GSE is a maternal factor involved in active DNA demethylation in zygotes
After fertilization, the sperm and oocyte genomes undergo extensive epigenetic reprogramming to form a totipotent zygote. The dynamic epigenetic changes during early embryo development primarily involve DNA methylation and demethylation. We have previously identified Gse (gonad-specific expression g...
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| creator | Hatanaka, Yuki Shimizu, Natsumi Nishikawa, Satoshi Tokoro, Mikiko Shin, Seung-Wook Nishihara, Takuji Amano, Tomoko Anzai, Masayuki Kato, Hiromi Mitani, Tasuku Hosoi, Yoshihiko Kishigami, Satoshi Matsumoto, Kazuya |
| description | After fertilization, the sperm and oocyte genomes undergo extensive epigenetic reprogramming to form a totipotent zygote. The dynamic epigenetic changes during early embryo development primarily involve DNA methylation and demethylation. We have previously identified Gse (gonad-specific expression gene) to be expressed specifically in germ cells and early embryos. Its encoded protein GSE is predominantly localized in the nuclei of cells from the zygote to blastocyst stages, suggesting possible roles in the epigenetic changes occurring during early embryo development. Here, we report the involvement of GSE in epigenetic reprogramming of the paternal genome during mouse zygote development. Preferential binding of GSE to the paternal chromatin was observed from pronuclear stage 2 (PN2) onward. A knockdown of GSE by antisense RNA in oocytes produced no apparent effect on the first and second cell cycles in preimplantation embryos, but caused a significant reduction in the loss of 5-methylcytosine (5mC) and the accumulation of 5-hydroxymethylcytosine (5hmC) in the paternal pronucleus. Furthermore, DNA methylation levels in CpG sites of LINE1 transposable elements, Lemd1, Nanog and the upstream regulatory region of the Oct4 (also known as Pou5f1) gene were clearly increased in GSE-knockdown zygotes at mid-pronuclear stages (PN3-4), but the imprinted H19-differential methylated region was not affected. Importantly, DNA immunoprecipitation of 5mC and 5hmC also indicates that knockdown of GSE in zygotes resulted in a significant reduction of the conversion of 5mC to 5hmC on LINE1. Therefore, our results suggest an important role of maternal GSE for mediating active DNA demethylation in the zygote. |
| doi_str_mv | 10.1371/journal.pone.0060205 |
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The dynamic epigenetic changes during early embryo development primarily involve DNA methylation and demethylation. We have previously identified Gse (gonad-specific expression gene) to be expressed specifically in germ cells and early embryos. Its encoded protein GSE is predominantly localized in the nuclei of cells from the zygote to blastocyst stages, suggesting possible roles in the epigenetic changes occurring during early embryo development. Here, we report the involvement of GSE in epigenetic reprogramming of the paternal genome during mouse zygote development. Preferential binding of GSE to the paternal chromatin was observed from pronuclear stage 2 (PN2) onward. A knockdown of GSE by antisense RNA in oocytes produced no apparent effect on the first and second cell cycles in preimplantation embryos, but caused a significant reduction in the loss of 5-methylcytosine (5mC) and the accumulation of 5-hydroxymethylcytosine (5hmC) in the paternal pronucleus. Furthermore, DNA methylation levels in CpG sites of LINE1 transposable elements, Lemd1, Nanog and the upstream regulatory region of the Oct4 (also known as Pou5f1) gene were clearly increased in GSE-knockdown zygotes at mid-pronuclear stages (PN3-4), but the imprinted H19-differential methylated region was not affected. Importantly, DNA immunoprecipitation of 5mC and 5hmC also indicates that knockdown of GSE in zygotes resulted in a significant reduction of the conversion of 5mC to 5hmC on LINE1. Therefore, our results suggest an important role of maternal GSE for mediating active DNA demethylation in the zygote.