Developmental dynamics of chromatin accessibility during post-implantation development of monkey embryos
Abstract Background Early post-implantation development, especially gastrulation in primates, is accompanied by extensive drastic chromatin reorganization, which remains largely elusive. Results To delineate the global chromatin landscape and understand the molecular dynamics during this period, a s...
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creator | Dai, Xi Shao, Honglian Sun, Nianqin Ci, Baiquan Wu, Jun Liu, Chuanyu Wu, Liang Yuan, Yue Wei, Xiaoyu Yang, Huanming Liu, Longqi Ji, Weizhi Bai, Bing Shang, Zhouchun Tan, Tao |
description | Abstract
Background
Early post-implantation development, especially gastrulation in primates, is accompanied by extensive drastic chromatin reorganization, which remains largely elusive.
Results
To delineate the global chromatin landscape and understand the molecular dynamics during this period, a single-cell assay for transposase accessible chromatin sequencing (scATAC-seq) was applied to in vitro cultured cynomolgus monkey (Macaca fascicularis, hereafter referred to as monkey) embryos to investigate the chromatin status. First, we delineated the cis-regulatory interactions and identified the regulatory networks and critical transcription factors involved in the epiblast (EPI), hypoblast, and trophectoderm/trophoblast (TE) lineage specification. Second, we observed that the chromatin opening of some genome regions preceded the gene expression during EPI and trophoblast specification. Third, we identified the opposing roles of FGF and BMP signaling in pluripotency regulation during EPI specification. Finally, we revealed the similarity between EPI and TE in gene expression profiles and demonstrated that PATZ1 and NR2F2 were involved in EPI and trophoblast specification during monkey post-implantation development.
Conclusions
Our findings provide a useful resource and insights into dissecting the transcriptional regulatory machinery during primate post-implantation development. |
doi_str_mv | 10.1093/gigascience/giad038 |
format | Article |
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Background
Early post-implantation development, especially gastrulation in primates, is accompanied by extensive drastic chromatin reorganization, which remains largely elusive.
Results
To delineate the global chromatin landscape and understand the molecular dynamics during this period, a single-cell assay for transposase accessible chromatin sequencing (scATAC-seq) was applied to in vitro cultured cynomolgus monkey (Macaca fascicularis, hereafter referred to as monkey) embryos to investigate the chromatin status. First, we delineated the cis-regulatory interactions and identified the regulatory networks and critical transcription factors involved in the epiblast (EPI), hypoblast, and trophectoderm/trophoblast (TE) lineage specification. Second, we observed that the chromatin opening of some genome regions preceded the gene expression during EPI and trophoblast specification. Third, we identified the opposing roles of FGF and BMP signaling in pluripotency regulation during EPI specification. Finally, we revealed the similarity between EPI and TE in gene expression profiles and demonstrated that PATZ1 and NR2F2 were involved in EPI and trophoblast specification during monkey post-implantation development.
