zebrafish containing estrogen responsive elements driving the expression of GFP (Tg(5xERE:GFP)). Finally, the identified embryonic estrogen-responsive genes were compared to already published estrogen-responsive genes identified in male adult zebrafish (Gene Expression Omnibus database). The expressions of a few genes were co-regulated by E2 in both embryonic and adult zebrafish. These could potentially be used as estrogenic biomarkers for exposure to estrogens or estrogenic endocrine disruptors in zebrafish. In conclusion, our data suggests that estrogen effects on early embryonic zebrafish development are stage- and tissue- specific.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0079020</identifier><identifier>PMID: 24223173</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>17β-Estradiol ; Animal genetic engineering ; Animals ; Animals, Genetically Modified ; Apoptosis ; Biochemistry ; Biological activity ; Biology ; Biomarkers ; Brain ; Brain research ; Cancer ; Cell cycle ; Cell growth ; Cluster Analysis ; Clustering ; Danio rerio ; Developmental stages ; DNA microarrays ; Dose-Response Relationship, Drug ; Embryo, Nonmammalian - drug effects ; Embryo, Nonmammalian - embryology ; Embryo, Nonmammalian - metabolism ; Embryogenesis ; Embryonic development ; Embryonic growth stage ; Embryos ; Endocrine disruptors ; Enrichment ; Environmental protection ; Estradiol ; Estradiol - pharmacology ; Estrogen Receptor alpha - genetics ; Estrogens ; Estrogens - pharmacology ; Fertilization ; Gene expression ; Gene Expression Regulation, Developmental - drug effects ; Gene Ontology ; Genes ; Genetic aspects ; Green Fluorescent Proteins - genetics ; Green Fluorescent Proteins - metabolism ; In Situ Hybridization ; Infertility ; Kinases ; Liver ; Male ; Microscopy, Fluorescence ; Oligonucleotide Array Sequence Analysis ; Pancreas ; Phenols (Class of compounds) ; Principal Component Analysis ; Proteins ; R&D ; Research & development ; Reverse Transcriptase Polymerase Chain Reaction ; Ribonucleic acid ; RNA ; Sex hormones ; Signaling ; Studies ; Target recognition ; Time Factors ; Tissue analysis ; Tissues ; Toxicology ; Transcriptome - drug effects ; Xenoestrogens ; Zebrafish ; Zebrafish - embryology ; Zebrafish - genetics ; Zebrafish - growth & development ; Zebrafish Proteins - genetics</subject><ispartof>PloS one, 2013-11, Vol.8 (11), p.e79020</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Hao et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Hao et al 2013 Hao et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c730t-33e65b6dc8d86261f2fd499565cf8883d8459908c6bf2fecdfb5d893dcb81a663</citedby><cites>FETCH-LOGICAL-c730t-33e65b6dc8d86261f2fd499565cf8883d8459908c6bf2fecdfb5d893dcb81a663</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/PMC3819264/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3819264/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,550,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24223173$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:127729353$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><contributor>Gong, Zhiyuan</contributor><creatorcontrib>Hao, Ruixin</creatorcontrib><creatorcontrib>Bondesson, Maria</creatorcontrib><creatorcontrib>Singh, Amar V</creatorcontrib><creatorcontrib>Riu, Anne</creatorcontrib><creatorcontrib>McCollum, Catherine W</creatorcontrib><creatorcontrib>Knudsen, Thomas B</creatorcontrib><creatorcontrib>Gorelick, Daniel A</creatorcontrib><creatorcontrib>Gustafsson, Jan-Åke</creatorcontrib><title>Identification of estrogen target genes during zebrafish embryonic development through transcriptomic analysis</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Estrogen signaling is important for vertebrate embryonic development. Here we have used zebrafish (Danio rerio) as a vertebrate model to analyze estrogen signaling during development. Zebrafish embryos were exposed to 1 µM 17β-estradiol (E2) or vehicle from 3 hours to 4 days post fertilization (dpf), harvested at 1, 2, 3 and 4 dpf, and subjected to RNA extraction for transcriptome analysis using microarrays. Differentially expressed genes by E2-treatment were analyzed with hierarchical clustering followed by biological process and tissue enrichment analysis. Markedly distinct sets of genes were up and down-regulated by E2 at the four different time points. Among these genes, only the well-known estrogenic marker vtg1 was co-regulated at all time points. Despite this, the biological functional categories targeted by E2 were relatively similar throughout zebrafish development. According to knowledge-based tissue enrichment, estrogen responsive genes were clustered mainly in the liver, pancreas and brain. This was in line with the developmental dynamics of estrogen-target tissues that were visualized using transgenic zebrafish containing estrogen responsive elements driving the expression of GFP (Tg(5xERE:GFP)). Finally, the identified embryonic estrogen-responsive genes were compared to already published estrogen-responsive genes identified in male adult zebrafish (Gene Expression Omnibus database). The expressions of a few genes were co-regulated by E2 in both embryonic and adult zebrafish. These could potentially be used as estrogenic biomarkers for exposure to estrogens or estrogenic endocrine disruptors in zebrafish. In conclusion, our data suggests that estrogen effects on early embryonic zebrafish development are stage- and tissue- specific.