Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas
Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside...
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description | Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside vertebrates and ecdysozoan models. However, the development of the Pacific oyster
is under the strong epigenetic influence of DNA methylation, and
histone-demethylase orthologues are highly expressed during
.
early life. This suggests a physiological relevance of histone methylation regulation in oyster development, raising the question of functional conservation of this epigenetic pathway in lophotrochozoan. Quantification of histone methylation using fluorescent ELISAs during oyster early life indicated significant variations in monomethyl histone H3 lysine 4 (H3K4me), an overall decrease in H3K9 mono- and tri-methylations, and in H3K36 methylations, respectively, whereas no significant modification could be detected in H3K27 methylation. Early in vivo treatment with the JmjC-specific inhibitor Methylstat induced hypermethylation of all the examined histone H3 lysines and developmental alterations as revealed by scanning electronic microscopy. Using microarrays, we identified 376 genes that were differentially expressed under methylstat treatment, which expression patterns could discriminate between samples as indicated by principal component analysis. Furthermore, Gene Ontology revealed that these genes were related to processes potentially important for embryonic stages such as binding, cell differentiation and development. These results suggest an important physiological significance of histone methylation in the oyster embryonic and larval life, providing, to our knowledge, the first insights into epigenetic regulation by histone methylation in lophotrochozoan development. |
doi_str_mv | 10.3390/genes10090695 |
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is under the strong epigenetic influence of DNA methylation, and
histone-demethylase orthologues are highly expressed during
.
early life. This suggests a physiological relevance of histone methylation regulation in oyster development, raising the question of functional conservation of this epigenetic pathway in lophotrochozoan. Quantification of histone methylation using fluorescent ELISAs during oyster early life indicated significant variations in monomethyl histone H3 lysine 4 (H3K4me), an overall decrease in H3K9 mono- and tri-methylations, and in H3K36 methylations, respectively, whereas no significant modification could be detected in H3K27 methylation. Early in vivo treatment with the JmjC-specific inhibitor Methylstat induced hypermethylation of all the examined histone H3 lysines and developmental alterations as revealed by scanning electronic microscopy. Using microarrays, we identified 376 genes that were differentially expressed under methylstat treatment, which expression patterns could discriminate between samples as indicated by principal component analysis. Furthermore, Gene Ontology revealed that these genes were related to processes potentially important for embryonic stages such as binding, cell differentiation and development. These results suggest an important physiological significance of histone methylation in the oyster embryonic and larval life, providing, to our knowledge, the first insights into epigenetic regulation by histone methylation in lophotrochozoan development.</description><identifier>ISSN: 2073-4425</identifier><identifier>EISSN: 2073-4425</identifier><identifier>DOI: 10.3390/genes10090695</identifier><identifier>PMID: 31509985</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Animals ; Cell cycle ; Cell differentiation ; chromatin ; Chromatin remodeling ; Crassostrea - genetics ; Crassostrea - growth & development ; Crassostrea gigas ; DNA methylation ; DNA microarrays ; early development ; Embryo, Nonmammalian - metabolism ; Embryo, Nonmammalian - ultrastructure ; Embryogenesis ; Embryos ; enzyme-linked immunosorbent assay ; Enzymes ; Epigenesis, Genetic ; Epigenetics ; fluorescence ; Gene expression ; gene expression regulation ; Gene Expression Regulation, Developmental ; gene ontology ; genes ; Histone Code ; histone demethylases ; Histone H3 ; Histones ; Histones - genetics ; Histones - metabolism ; larvae ; Life Sciences ; Lysine ; mammals ; Methylation ; microarray technology ; oysters ; Physiology ; Pluripotency ; principal component analysis ; Protein Processing, Post-Translational ; Proteins ; Scanning electron microscopy ; Stem cells ; Sucrose ; Transcription ; transcription (genetics)</subject><ispartof>Genes, 2019-09, Vol.10 (9), p.695</ispartof><rights>2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Attribution</rights><rights>2019 by the authors. 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c618t-6d73bdc6891798119f183e158290921ba9c7e44493c19de84de986b2b19117133</citedby><cites>FETCH-LOGICAL-c618t-6d73bdc6891798119f183e158290921ba9c7e44493c19de84de986b2b19117133</cites><orcidid>0000-0001-8372-8715 ; 0000-0002-4051-4415</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/PMC6771004/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6771004/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31509985$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04571004$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Fellous, Alexandre</creatorcontrib><creatorcontrib>Lefranc, Lorane</creatorcontrib><creatorcontrib>Jouaux, Aude</creatorcontrib><creatorcontrib>Goux, Didier</creatorcontrib><creatorcontrib>Favrel, Pascal</creatorcontrib><creatorcontrib>Rivière, Guillaume</creatorcontrib><title>Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas</title><title>Genes</title><addtitle>Genes (Basel)</addtitle><description>Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside vertebrates and ecdysozoan models. However, the development of the Pacific oyster
is under the strong epigenetic influence of DNA methylation, and
histone-demethylase orthologues are highly expressed during
.