Conclusions
Our findings provide a useful resource and insights into dissecting the transcriptional regulatory machinery during primate post-implantation development.</description><identifier>ISSN: 2047-217X</identifier><identifier>EISSN: 2047-217X</identifier><identifier>DOI: 10.1093/gigascience/giad038</identifier><identifier>PMID: 37226912</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Accessibility ; Animals ; Chromatin ; Chromatin - genetics ; Embryos ; Gastrulation ; Gene expression ; Implantation ; Macaca fascicularis ; Molecular dynamics ; Monkeys ; Pluripotency ; Primates ; Specifications ; Transcription Factors ; Transposase ; Transposases ; Trophectoderm</subject><ispartof>Gigascience, 2022-12, Vol.12</ispartof><rights>The Author(s) 2023. Published by Oxford University Press GigaScience. 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press GigaScience.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c423t-471a280ac11a24d82da2c37ebed1877e7a2d0df7d1fb1b6c2a367bcff6635b2b3</cites><orcidid>0000-0001-9863-1668 ; 0000-0001-8269-8032 ; 0000-0002-8758-1834 ; 0000-0003-2550-4224 ; 0000-0002-8240-5487 ; 0000-0003-2258-0897 ; 0000-0002-5828-5542 ; 0000-0002-0858-3410 ; 0000-0001-9461-3307 ; 0000-0002-6784-0181 ; 0000-0001-8650-0388 ; 0000-0001-9592-3083 ; 0000-0002-1740-7961</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/PMC10209733/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10209733/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,1598,27903,27904,53770,53772</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37226912$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dai, Xi</creatorcontrib><creatorcontrib>Shao, Honglian</creatorcontrib><creatorcontrib>Sun, Nianqin</creatorcontrib><creatorcontrib>Ci, Baiquan</creatorcontrib><creatorcontrib>Wu, Jun</creatorcontrib><creatorcontrib>Liu, Chuanyu</creatorcontrib><creatorcontrib>Wu, Liang</creatorcontrib><creatorcontrib>Yuan, Yue</creatorcontrib><creatorcontrib>Wei, Xiaoyu</creatorcontrib><creatorcontrib>Yang, Huanming</creatorcontrib><creatorcontrib>Liu, Longqi</creatorcontrib><creatorcontrib>Ji, Weizhi</creatorcontrib><creatorcontrib>Bai, Bing</creatorcontrib><creatorcontrib>Shang, Zhouchun</creatorcontrib><creatorcontrib>Tan, Tao</creatorcontrib><title>Developmental dynamics of chromatin accessibility during post-implantation development of monkey embryos</title><title>Gigascience</title><addtitle>Gigascience</addtitle><description>Abstract
Background
Early post-implantation development, especially gastrulation in primates, is accompanied by extensive drastic chromatin reorganization, which remains largely elusive.
Results
To delineate the global chromatin landscape and understand the molecular dynamics during this period, a single-cell assay for transposase accessible chromatin sequencing (scATAC-seq) was applied to in vitro cultured cynomolgus monkey (Macaca fascicularis, hereafter referred to as monkey) embryos to investigate the chromatin status. First, we delineated the cis-regulatory interactions and identified the regulatory networks and critical transcription factors involved in the epiblast (EPI), hypoblast, and trophectoderm/trophoblast (TE) lineage specification. Second, we observed that the chromatin opening of some genome regions preceded the gene expression during EPI and trophoblast specification. Third, we identified the opposing roles of FGF and BMP signaling in pluripotency regulation during EPI specification. Finally, we revealed the similarity between EPI and TE in gene expression profiles and demonstrated that PATZ1 and NR2F2 were involved in EPI and trophoblast specification during monkey post-implantation development.
Conclusions
