Stage-specific histone modification profiles reveal global transitions in the Xenopus embryonic epigenome
Vertebrate embryos are derived from a transitory pool of pluripotent cells. By the process of embryonic induction, these precursor cells are assigned to specific fates and differentiation programs. Histone post-translational modifications are thought to play a key role in the establishment and maint...
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| creator | Schneider, Tobias D Arteaga-Salas, Jose M Mentele, Edith David, Robert Nicetto, Dario Imhof, Axel Rupp, Ralph A W |
| description | Vertebrate embryos are derived from a transitory pool of pluripotent cells. By the process of embryonic induction, these precursor cells are assigned to specific fates and differentiation programs. Histone post-translational modifications are thought to play a key role in the establishment and maintenance of stable gene expression patterns underlying these processes. While on gene level histone modifications are known to change during differentiation, very little is known about the quantitative fluctuations in bulk histone modifications during development. To investigate this issue we analysed histones isolated from four different developmental stages of Xenopus laevis by mass spectrometry. In toto, we quantified 59 modification states on core histones H3 and H4 from blastula to tadpole stages. During this developmental period, we observed in general an increase in the unmodified states, and a shift from histone modifications associated with transcriptional activity to transcriptionally repressive histone marks. We also compared these naturally occurring patterns with the histone modifications of murine ES cells, detecting large differences in the methylation patterns of histone H3 lysines 27 and 36 between pluripotent ES cells and pluripotent cells from Xenopus blastulae. By combining all detected modification transitions we could cluster their patterns according to their embryonic origin, defining specific histone modification profiles (HMPs) for each developmental stage. To our knowledge, this data set represents the first compendium of covalent histone modifications and their quantitative flux during normogenesis in a vertebrate model organism. The HMPs indicate a stepwise maturation of the embryonic epigenome, which may be causal to the progressing restriction of cellular potency during development. |
| doi_str_mv | 10.1371/journal.pone.0022548 |
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By the process of embryonic induction, these precursor cells are assigned to specific fates and differentiation programs. Histone post-translational modifications are thought to play a key role in the establishment and maintenance of stable gene expression patterns underlying these processes. While on gene level histone modifications are known to change during differentiation, very little is known about the quantitative fluctuations in bulk histone modifications during development. To investigate this issue we analysed histones isolated from four different developmental stages of Xenopus laevis by mass spectrometry. In toto, we quantified 59 modification states on core histones H3 and H4 from blastula to tadpole stages. During this developmental period, we observed in general an increase in the unmodified states, and a shift from histone modifications associated with transcriptional activity to transcriptionally repressive histone marks. We also compared these naturally occurring patterns with the histone modifications of murine ES cells, detecting large differences in the methylation patterns of histone H3 lysines 27 and 36 between pluripotent ES cells and pluripotent cells from Xenopus blastulae. By combining all detected modification transitions we could cluster their patterns according to their embryonic origin, defining specific histone modification profiles (HMPs) for each developmental stage. To our knowledge, this data set represents the first compendium of covalent histone modifications and their quantitative flux during normogenesis in a vertebrate model organism. The HMPs indicate a stepwise maturation of the embryonic epigenome, which may be causal to the progressing restriction of cellular potency during development.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0022548</identifier><identifier>PMID: 21814581</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Biology ; Blastula ; Blastula - cytology ; Blastula - metabolism ; Blotting, Western ; Cell Differentiation ; Chromatin ; Chromatography, Liquid ; Cloning ; Deoxyribonucleic acid ; Developmental stages ; Differentiation ; DNA ; DNA binding proteins ; DNA methylation ; Embryo, Nonmammalian - cytology ; Embryo, Nonmammalian - metabolism ; Embryonic development ; Embryonic Stem Cells - metabolism ; Embryos ; Epigenetics ; Epigenomics ; Gene expression ; Gene Expression Profiling ; Genes ; Genomes ; Histone H3 ; Histones ; Histones - chemistry ; Histones - metabolism ; Laboratories ; Lysine - chemistry ; Lysine - genetics ; Mass spectrometry ; Mass spectroscopy ; Methylation ; Mice ; Mice, Inbred ICR ; Molecular biology ; Pluripotency ; Post-translation ; Protein Processing, Post-Translational ; Scientific imaging ; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization ; Sperm ; Toads ; Transcription ; Xenopus ; Xenopus laevis ; Xenopus laevis - embryology ; Xenopus laevis - genetics</subject><ispartof>PloS one, 2011-07, Vol.6 (7), p.e22548-e22548</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Schneider 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. 