early life. This suggests a physiological relevance of histone methylation regulation in oyster development, raising the question of functional conservation of this epigenetic pathway in lophotrochozoan. Quantification of histone methylation using fluorescent ELISAs during oyster early life indicated significant variations in monomethyl histone H3 lysine 4 (H3K4me), an overall decrease in H3K9 mono- and tri-methylations, and in H3K36 methylations, respectively, whereas no significant modification could be detected in H3K27 methylation. Early in vivo treatment with the JmjC-specific inhibitor Methylstat induced hypermethylation of all the examined histone H3 lysines and developmental alterations as revealed by scanning electronic microscopy. Using microarrays, we identified 376 genes that were differentially expressed under methylstat treatment, which expression patterns could discriminate between samples as indicated by principal component analysis. Furthermore, Gene Ontology revealed that these genes were related to processes potentially important for embryonic stages such as binding, cell differentiation and development. These results suggest an important physiological significance of histone methylation in the oyster embryonic and larval life, providing, to our knowledge, the first insights into epigenetic regulation by histone methylation in lophotrochozoan development.</description><subject>Animals</subject><subject>Cell cycle</subject><subject>Cell differentiation</subject><subject>chromatin</subject><subject>Chromatin remodeling</subject><subject>Crassostrea - genetics</subject><subject>Crassostrea - growth & development</subject><subject>Crassostrea gigas</subject><subject>DNA methylation</subject><subject>DNA microarrays</subject><subject>early development</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Embryo, Nonmammalian - ultrastructure</subject><subject>Embryogenesis</subject><subject>Embryos</subject><subject>enzyme-linked immunosorbent assay</subject><subject>Enzymes</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetics</subject><subject>fluorescence</subject><subject>Gene expression</subject><subject>gene expression regulation</subject><subject>Gene Expression Regulation, Developmental</subject><subject>gene ontology</subject><subject>genes</subject><subject>Histone Code</subject><subject>histone demethylases</subject><subject>Histone H3</subject><subject>Histones</subject><subject>Histones - genetics</subject><subject>Histones - metabolism</subject><subject>larvae</subject><subject>Life Sciences</subject><subject>Lysine</subject><subject>mammals</subject><subject>Methylation</subject><subject>microarray technology</subject><subject>oysters</subject><subject>Physiology</subject><subject>Pluripotency</subject><subject>principal component analysis</subject><subject>Protein Processing, Post-Translational</subject><subject>Proteins</subject><subject>Scanning electron microscopy</subject><subject>Stem cells</subject><subject>Sucrose</subject><subject>Transcription</subject><subject>transcription (genetics)</subject><issn>2073-4425</issn><issn>2073-4425</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNqFkrFv3CAUxq2qVROlGbtWSF3awSkYjGGpFF2TXKWrkqGdEcbPPiIfuIBPua1_erlcGiVZygLi-_G9p49XFO8JPqNU4i8DOIgEY4m5rF8VxxVuaMlYVb9-cj4qTmO8xXkxXGFcvy2OKKmxlKI-Lv4sbUzeAfoBab0bdbLeoRsdkjV20gkisg5d5TLo4m4KEONeX3iXgh9RNwfrBpTWWdVh3KFvsIXRTxtwCfn-XrjRxvbWoOtdTBDQIugYfUwBNBrsoOO74k2vxwinD_tJ8evy4udiWa6ur74vzlel4USkkncNbTvDhSSNFITInggKpBaVxLIirZamAcaYpIbIDgTrQAreVi2RhDSE0pPi68F3mtsNdCa3GPSopmA3OuyU11Y9V5xdq8FvFW-anDDLBp8PBusXz5bnK7W_w6y-J7cks58eigX_e4aY1MZGA-OoHfg5qoqx_GOcYfF_tBIy-4pGZvTjC_TWz8Hl1FRVM1ETxgXPVHmgTPAxBugfmyVY7adGPZuazH94Gswj_W9G6F9lTb2w</recordid><startdate>20190910</startdate><enddate>20190910</enddate><creator>Fellous, Alexandre</creator><creator>Lefranc, Lorane</creator><creator>Jouaux, Aude</creator><creator>Goux, Didier</creator><creator>Favrel, Pascal</creator><creator>Rivière, Guillaume</creator><general>MDPI AG</general><general>MDPI</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>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8372-8715</orcidid><orcidid>https://orcid.org/0000-0002-4051-4415</orcidid></search><sort><creationdate>20190910</creationdate><title>Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas</title><author>Fellous, Alexandre ; Lefranc, Lorane ; Jouaux, Aude ; Goux, Didier ; Favrel, Pascal ; Rivière, Guillaume</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c618t-6d73bdc6891798119f183e158290921ba9c7e44493c19de84de986b2b19117133</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Cell cycle</topic><topic>Cell differentiation</topic><topic>chromatin</topic><topic>Chromatin remodeling</topic><topic>Crassostrea - genetics</topic><topic>Crassostrea - growth & development</topic><topic>Crassostrea gigas</topic><topic>DNA methylation</topic><topic>DNA microarrays</topic><topic>early development</topic><topic>Embryo, Nonmammalian - metabolism</topic><topic>Embryo, Nonmammalian - ultrastructure</topic><topic>Embryogenesis</topic><topic>Embryos</topic><topic>enzyme-linked immunosorbent assay</topic><topic>Enzymes</topic><topic>Epigenesis, Genetic</topic><topic>Epigenetics</topic><topic>fluorescence</topic><topic>Gene expression</topic><topic>gene expression regulation</topic><topic>Gene Expression Regulation, Developmental</topic><topic>gene ontology</topic><topic>genes</topic><topic>Histone Code</topic><topic>histone demethylases</topic><topic>Histone H3</topic><topic>Histones</topic><topic>Histones - genetics</topic><topic>Histones - metabolism</topic><topic>larvae</topic><topic>Life Sciences</topic><topic>Lysine</topic><topic>mammals</topic><topic>Methylation</topic><topic>microarray technology</topic><topic>oysters</topic><topic>Physiology</topic><topic>Pluripotency</topic><topic>principal component analysis</topic><topic>Protein Processing, Post-Translational</topic><topic>Proteins</topic><topic>Scanning electron microscopy</topic><topic>Stem cells</topic><topic>Sucrose</topic><topic>Transcription</topic><topic>transcription (genetics)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fellous, Alexandre</creatorcontrib><creatorcontrib>Lefranc, Lorane</creatorcontrib><creatorcontrib>Jouaux, Aude</creatorcontrib><creatorcontrib>Goux, Didier</creatorcontrib><creatorcontrib>Favrel, Pascal</creatorcontrib><creatorcontrib>Rivière, Guillaume</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</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>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genes</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fellous, Alexandre</au><au>Lefranc, Lorane</au><au>Jouaux, Aude</au><au>Goux, Didier</au><au>Favrel, Pascal</au><au>Rivière, Guillaume</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas</atitle><jtitle>Genes</jtitle><addtitle>Genes (Basel)</addtitle><date>2019-09-10</date><risdate>2019</risdate><volume>10</volume><issue>9</issue><spage>695</spage><pages>695-</pages><issn>2073-4425</issn><eissn>2073-4425</eissn><abstract>Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside vertebrates and ecdysozoan models. However, the development of the Pacific oyster
is under the strong epigenetic influence of DNA methylation, and
histone-demethylase orthologues are highly expressed during
.
early life. This suggests a physiological relevance of histone methylation regulation in oyster development, raising the question of functional conservation of this epigenetic pathway in lophotrochozoan. Quantification of histone methylation using fluorescent ELISAs during oyster early life indicated significant variations in monomethyl histone H3 lysine 4 (H3K4me), an overall decrease in H3K9 mono- and tri-methylations, and in H3K36 methylations, respectively, whereas no significant modification could be detected in H3K27 methylation. Early in vivo treatment with the JmjC-specific inhibitor Methylstat induced hypermethylation of all the examined histone H3 lysines and developmental alterations as revealed by scanning electronic microscopy. Using microarrays, we identified 376 genes that were differentially expressed under methylstat treatment, which expression patterns could discriminate between samples as indicated by principal component analysis. Furthermore, Gene Ontology revealed that these genes were related to processes potentially important for embryonic stages such as binding, cell differentiation and development. These results suggest an important physiological significance of histone methylation in the oyster embryonic and larval life, providing, to our knowledge, the first insights into epigenetic regulation by histone methylation in lophotrochozoan development.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>31509985</pmid><doi>10.3390/genes10090695</doi><orcidid>https://orcid.org/0000-0001-8372-8715</orcidid><orcidid>https://orcid.org/0000-0002-4051-4415</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Cell cycle Cell differentiation chromatin Chromatin remodeling Crassostrea - genetics Crassostrea - growth & development Crassostrea gigas DNA methylation DNA microarrays early development Embryo, Nonmammalian - metabolism Embryo, Nonmammalian - ultrastructure Embryogenesis Embryos enzyme-linked immunosorbent assay Enzymes Epigenesis, Genetic Epigenetics fluorescence Gene expression gene expression regulation Gene Expression Regulation, Developmental gene ontology genes Histone Code histone demethylases Histone H3 Histones Histones - genetics Histones - metabolism larvae Life Sciences Lysine mammals Methylation microarray technology oysters Physiology Pluripotency principal component analysis Protein Processing, Post-Translational Proteins Scanning electron microscopy Stem cells Sucrose Transcription transcription (genetics) |
title | Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas |
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