Our findings provide a useful resource and insights into dissecting the transcriptional regulatory machinery during primate post-implantation development.</description><subject>Accessibility</subject><subject>Animals</subject><subject>Chromatin</subject><subject>Chromatin - genetics</subject><subject>Embryos</subject><subject>Gastrulation</subject><subject>Gene expression</subject><subject>Implantation</subject><subject>Macaca fascicularis</subject><subject>Molecular dynamics</subject><subject>Monkeys</subject><subject>Pluripotency</subject><subject>Primates</subject><subject>Specifications</subject><subject>Transcription Factors</subject><subject>Transposase</subject><subject>Transposases</subject><subject>Trophectoderm</subject><issn>2047-217X</issn><issn>2047-217X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNqNkUtLJDEUhcOgjKL-AmEocOOmNI-aSnolos4DhNnMgLuQx63uaCUpkyqh_r1pusdpXU0290LO-biHg9ApwRcEL9jl0i1VNg6CgbIri5n4hA4pbnhNCX_Y29kP0EnOj7g8zoXg7DM6YJzSdkHoIVrdwgv0cfAQRtVXdg7KO5Or2FVmlaJXowuVMgZydtr1bpwrOyUXltUQ81g7P_SqOEcXQ2X_odZ-H8MTzBV4neaYj9F-p_oMJ9t5hP58u_t986O-__X95831fW0aysa64URRgZUhZTZWUKuoYRw0WCI4B66oxbbjlnSa6NZQxVquTde1LfuqqWZH6GrDHSbtwZpyTFK9HJLzKs0yKiff_wS3ksv4IgmmeMEZK4TzLSHF5wnyKL3LBvoSFOKUJRVkQbnADBfp2QfpY5xSKPkkI6zgGiLWQLZRmRRzTtC9XUOwXLcpd9qU2zaL68tukDfP3-6K4GIjiNPwX8RXrVCz0A</recordid><startdate>20221228</startdate><enddate>20221228</enddate><creator>Dai, Xi</creator><creator>Shao, Honglian</creator><creator>Sun, Nianqin</creator><creator>Ci, Baiquan</creator><creator>Wu, Jun</creator><creator>Liu, Chuanyu</creator><creator>Wu, Liang</creator><creator>Yuan, Yue</creator><creator>Wei, Xiaoyu</creator><creator>Yang, Huanming</creator><creator>Liu, Longqi</creator><creator>Ji, Weizhi</creator><creator>Bai, Bing</creator><creator>Shang, Zhouchun</creator><creator>Tan, Tao</creator><general>Oxford University Press</general><scope>TOX</scope><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>JQ2</scope><scope>K9.</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9863-1668</orcidid><orcidid>https://orcid.org/0000-0001-8269-8032</orcidid><orcidid>https://orcid.org/0000-0002-8758-1834</orcidid><orcidid>https://orcid.org/0000-0003-2550-4224</orcidid><orcidid>https://orcid.org/0000-0002-8240-5487</orcidid><orcidid>https://orcid.org/0000-0003-2258-0897</orcidid><orcidid>https://orcid.org/0000-0002-5828-5542</orcidid><orcidid>https://orcid.org/0000-0002-0858-3410</orcidid><orcidid>https://orcid.org/0000-0001-9461-3307</orcidid><orcidid>https://orcid.org/0000-0002-6784-0181</orcidid><orcidid>https://orcid.org/0000-0001-8650-0388</orcidid><orcidid>https://orcid.org/0000-0001-9592-3083</orcidid><orcidid>https://orcid.org/0000-0002-1740-7961</orcidid></search><sort><creationdate>20221228</creationdate><title>Developmental dynamics of chromatin accessibility during post-implantation development of monkey embryos</title><author>Dai, Xi ; Shao, Honglian ; Sun, Nianqin ; Ci, Baiquan ; Wu, Jun ; Liu, Chuanyu ; Wu, Liang ; Yuan, Yue ; Wei, Xiaoyu ; Yang, Huanming ; Liu, Longqi ; Ji, Weizhi ; Bai, Bing ; Shang, Zhouchun ; Tan, Tao</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c423t-471a280ac11a24d82da2c37ebed1877e7a2d0df7d1fb1b6c2a367bcff6635b2b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Accessibility</topic><topic>Animals</topic><topic>Chromatin</topic><topic>Chromatin - genetics</topic><topic>Embryos</topic><topic>Gastrulation</topic><topic>Gene expression</topic><topic>Implantation</topic><topic>Macaca fascicularis</topic><topic>Molecular dynamics</topic><topic>Monkeys</topic><topic>Pluripotency</topic><topic>Primates</topic><topic>Specifications</topic><topic>Transcription