</description><subject>17β-Estradiol</subject><subject>Animal genetic engineering</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Apoptosis</subject><subject>Biochemistry</subject><subject>Biological activity</subject><subject>Biology</subject><subject>Biomarkers</subject><subject>Brain</subject><subject>Brain research</subject><subject>Cancer</subject><subject>Cell cycle</subject><subject>Cell growth</subject><subject>Cluster Analysis</subject><subject>Clustering</subject><subject>Danio rerio</subject><subject>Developmental stages</subject><subject>DNA microarrays</subject><subject>Dose-Response Relationship, Drug</subject><subject>Embryo, Nonmammalian - drug effects</subject><subject>Embryo, Nonmammalian - embryology</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Embryogenesis</subject><subject>Embryonic development</subject><subject>Embryonic growth stage</subject><subject>Embryos</subject><subject>Endocrine disruptors</subject><subject>Enrichment</subject><subject>Environmental protection</subject><subject>Estradiol</subject><subject>Estradiol - pharmacology</subject><subject>Estrogen Receptor alpha - genetics</subject><subject>Estrogens</subject><subject>Estrogens - pharmacology</subject><subject>Fertilization</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental - drug effects</subject><subject>Gene Ontology</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Green Fluorescent Proteins - genetics</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>In Situ Hybridization</subject><subject>Infertility</subject><subject>Kinases</subject><subject>Liver</subject><subject>Male</subject><subject>Microscopy, Fluorescence</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Pancreas</subject><subject>Phenols (Class of compounds)</subject><subject>Principal Component Analysis</subject><subject>Proteins</subject><subject>R&D</subject><subject>Research & development</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Sex hormones</subject><subject>Signaling</subject><subject>Studies</subject><subject>Target recognition</subject><subject>Time Factors</subject><subject>Tissue analysis</subject><subject>Tissues</subject><subject>Toxicology</subject><subject>Transcriptome - drug effects</subject><subject>Xenoestrogens</subject><subject>Zebrafish</subject><subject>Zebrafish - embryology</subject><subject>Zebrafish - genetics</subject><subject>Zebrafish - growth & development</subject><subject>Zebrafish Proteins - 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>BENPR</sourceid><sourceid>D8T</sourceid><sourceid>DOA</sourceid><recordid>eNqNk12L1DAUhoso7rr6D0QLguDFjPlqmt4Iy-LHwMKCX7chTdI2a9uMSbo6_nrPON1lCgq2Fz2cPOftyZucLHuK0RrTEr--9lMYVb_e-tGuESorRNC97BRXlKw4QfT-UXySPYrxGqGCCs4fZieEEUJxSU-zcWPsmFzjtErOj7lvchtT8K0d86RCa1MOoY25mYIb2_yXrYNqXOxyO9Rh50enc2NvbO-3AwjlqQt-ars8BTVGHdw2-QEQBZ3uoouPsweN6qN9Mn_Psi_v3n6--LC6vHq_uTi_XOmSorSi1PKi5kYLIzjhuCGNYVVV8EI3QghqBCuqCgnNa1iy2jR1YURFja4FVpzTs-z5QXfb-yhnq6LErMAU3CMCiM2BMF5dy21wgwo76ZWTfxI-tFKF5HRvJcFlBVYyyuDBmtWYl6gobc1ZXXK9_9vqoBV_2O1UL9Tm1DeIrCwIbKEE_s3c3VQP1mgwLqh-UbZcGV0nW38jqcAV4QwEXswCwX-f4MD-scWZahXswo2NBzE9uKjlOSsFQwy6AWr9FwpeY-Hk4HI1DvKLgleLAmCS_ZlaNcUoN58-_j979XXJvjxiO6v61EXfT_t7GZcgO4A6-BiDbe6cw0juZ-PWDbmfDTnPBpQ9O3b9ruh2GOhv9SMMAQ</recordid><startdate>20131106</startdate><enddate>20131106</enddate><creator>Hao, Ruixin</creator><creator>Bondesson, Maria</creator><creator>Singh, Amar V</creator><creator>Riu, Anne</creator><creator>McCollum, Catherine W</creator><creator>Knudsen, Thomas B</creator><creator>Gorelick, Daniel A</creator><creator>Gustafsson, Jan-Åke</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>AEUYN</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>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>ZZAVC</scope><scope>DOA</scope></search><sort><creationdate>20131106</creationdate><title>Identification of estrogen target genes during zebrafish embryonic development through transcriptomic analysis</title><author>Hao, Ruixin ; Bondesson, Maria ; Singh, Amar V ; Riu, Anne ; McCollum, Catherine W ; Knudsen, Thomas B ; Gorelick, Daniel A ; Gustafsson, Jan-Åke</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c730t-33e65b6dc8d86261f2fd499565cf8883d8459908c6bf2fecdfb5d893dcb81a663</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>17β-Estradiol</topic><topic>Animal genetic engineering</topic><topic>Animals</topic><topic>Animals, Genetically