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By the process of embryonic induction, these precursor cells are assigned to specific fates and differentiation programs. Histone post-translational modifications are thought to play a key role in the establishment and maintenance of stable gene expression patterns underlying these processes. While on gene level histone modifications are known to change during differentiation, very little is known about the quantitative fluctuations in bulk histone modifications during development. To investigate this issue we analysed histones isolated from four different developmental stages of Xenopus laevis by mass spectrometry. In toto, we quantified 59 modification states on core histones H3 and H4 from blastula to tadpole stages. During this developmental period, we observed in general an increase in the unmodified states, and a shift from histone modifications associated with transcriptional activity to transcriptionally repressive histone marks. We also compared these naturally occurring patterns with the histone modifications of murine ES cells, detecting large differences in the methylation patterns of histone H3 lysines 27 and 36 between pluripotent ES cells and pluripotent cells from Xenopus blastulae. By combining all detected modification transitions we could cluster their patterns according to their embryonic origin, defining specific histone modification profiles (HMPs) for each developmental stage. To our knowledge, this data set represents the first compendium of covalent histone modifications and their quantitative flux during normogenesis in a vertebrate model organism. The HMPs indicate a stepwise maturation of the embryonic epigenome, which may be causal to the progressing restriction of cellular potency during development.</description><subject>Animals</subject><subject>Biology</subject><subject>Blastula</subject><subject>Blastula - cytology</subject><subject>Blastula - metabolism</subject><subject>Blotting, Western</subject><subject>Cell Differentiation</subject><subject>Chromatin</subject><subject>Chromatography, Liquid</subject><subject>Cloning</subject><subject>Deoxyribonucleic acid</subject><subject>Developmental stages</subject><subject>Differentiation</subject><subject>DNA</subject><subject>DNA binding proteins</subject><subject>DNA methylation</subject><subject>Embryo, Nonmammalian - cytology</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Embryonic development</subject><subject>Embryonic Stem Cells - metabolism</subject><subject>Embryos</subject><subject>Epigenetics</subject><subject>Epigenomics</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Genes</subject><subject>Genomes</subject><subject>Histone H3</subject><subject>Histones</subject><subject>Histones - chemistry</subject><subject>Histones - metabolism</subject><subject>Laboratories</subject><subject>Lysine - chemistry</subject><subject>Lysine - genetics</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Methylation</subject><subject>Mice</subject><subject>Mice, Inbred ICR</subject><subject>Molecular biology</subject><subject>Pluripotency</subject><subject>Post-translation</subject><subject>Protein Processing, Post-Translational</subject><subject>Scientific imaging</subject><subject>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization</subject><subject>Sperm</subject><subject>Toads</subject><subject>Transcription</subject><subject>Xenopus</subject><subject>Xenopus laevis</subject><subject>Xenopus laevis - embryology</subject><subject>Xenopus laevis - genetics</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11r1TAYx4s43Jx-A9GCoOziHPPWNLkRxvDlwGDgVLwLafq0J4e2qUk73Lc33enGqexCcpG33_N_kuclSV5htMY0xx92bvSdbta962CNECEZE0-SEywpWXGC6NOD9XHyPIQdQhkVnD9LjgkWmGUCnyT2etA1rEIPxlbWpFsbhiiYtq6c9nqwrkt77yrbQEg93IBu0rpxRZwGr7tgJyKktkuHLaS_oHP9GFJoC3_ruigIva3jYQsvkqNKNwFezvNp8uPzp-8XX1eXV182F-eXK8MlHlZC8BxLI6UpNOEGZzjLkMG0EIYSUgGjRJKc0bzkQpcISyKBZ7RCOeRVRSQ9Td7sdfvGBTVHKShMEaccE8QisdkTpdM71Xvban-rnLbq7sD5Wmk_WNOAQizDpopOkCasQFxSxrmhGZdliRGrotbH2dtYtFAa6GJUmoXo8qazW1W7G0Uxi1mYHvN-FvDu9whhUK0NBppGd-DGoITASAiR80i-_Yd8_HMzVev4fttVLro1k6Y6ZzkXgiEmIrV-hIqjhNaaWABTvpcGZwuDyAzwZ6j1GILaXH_7f_bq55J9d8BuY3UN2-Ca8a6qliDbg8a7EDxUDzHGSE0NcR8NNTWEmhsimr0-zM-D0X0H0L_QJwVt</recordid><startdate>20110722</startdate><enddate>20110722</enddate><creator>Schneider, Tobias