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Genome-wide DNA methylation analysis reveals phytoestrogen modification of promoter methylation patterns during embryonic stem cell differentiation
Environmental challenges during development affect the fetal epigenome, but the period(s) vulnerable to epigenetic dysregulation is(are) not clear. By employing a soy phytoestrogen, genistein, that is known to alter the epigenetic states of the A(vy) allele during embryogenesis, we have explored the...
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Published in: | PloS one 2011-04, Vol.6 (4), p.e19278-e19278 |
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description | Environmental challenges during development affect the fetal epigenome, but the period(s) vulnerable to epigenetic dysregulation is(are) not clear. By employing a soy phytoestrogen, genistein, that is known to alter the epigenetic states of the A(vy) allele during embryogenesis, we have explored the sensitive period for epigenetic regulation. The post-implantation period, when de novo DNA methylation actively proceeds, is amenable to in vitro analysis using a mouse embryonic stem (ES) cell differentiation system.
Mouse ES cells were differentiated in the presence or absence of genistein, and DNA methylation patterns on day 10 were compared by microarray-based promoter methylation analysis coupled with a methylation-sensitive endonuclease (HpaII/McrBC)-dependent enrichment procedure. Moderate changes in methylation levels were observed in a subset of promoters following genistein treatment. Detailed investigation of the Ucp1 and Sytl1 promoters further revealed that genistein does not affect de novo methylation occurring between day 0 and day 4, but interferes with subsequent regulatory processes and leads to a decrease in methylation level for both promoters.
Genistein perturbed the methylation pattern of differentiated ES cells after de novo methylation. Our observations suggest that, for a subset of genes, regulation after de novo DNA methylation in the early embryo may be sensitive to genistein. |
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Mouse ES cells were differentiated in the presence or absence of genistein, and DNA methylation patterns on day 10 were compared by microarray-based promoter methylation analysis coupled with a methylation-sensitive endonuclease (HpaII/McrBC)-dependent enrichment procedure. Moderate changes in methylation levels were observed in a subset of promoters following genistein treatment. Detailed investigation of the Ucp1 and Sytl1 promoters further revealed that genistein does not affect de novo methylation occurring between day 0 and day 4, but interferes with subsequent regulatory processes and leads to a decrease in methylation level for both promoters.
Genistein perturbed the methylation pattern of differentiated ES cells after de novo methylation. Our observations suggest that, for a subset of genes, regulation after de novo DNA methylation in the early embryo may be sensitive to genistein.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0019278</identifier><identifier>PMID: 21559447</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adipocytes ; Analysis ; Animals ; Biology ; Biosynthesis ; Bisphenol A ; Cell differentiation ; Cell Differentiation - drug effects ; Chemistry ; CpG Islands ; Critical period ; Deoxyribonucleic acid ; Differentiation (biology) ; DNA ; DNA - genetics ; DNA Methylation ; DNA microarrays ; Embryogenesis ; Embryonic growth stage ; Embryonic stem cells ; Embryonic Stem Cells - cytology ; Endonuclease ; Environment ; Epidemiology ; Epigenesis, Genetic ; Epigenetic inheritance ; Epigenetics ; Fetuses ; Gene expression ; Gene regulation ; Genes ; Genetic testing ; Genistein ; Genistein - pharmacology ; Genome ; Genomes ; Genomics ; Geriatrics ; Glycine max ; Implantation ; Isoflavones ; Leukemia ; Medical research ; Medicine ; Methylation ; Mice ; Mice, Inbred C57BL ; Mitochondrial DNA ; Phytoestrogens - metabolism ; Promoter Regions, Genetic ; Proteins ; Reverse Transcriptase Polymerase Chain Reaction ; Science ; Stem cells</subject><ispartof>PloS one, 2011-04, Vol.6 (4), p.e19278-e19278</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Sato 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>Sato et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c691t-8064b1a1e2ee9f2cabf7dc9d79ae1a9f130d35b6cee232ff70f61c7612898cd93</citedby><cites>FETCH-LOGICAL-c691t-8064b1a1e2ee9f2cabf7dc9d79ae1a9f130d35b6cee232ff70f61c7612898cd93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1296874755/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1296874755?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21559447$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Cooney, Austin John</contributor><creatorcontrib>Sato, Noriko</creatorcontrib><creatorcontrib>Yamakawa, Naomi</creatorcontrib><creatorcontrib>Masuda, Moe</creatorcontrib><creatorcontrib>Sudo, Katsuko</creatorcontrib><creatorcontrib>Hatada, Izuho</creatorcontrib><creatorcontrib>Muramatsu, Masaaki</creatorcontrib><title>Genome-wide DNA methylation analysis reveals phytoestrogen modification of promoter methylation patterns during embryonic stem cell differentiation</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Environmental challenges during development affect the fetal epigenome, but the period(s) vulnerable to epigenetic dysregulation is(are) not clear. By employing a soy phytoestrogen, genistein, that is known to alter the epigenetic states of the A(vy) allele during embryogenesis, we have explored the sensitive period for epigenetic regulation. The post-implantation period, when de novo DNA methylation actively proceeds, is amenable to in vitro analysis using a mouse embryonic stem (ES) cell differentiation system.
