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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Veröffentlicht in:Gigascience 2022-12, Vol.12
Hauptverfasser: 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
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container_title Gigascience
container_volume 12
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
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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. 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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. 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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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