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0060205</identifier><identifier>PMID: 23560077</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>5-Methylcytosine - metabolism ; Animals ; Antisense RNA ; Biology ; Blastocyst - cytology ; Blastocyst - metabolism ; Chromatin ; Chromatin - genetics ; Chromatin - metabolism ; CpG islands ; Cytosine - analogs & derivatives ; Cytosine - metabolism ; Demethylation ; Deoxyribonucleic acid ; DNA ; DNA Methylation ; Embryo, Mammalian ; Embryonic Development ; Embryos ; Epigenesis, Genetic ; Epigenetics ; Female ; Fertilization ; Gene expression ; Gene Expression Regulation, Developmental ; Genetic aspects ; Genomes ; Germ cells ; Homeodomain Proteins - genetics ; Homeodomain Proteins - metabolism ; Immunoprecipitation ; In vitro fertilization ; Laboratory animals ; Localization ; Long Interspersed Nucleotide Elements - genetics ; Male ; Mammals ; Methylation ; Mice ; Nanog Homeobox Protein ; Nuclei ; Nuclei (cytology) ; Oct-4 protein ; Octamer Transcription Factor-3 - genetics ; Octamer Transcription Factor-3 - metabolism ; Oocytes ; Pronucleus ; Protein Binding ; Proteins ; Proteins - antagonists & inhibitors ; Proteins - genetics ; Proteins - metabolism ; Reduction ; Ribonucleic acid ; RNA ; RNA, Small Interfering - genetics ; RNA, Small Interfering - metabolism ; Science ; Sex Factors ; Sperm ; University graduates ; Zygote ; Zygote - cytology ; Zygote - metabolism ; Zygotes</subject><ispartof>PloS one, 2013-04, Vol.8 (4), p.e60205-e60205</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 HATANAKA 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 HATANAKA et al 2013 HATANAKA et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-623bb0eaff85d0a782ca57b4b87ccabd77c757c66e831c8fbebe36e95ca4bbb23</citedby><cites>FETCH-LOGICAL-c758t-623bb0eaff85d0a782ca57b4b87ccabd77c757c66e831c8fbebe36e95ca4bbb23</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/PMC3613368/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3613368/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23560077$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Dean, Wendy</contributor><creatorcontrib>Hatanaka, Yuki</creatorcontrib><creatorcontrib>Shimizu, Natsumi</creatorcontrib><creatorcontrib>Nishikawa, Satoshi</creatorcontrib><creatorcontrib>Tokoro, Mikiko</creatorcontrib><creatorcontrib>Shin, Seung-Wook</creatorcontrib><creatorcontrib>Nishihara, Takuji</creatorcontrib><creatorcontrib>Amano, Tomoko</creatorcontrib><creatorcontrib>Anzai, Masayuki</creatorcontrib><creatorcontrib>Kato, Hiromi</creatorcontrib><creatorcontrib>Mitani, Tasuku</creatorcontrib><creatorcontrib>Hosoi, Yoshihiko</creatorcontrib><creatorcontrib>Kishigami, Satoshi</creatorcontrib><creatorcontrib>Matsumoto, Kazuya</creatorcontrib><title>GSE is a maternal factor involved in active DNA demethylation in zygotes</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>After fertilization, the sperm and oocyte genomes undergo extensive epigenetic reprogramming to form a totipotent zygote. The dynamic epigenetic changes during early embryo development primarily involve DNA methylation and demethylation. We have previously identified Gse (gonad-specific expression gene) to be expressed specifically in germ cells and early embryos. Its encoded protein GSE is predominantly localized in the nuclei of cells from the zygote to blastocyst stages, suggesting possible roles in the epigenetic changes occurring during early embryo development. Here, we report the involvement of GSE in epigenetic reprogramming of the paternal genome during mouse zygote development. Preferential binding of GSE to the paternal chromatin was observed from pronuclear stage 2 (PN2) onward. A knockdown of GSE by antisense RNA in oocytes produced no apparent effect on the first and second cell cycles in preimplantation embryos, but caused a significant reduction in the loss of 5-methylcytosine (5mC) and the accumulation of 5-hydroxymethylcytosine (5hmC) in the paternal pronucleus. Furthermore, DNA methylation levels in CpG sites of LINE1 transposable elements, Lemd1, Nanog and the upstream regulatory region of the Oct4 (also known as Pou5f1) gene were clearly increased in GSE-knockdown zygotes at mid-pronuclear stages (PN3-4), but the imprinted H19-differential methylated region was not affected. Importantly, DNA immunoprecipitation of 5mC and 5hmC also indicates that knockdown of GSE in zygotes resulted in a significant reduction of the conversion of 5mC to 5hmC on LINE1. Therefore, our results suggest an important role of maternal GSE for mediating active DNA demethylation in the zygote.