Mouse ES cells were differentiated in the presence or absence of genistein, and DNA methylation patterns on day 10 were compared by microarray-based promoter methylation analysis coupled with a methylation-sensitive endonuclease (HpaII/McrBC)-dependent enrichment procedure. Moderate changes in methylation levels were observed in a subset of promoters following genistein treatment. Detailed investigation of the Ucp1 and Sytl1 promoters further revealed that genistein does not affect de novo methylation occurring between day 0 and day 4, but interferes with subsequent regulatory processes and leads to a decrease in methylation level for both promoters.
Genistein perturbed the methylation pattern of differentiated ES cells after de novo methylation. 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pharmacology</subject><subject>Genome</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Geriatrics</subject><subject>Glycine max</subject><subject>Implantation</subject><subject>Isoflavones</subject><subject>Leukemia</subject><subject>Medical research</subject><subject>Medicine</subject><subject>Methylation</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mitochondrial DNA</subject><subject>Phytoestrogens - metabolism</subject><subject>Promoter Regions, Genetic</subject><subject>Proteins</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Science</subject><subject>Stem cells</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk8tu1DAUhiMEomXgDRBEQgKxmMF2EjveII0KlJEqKnHbWo59POMqiae2U5jn4IXxXFpNUBcoi0Qn3_8f-1yy7DlGM1ww_O7KDb6X7WztepghhDlh9YPsFPOCTClBxcOj75PsSQhXCFVFTenj7ITgquJlyU6zP-fQuw6mv6yG_MOXed5BXG1aGa3rc5n8N8GG3MMNyDbk69UmOgjRuyX0eee0NVbtWWfytXedi-BHHmsZU6gPuR687Zc5dI3fuN6qPETocgVtmycbAx76aHeap9kjk7LBs8N7kv349PH72efpxeX54mx-MVWU4zitES0bLDEQAG6Iko1hWnHNuAQsucEF0kXVUAVACmIMQ4ZixSgmNa-V5sUke7n3XbcuiEM9g8CE05qVrKoSsdgT2skrsfa2k34jnLRiF3B-KaSPVrUgdCEbrBvNaMVKQw1nSta4qAiirIF0mEn2_pBtaDrQKl3Xy3ZkOv7T25VYuhtRoLqsEUsGbw4G3l0PqQuis2FbP9mDG4JIrSVVGo06ka_-Ie-_3IFaynR-2xuX0qqtp5iXjNacVDtqdg-VHg2dVWn2jE3xkeDtSJCYCL_jUg4hiMW3r__PXv4cs6-P2FWax7gKrh22ExPGYLkHlXcheDB3NcZIbFfnthpiuzrisDpJ9uK4P3ei210p_gJSFxk6</recordid><startdate>20110429</startdate><enddate>20110429</enddate><creator>Sato, Noriko</creator><creator>Yamakawa, Naomi</creator><creator>Masuda, Moe</creator><creator>Sudo, Katsuko</creator><creator>Hatada, Izuho</creator><creator>Muramatsu, Masaaki</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>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20110429</creationdate><title>Genome-wide DNA methylation analysis reveals phytoestrogen modification of promoter methylation patterns during embryonic stem cell differentiation</title><author>Sato, Noriko ; Yamakawa, Naomi ; Masuda, Moe ; Sudo, Katsuko ; Hatada, Izuho ; Muramatsu, Masaaki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c691t-8064b1a1e2ee9f2cabf7dc9d79ae1a9f130d35b6cee232ff70f61c7612898cd93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Adipocytes</topic><topic>Analysis</topic><topic>Animals</topic><topic>Biology</topic><topic>Biosynthesis</topic><topic>Bisphenol A</topic><topic>Cell differentiation</topic><topic>Cell Differentiation - drug effects</topic><topic>Chemistry</topic><topic>CpG Islands</topic><topic>Critical period</topic><topic>Deoxyribonucleic acid</topic><topic>Differentiation (biology)</topic><topic>DNA</topic><topic>DNA - genetics</topic><topic>DNA Methylation</topic><topic>DNA