D</creator><creator>Arteaga-Salas, Jose M</creator><creator>Mentele, Edith</creator><creator>David, Robert</creator><creator>Nicetto, Dario</creator><creator>Imhof, Axel</creator><creator>Rupp, Ralph A W</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>PHGZM</scope><scope>PHGZT</scope><scope>PIMPY</scope><scope>PJZUB</scope><scope>PKEHL</scope><scope>PPXIY</scope><scope>PQEST</scope><scope>PQGLB</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>20110722</creationdate><title>Stage-specific histone modification profiles reveal global transitions in the Xenopus embryonic epigenome</title><author>Schneider, Tobias D ; Arteaga-Salas, Jose M ; Mentele, Edith ; David, Robert ; Nicetto, Dario ; Imhof, Axel ; Rupp, Ralph A W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c691t-886719c99cba26c151550c13b8c322fe432927437d68ad01929e653f07e7ff293</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Animals</topic><topic>Biology</topic><topic>Blastula</topic><topic>Blastula - 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By the process of embryonic induction, these precursor cells are assigned to specific fates and differentiation programs. Histone post-translational modifications are thought to play a key role in the establishment and maintenance of stable gene expression patterns underlying these processes. While on gene level histone modifications are known to change during differentiation, very little is known about the quantitative fluctuations in bulk histone modifications during development. To investigate this issue we analysed histones isolated from four different developmental stages of Xenopus laevis by mass spectrometry. In toto, we quantified 59 modification states on core histones H3 and H4 from blastula to tadpole stages. During this developmental period, we observed in general an increase in the unmodified states, and a shift from histone modifications associated with transcriptional activity to transcriptionally repressive histone marks. We also compared these naturally occurring patterns with the histone modifications of murine ES cells, detecting large differences in the methylation patterns of histone H3 lysines 27 and 36 between pluripotent ES cells and pluripotent cells from Xenopus blastulae. By combining all detected modification transitions we could cluster their patterns according to their embryonic origin, defining specific histone modification profiles (HMPs) for each developmental stage. To our knowledge, this data set represents the first compendium of covalent histone modifications and their quantitative flux during normogenesis in a vertebrate model organism. The HMPs indicate a stepwise maturation of the embryonic epigenome, which may be causal to the progressing restriction of cellular potency during development.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21814581</pmid><doi>10.1371/journal.pone.0022548</doi><tpages>e22548</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | PloS one, 2011-07, Vol.6 (7), p.e22548-e22548 |
| issn | 1932-6203 1932-6203 |
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| source | PLoS; MEDLINE; DOAJ Directory of Open Access Journals; PubMed Central; Free Full-Text Journals in Chemistry; EZB Electronic Journals Library |
| subjects | Animals Biology Blastula Blastula - cytology Blastula - metabolism Blotting, Western Cell Differentiation Chromatin Chromatography, Liquid Cloning Deoxyribonucleic acid Developmental stages Differentiation DNA DNA binding proteins DNA methylation Embryo, Nonmammalian - cytology Embryo, Nonmammalian - metabolism Embryonic development Embryonic Stem Cells - metabolism Embryos Epigenetics Epigenomics Gene expression Gene Expression Profiling Genes Genomes Histone H3 Histones Histones - chemistry Histones - metabolism Laboratories Lysine - chemistry Lysine - genetics Mass spectrometry Mass spectroscopy Methylation Mice Mice, Inbred ICR Molecular biology Pluripotency Post-translation Protein Processing, Post-Translational Scientific imaging Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization Sperm Toads Transcription Xenopus Xenopus laevis Xenopus laevis - embryology Xenopus laevis - genetics |
| title | Stage-specific histone modification profiles reveal global transitions in the Xenopus embryonic epigenome |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-14T18%3A30%3A35IST&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=Stage-specific%20histone%20modification%20profiles%20reveal%20global%20transitions%20in%20the%20Xenopus%20embryonic%20epigenome&rft.jtitle=PloS%20one&rft.au=Schneider,%20Tobias%20D&rft.date=2011-07-22&rft.volume=6&rft.issue=7&rft.spage=e22548&rft.epage=e22548&rft.pages=e22548-e22548&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0022548&rft_dat=%3Cgale_plos_%3EA476884048%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=1306361204&rft_id=info:pmid/21814581&rft_galeid=A476884048&rft_doaj_id=oai_doaj_org_article_0451cf1920a24b0693466c3569dd104f&rfr_iscdi=true |