</description><subject>5-Methylcytosine - metabolism</subject><subject>Animals</subject><subject>Antisense RNA</subject><subject>Biology</subject><subject>Blastocyst - cytology</subject><subject>Blastocyst - metabolism</subject><subject>Chromatin</subject><subject>Chromatin - genetics</subject><subject>Chromatin - metabolism</subject><subject>CpG islands</subject><subject>Cytosine - analogs & derivatives</subject><subject>Cytosine - metabolism</subject><subject>Demethylation</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA Methylation</subject><subject>Embryo, Mammalian</subject><subject>Embryonic Development</subject><subject>Embryos</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetics</subject><subject>Female</subject><subject>Fertilization</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Germ cells</subject><subject>Homeodomain Proteins - genetics</subject><subject>Homeodomain Proteins - metabolism</subject><subject>Immunoprecipitation</subject><subject>In vitro fertilization</subject><subject>Laboratory animals</subject><subject>Localization</subject><subject>Long Interspersed Nucleotide Elements - genetics</subject><subject>Male</subject><subject>Mammals</subject><subject>Methylation</subject><subject>Mice</subject><subject>Nanog Homeobox Protein</subject><subject>Nuclei</subject><subject>Nuclei (cytology)</subject><subject>Oct-4 protein</subject><subject>Octamer Transcription Factor-3 - genetics</subject><subject>Octamer Transcription Factor-3 - metabolism</subject><subject>Oocytes</subject><subject>Pronucleus</subject><subject>Protein Binding</subject><subject>Proteins</subject><subject>Proteins - antagonists & inhibitors</subject><subject>Proteins - genetics</subject><subject>Proteins - metabolism</subject><subject>Reduction</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Small Interfering - genetics</subject><subject>RNA, Small Interfering - metabolism</subject><subject>Science</subject><subject>Sex Factors</subject><subject>Sperm</subject><subject>University graduates</subject><subject>Zygote</subject><subject>Zygote - cytology</subject><subject>Zygote - metabolism</subject><subject>Zygotes</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>eNqNkl1v0zAUhiMEYmPwDxBEQkJw0WLH8UdukKoxtkoTkxhwa9nOSeoqjUvsVJRfj0OzqUG7QL6wdfyc9xwfv0nyEqM5Jhx_WLu-a1Uz37oW5ggxlCH6KDnFBclmLEPk8dH5JHnm_RohSgRjT5OTjFCGEOenydXl7UVqfarSjQowCKaVMsF1qW13rtlBGQ9pjNgdpJ--LNISNhBW-0YF69rh7ve-dgH88-RJpRoPL8b9LPn--eLb-dXs-uZyeb64nhlORYjdEK0RqKoStESKi8woynWuBTdG6ZLzyHHDGAiCjag0aCAMCmpUrrXOyFny-qC7bZyX4xC8xISgAueI5JFYHojSqbXcdnajur10ysq_AdfVUnXBmgakKLDBFAtakCIHYwRTuNCiKDEuKa541Po4Vuv1BkoDbehUMxGd3rR2JWu3k4TFjpiIAu9Ggc797MEHubHeQNOoFlw_9J3lpEAZIxF98w_68OtGqlbxAbatXKxrBlG5yLnIKaM5jtT8ASqu-H3WRMdUNsYnCe8nCZEJ8CvUqvdeLm-__j9782PKvj1iV6CasPKu6Qf3-CmYH0DTOe87qO6HjJEcDH83DTkYXo6Gj2mvjj_oPunO4eQPMef6BA</recordid><startdate>20130401</startdate><enddate>20130401</enddate><creator>Hatanaka, Yuki</creator><creator>Shimizu, Natsumi</creator><creator>Nishikawa, Satoshi</creator><creator>Tokoro, Mikiko</creator><creator>Shin, Seung-Wook</creator><creator>Nishihara, Takuji</creator><creator>Amano, Tomoko</creator><creator>Anzai, Masayuki</creator><creator>Kato, Hiromi</creator><creator>Mitani, Tasuku</creator><creator>Hosoi, Yoshihiko</creator><creator>Kishigami, Satoshi</creator><creator>Matsumoto, Kazuya</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>20130401</creationdate><title>GSE is a maternal factor involved in active DNA demethylation in zygotes</title><author>Hatanaka, Yuki ; Shimizu, Natsumi ; Nishikawa, Satoshi ; Tokoro, Mikiko ; Shin, Seung-Wook ; Nishihara, Takuji ; Amano, Tomoko ; Anzai, Masayuki ; Kato, Hiromi ; Mitani, Tasuku ; Hosoi, Yoshihiko ; Kishigami, Satoshi ; Matsumoto, Kazuya</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-623bb0eaff85d0a782ca57b4b87ccabd77c757c66e831c8fbebe36e95ca4bbb23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>5-Methylcytosine - 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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>Access via