microarrays</topic><topic>Embryogenesis</topic><topic>Embryonic growth stage</topic><topic>Embryonic stem cells</topic><topic>Embryonic Stem Cells - cytology</topic><topic>Endonuclease</topic><topic>Environment</topic><topic>Epidemiology</topic><topic>Epigenesis, Genetic</topic><topic>Epigenetic inheritance</topic><topic>Epigenetics</topic><topic>Fetuses</topic><topic>Gene expression</topic><topic>Gene regulation</topic><topic>Genes</topic><topic>Genetic testing</topic><topic>Genistein</topic><topic>Genistein - pharmacology</topic><topic>Genome</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Geriatrics</topic><topic>Glycine max</topic><topic>Implantation</topic><topic>Isoflavones</topic><topic>Leukemia</topic><topic>Medical research</topic><topic>Medicine</topic><topic>Methylation</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mitochondrial DNA</topic><topic>Phytoestrogens - 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By employing a soy phytoestrogen, genistein, that is known to alter the epigenetic states of the A(vy) allele during embryogenesis, we have explored the sensitive period for epigenetic regulation. The post-implantation period, when de novo DNA methylation actively proceeds, is amenable to in vitro analysis using a mouse embryonic stem (ES) cell differentiation system.
Mouse ES cells were differentiated in the presence or absence of genistein, and DNA methylation patterns on day 10 were compared by microarray-based promoter methylation analysis coupled with a methylation-sensitive endonuclease (HpaII/McrBC)-dependent enrichment procedure. Moderate changes in methylation levels were observed in a subset of promoters following genistein treatment. Detailed investigation of the Ucp1 and Sytl1 promoters further revealed that genistein does not affect de novo methylation occurring between day 0 and day 4, but interferes with subsequent regulatory processes and leads to a decrease in methylation level for both promoters.
Genistein perturbed the methylation pattern of differentiated ES cells after de novo methylation. Our observations suggest that, for a subset of genes, regulation after de novo DNA methylation in the early embryo may be sensitive to genistein.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21559447</pmid><doi>10.1371/journal.pone.0019278</doi><tpages>e19278</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adipocytes Analysis Animals Biology Biosynthesis Bisphenol A Cell differentiation Cell Differentiation - drug effects Chemistry CpG Islands Critical period Deoxyribonucleic acid Differentiation (biology) DNA DNA - genetics DNA Methylation DNA microarrays Embryogenesis Embryonic growth stage Embryonic stem cells Embryonic Stem Cells - cytology Endonuclease Environment Epidemiology Epigenesis, Genetic Epigenetic inheritance Epigenetics Fetuses Gene expression Gene regulation Genes Genetic testing Genistein Genistein - pharmacology Genome Genomes Genomics Geriatrics Glycine max Implantation Isoflavones Leukemia Medical research Medicine Methylation Mice Mice, Inbred C57BL Mitochondrial DNA Phytoestrogens - metabolism Promoter Regions, Genetic Proteins Reverse Transcriptase Polymerase Chain Reaction Science Stem cells |
title | Genome-wide DNA methylation analysis reveals phytoestrogen modification of promoter methylation patterns during embryonic stem cell differentiation |
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