Modified</topic><topic>Apoptosis</topic><topic>Biochemistry</topic><topic>Biological activity</topic><topic>Biology</topic><topic>Biomarkers</topic><topic>Brain</topic><topic>Brain research</topic><topic>Cancer</topic><topic>Cell cycle</topic><topic>Cell growth</topic><topic>Cluster Analysis</topic><topic>Clustering</topic><topic>Danio rerio</topic><topic>Developmental stages</topic><topic>DNA microarrays</topic><topic>Dose-Response Relationship, Drug</topic><topic>Embryo, Nonmammalian - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SwePub Articles full text</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>Hao, Ruixin</au><au>Bondesson, Maria</au><au>Singh, Amar V</au><au>Riu, Anne</au><au>McCollum, Catherine W</au><au>Knudsen, Thomas B</au><au>Gorelick, Daniel A</au><au>Gustafsson, Jan-Åke</au><au>Gong, Zhiyuan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Identification of estrogen target genes during zebrafish embryonic development through transcriptomic analysis</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-11-06</date><risdate>2013</risdate><volume>8</volume><issue>11</issue><spage>e79020</spage><pages>e79020-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Estrogen signaling is important for vertebrate embryonic development. Here we have used zebrafish (Danio rerio) as a vertebrate model to analyze estrogen signaling during development. Zebrafish embryos were exposed to 1 µM 17β-estradiol (E2) or vehicle from 3 hours to 4 days post fertilization (dpf), harvested at 1, 2, 3 and 4 dpf, and subjected to RNA extraction for transcriptome analysis using microarrays. Differentially expressed genes by E2-treatment were analyzed with hierarchical clustering followed by biological process and tissue enrichment analysis. Markedly distinct sets of genes were up and down-regulated by E2 at the four different time points. Among these genes, only the well-known estrogenic marker vtg1 was co-regulated at all time points. Despite this, the biological functional categories targeted by E2 were relatively similar throughout zebrafish development. According to knowledge-based tissue enrichment, estrogen responsive genes were clustered mainly in the liver, pancreas and brain. This was in line with the developmental dynamics of estrogen-target tissues that were visualized using transgenic zebrafish containing estrogen responsive elements driving the expression of GFP (Tg(5xERE:GFP)). Finally, the identified embryonic estrogen-responsive genes were compared to already published estrogen-responsive genes identified in male adult zebrafish (Gene Expression Omnibus database). The expressions of a few genes were co-regulated by E2 in both embryonic and adult zebrafish. These could potentially be used as estrogenic biomarkers for exposure to estrogens or estrogenic endocrine disruptors in zebrafish. In conclusion, our data suggests that estrogen effects on early embryonic zebrafish development are stage- and tissue- specific.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24223173</pmid><doi>10.1371/journal.pone.0079020</doi><tpages>e79020</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-11, Vol.8 (11), p.e79020 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1451313728 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; SWEPUB Freely available online; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | 17β-Estradiol Animal genetic engineering Animals Animals, Genetically Modified Apoptosis Biochemistry Biological activity Biology Biomarkers Brain Brain research Cancer Cell cycle Cell growth Cluster Analysis Clustering Danio rerio Developmental stages DNA microarrays Dose-Response Relationship, Drug Embryo, Nonmammalian - drug effects Embryo, Nonmammalian - embryology Embryo, Nonmammalian - metabolism Embryogenesis Embryonic development Embryonic growth stage Embryos Endocrine disruptors Enrichment Environmental protection Estradiol Estradiol - pharmacology Estrogen Receptor alpha - genetics Estrogens Estrogens - pharmacology Fertilization Gene expression Gene Expression Regulation, Developmental - drug effects Gene Ontology Genes Genetic aspects Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism In Situ Hybridization Infertility Kinases Liver Male Microscopy, Fluorescence Oligonucleotide Array Sequence Analysis Pancreas Phenols (Class of compounds) Principal Component Analysis Proteins R&D Research & development Reverse Transcriptase Polymerase Chain Reaction Ribonucleic acid RNA Sex hormones Signaling Studies Target recognition Time Factors Tissue analysis Tissues Toxicology Transcriptome - drug effects Xenoestrogens Zebrafish Zebrafish - embryology Zebrafish - genetics Zebrafish - growth & development Zebrafish Proteins - genetics |
| title | Identification of estrogen target genes during zebrafish embryonic development through transcriptomic analysis |
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