ProQuest (Open Access)</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>MEDLINE - 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>Hatanaka, Yuki</au><au>Shimizu, Natsumi</au><au>Nishikawa, Satoshi</au><au>Tokoro, Mikiko</au><au>Shin, Seung-Wook</au><au>Nishihara, Takuji</au><au>Amano, Tomoko</au><au>Anzai, Masayuki</au><au>Kato, Hiromi</au><au>Mitani, Tasuku</au><au>Hosoi, Yoshihiko</au><au>Kishigami, Satoshi</au><au>Matsumoto, Kazuya</au><au>Dean, Wendy</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>GSE is a maternal factor involved in active DNA demethylation in zygotes</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-04-01</date><risdate>2013</risdate><volume>8</volume><issue>4</issue><spage>e60205</spage><epage>e60205</epage><pages>e60205-e60205</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>After fertilization, the sperm and oocyte genomes undergo extensive epigenetic reprogramming to form a totipotent zygote. The dynamic epigenetic changes during early embryo development primarily involve DNA methylation and demethylation. We have previously identified Gse (gonad-specific expression gene) to be expressed specifically in germ cells and early embryos. Its encoded protein GSE is predominantly localized in the nuclei of cells from the zygote to blastocyst stages, suggesting possible roles in the epigenetic changes occurring during early embryo development. Here, we report the involvement of GSE in epigenetic reprogramming of the paternal genome during mouse zygote development. Preferential binding of GSE to the paternal chromatin was observed from pronuclear stage 2 (PN2) onward. A knockdown of GSE by antisense RNA in oocytes produced no apparent effect on the first and second cell cycles in preimplantation embryos, but caused a significant reduction in the loss of 5-methylcytosine (5mC) and the accumulation of 5-hydroxymethylcytosine (5hmC) in the paternal pronucleus. Furthermore, DNA methylation levels in CpG sites of LINE1 transposable elements, Lemd1, Nanog and the upstream regulatory region of the Oct4 (also known as Pou5f1) gene were clearly increased in GSE-knockdown zygotes at mid-pronuclear stages (PN3-4), but the imprinted H19-differential methylated region was not affected. Importantly, DNA immunoprecipitation of 5mC and 5hmC also indicates that knockdown of GSE in zygotes resulted in a significant reduction of the conversion of 5mC to 5hmC on LINE1. Therefore, our results suggest an important role of maternal GSE for mediating active DNA demethylation in the zygote.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23560077</pmid><doi>10.1371/journal.pone.0060205</doi><tpages>e60205</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-04, Vol.8 (4), p.e60205-e60205 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1330914034 |
| source | PubMed Central Free; MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; Free Full-Text Journals in Chemistry |
| subjects | 5-Methylcytosine - metabolism Animals Antisense RNA Biology Blastocyst - cytology Blastocyst - metabolism Chromatin Chromatin - genetics Chromatin - metabolism CpG islands Cytosine - analogs & derivatives Cytosine - metabolism Demethylation Deoxyribonucleic acid DNA DNA Methylation Embryo, Mammalian Embryonic Development Embryos Epigenesis, Genetic Epigenetics Female Fertilization Gene expression Gene Expression Regulation, Developmental Genetic aspects Genomes Germ cells Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Immunoprecipitation In vitro fertilization Laboratory animals Localization Long Interspersed Nucleotide Elements - genetics Male Mammals Methylation Mice Nanog Homeobox Protein Nuclei Nuclei (cytology) Oct-4 protein Octamer Transcription Factor-3 - genetics Octamer Transcription Factor-3 - metabolism Oocytes Pronucleus Protein Binding Proteins Proteins - antagonists & inhibitors Proteins - genetics Proteins - metabolism Reduction Ribonucleic acid RNA RNA, Small Interfering - genetics RNA, Small Interfering - metabolism Science Sex Factors Sperm University graduates Zygote Zygote - cytology Zygote - metabolism Zygotes |
| title | GSE is a maternal factor involved in active DNA demethylation in zygotes |
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