Factors</topic><topic>Transposase</topic><topic>Transposases</topic><topic>Trophectoderm</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dai, Xi</creatorcontrib><creatorcontrib>Shao, Honglian</creatorcontrib><creatorcontrib>Sun, Nianqin</creatorcontrib><creatorcontrib>Ci, Baiquan</creatorcontrib><creatorcontrib>Wu, Jun</creatorcontrib><creatorcontrib>Liu, Chuanyu</creatorcontrib><creatorcontrib>Wu, Liang</creatorcontrib><creatorcontrib>Yuan, Yue</creatorcontrib><creatorcontrib>Wei, Xiaoyu</creatorcontrib><creatorcontrib>Yang, Huanming</creatorcontrib><creatorcontrib>Liu, Longqi</creatorcontrib><creatorcontrib>Ji, Weizhi</creatorcontrib><creatorcontrib>Bai, Bing</creatorcontrib><creatorcontrib>Shang, Zhouchun</creatorcontrib><creatorcontrib>Tan, Tao</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Gigascience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dai, Xi</au><au>Shao, Honglian</au><au>Sun, Nianqin</au><au>Ci, Baiquan</au><au>Wu, Jun</au><au>Liu, Chuanyu</au><au>Wu, Liang</au><au>Yuan, Yue</au><au>Wei, Xiaoyu</au><au>Yang, Huanming</au><au>Liu, Longqi</au><au>Ji, Weizhi</au><au>Bai, Bing</au><au>Shang, Zhouchun</au><au>Tan, Tao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Developmental dynamics of chromatin accessibility during post-implantation development of monkey embryos</atitle><jtitle>Gigascience</jtitle><addtitle>Gigascience</addtitle><date>2022-12-28</date><risdate>2022</risdate><volume>12</volume><issn>2047-217X</issn><eissn>2047-217X</eissn><abstract>Abstract
Background
Early post-implantation development, especially gastrulation in primates, is accompanied by extensive drastic chromatin reorganization, which remains largely elusive.
Results
To delineate the global chromatin landscape and understand the molecular dynamics during this period, a single-cell assay for transposase accessible chromatin sequencing (scATAC-seq) was applied to in vitro cultured cynomolgus monkey (Macaca fascicularis, hereafter referred to as monkey) embryos to investigate the chromatin status. First, we delineated the cis-regulatory interactions and identified the regulatory networks and critical transcription factors involved in the epiblast (EPI), hypoblast, and trophectoderm/trophoblast (TE) lineage specification. Second, we observed that the chromatin opening of some genome regions preceded the gene expression during EPI and trophoblast specification. Third, we identified the opposing roles of FGF and BMP signaling in pluripotency regulation during EPI specification. Finally, we revealed the similarity between EPI and TE in gene expression profiles and demonstrated that PATZ1 and NR2F2 were involved in EPI and trophoblast specification during monkey post-implantation development.
Conclusions
Our findings provide a useful resource and insights into dissecting the transcriptional regulatory machinery during primate post-implantation development.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>37226912</pmid><doi>10.1093/gigascience/giad038</doi><orcidid>https://orcid.org/0000-0001-9863-1668</orcidid><orcidid>https://orcid.org/0000-0001-8269-8032</orcidid><orcidid>https://orcid.org/0000-0002-8758-1834</orcidid><orcidid>https://orcid.org/0000-0003-2550-4224</orcidid><orcidid>https://orcid.org/0000-0002-8240-5487</orcidid><orcidid>https://orcid.org/0000-0003-2258-0897</orcidid><orcidid>https://orcid.org/0000-0002-5828-5542</orcidid><orcidid>https://orcid.org/0000-0002-0858-3410</orcidid><orcidid>https://orcid.org/0000-0001-9461-3307</orcidid><orcidid>https://orcid.org/0000-0002-6784-0181</orcidid><orcidid>https://orcid.org/0000-0001-8650-0388</orcidid><orcidid>https://orcid.org/0000-0001-9592-3083</orcidid><orcidid>https://orcid.org/0000-0002-1740-7961</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Accessibility Animals Chromatin Chromatin - genetics Embryos Gastrulation Gene expression Implantation Macaca fascicularis Molecular dynamics Monkeys Pluripotency Primates Specifications Transcription Factors Transposase Transposases Trophectoderm |
title | Developmental dynamics of chromatin accessibility during post-implantation development of monkey embryos |
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