Early Developmental and Evolutionary Origins of Gene Body DNA Methylation Patterns in Mammalian Placentas
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{"title"=>"Early Developmental and Evolutionary Origins of Gene Body DNA Methylation Patterns in Mammalian Placentas", "type"=>"journal", "authors"=>[{"first_name"=>"Diane I.", "last_name"=>"Schroeder", "scopus_author_id"=>"8079230800"}, {"first_name"=>"Kartika", "last_name"=>"Jayashankar", "scopus_author_id"=>"16646046900"}, {"first_name"=>"Kory C.", "last_name"=>"Douglas", "scopus_author_id"=>"36545887900"}, {"first_name"=>"Twanda L.", "last_name"=>"Thirkill", "scopus_author_id"=>"6602713622"}, {"first_name"=>"Daniel", "last_name"=>"York", "scopus_author_id"=>"56583577900"}, {"first_name"=>"Pete J.", "last_name"=>"Dickinson", "scopus_author_id"=>"7006444753"}, {"first_name"=>"Lawrence E.", "last_name"=>"Williams", "scopus_author_id"=>"55462626500"}, {"first_name"=>"Paul B.", "last_name"=>"Samollow", "scopus_author_id"=>"6603951377"}, {"first_name"=>"Pablo J.", "last_name"=>"Ross", "scopus_author_id"=>"7402412763"}, {"first_name"=>"Danika L.", "last_name"=>"Bannasch", "scopus_author_id"=>"6603323478"}, {"first_name"=>"Gordon C.", "last_name"=>"Douglas", "scopus_author_id"=>"7202370054"}, {"first_name"=>"Janine M.", "last_name"=>"LaSalle", "scopus_author_id"=>"7005702015"}], "year"=>2015, "source"=>"PLoS Genetics", "identifiers"=>{"sgr"=>"84940752163", "doi"=>"10.1371/journal.pgen.1005442", "pui"=>"605889538", "pmid"=>"26241857", "scopus"=>"2-s2.0-84940752163", "issn"=>"15537404", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)"}, "id"=>"2a6b3809-f8a6-3463-b704-d66f5f057426", "abstract"=>"Over the last 20-80 million years the mammalian placenta has taken on a variety of morphologies through both divergent and convergent evolution. Recently we have shown that the human placenta genome has a unique epigenetic pattern of large partially methylated domains (PMDs) and highly methylated domains (HMDs) with gene body DNA methylation positively correlating with level of gene expression. In order to determine the evolutionary conservation of DNA methylation patterns and transcriptional regulatory programs in the placenta, we performed a genome-wide methylome (MethylC-seq) analysis of human, rhesus macaque, squirrel monkey, mouse, dog, horse, and cow placentas as well as opossum extraembryonic membrane. We found that, similar to human placenta, mammalian placentas and opossum extraembryonic membrane have globally lower levels of methylation compared to somatic tissues. Higher relative gene body methylation was the conserved feature across all mammalian placentas, despite differences in PMD/HMDs and absolute methylation levels. Specifically, higher methylation over the bodies of genes involved in mitosis, vesicle-mediated transport, protein phosphorylation, and chromatin modification was observed compared with the rest of the genome. As in human placenta, higher methylation is associated with higher gene expression and is predictive of genic location across species. Analysis of DNA methylation in oocytes and preimplantation embryos shows a conserved pattern of gene body methylation similar to the placenta. Intriguingly, mouse and cow oocytes and mouse early embryos have PMD/HMDs but their placentas do not, suggesting that PMD/HMDs are a feature of early preimplantation methylation patterns that become lost during placental development in some species and following implantation of the embryo.", "link"=>"http://www.mendeley.com/research/early-developmental-evolutionary-origins-gene-body-dna-methylation-patterns-mammalian-placentas", "reader_count"=>54, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Student > Doctoral Student"=>3, "Researcher"=>16, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Student > Doctoral Student"=>3, "Researcher"=>16, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>17, "Medicine and Dentistry"=>3, "Agricultural and Biological Sciences"=>27, "Computer Science"=>3, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>27}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>17}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>3, "Japan"=>1, "Ukraine"=>1, "United Kingdom"=>1, "Australia"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2200456"], "description"=>"<p>(A) Phylogenetic tree of the species studied and the classification of their placenta types. Branch lengths are not to scale. (B) Density curves of average percent methylation in non-overlapping 20 kb windows in mammalian placentas. For comparison, the methylation distribution for brain tissue is shown in beige for some species and human cord blood is shown in aquamarine. The opossum brain sample was fetal whereas the other brain samples were postnatal. The interquartile range and medians are shown as black bars and white dots, respectively, for the placenta samples. Mouse brain data is from Hon et al. [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.ref019\" target=\"_blank\">19</a>] (GSE42836), human placenta data is from Schroeder et al [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.ref021\" target=\"_blank\">21</a>] (GSE25930). (C) Comparison of global methylation patterns in select species after liftOver to the human genome and smoothing (for full figure, see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.s004\" target=\"_blank\">S4 Fig</a>). Human placenta PMDs, as determined by HMM, are shown in black bars at top. (D) Comparison of methylation patterns at the <i>CNTNAP2</i> locus in select species (for full figure, see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.s005\" target=\"_blank\">S5 Fig</a>). Raw species CpG site methylation wig data were graphed on the UCSC Genome Browser without preprocessing. Black line represents 50% methylation. Genes of interest are orange. EEM = extra-embryonic membrane.</p>", "links"=>[], "tags"=>["DNA Methylation Patterns", "preimplantation methylation patterns", "placenta", "methylated domains", "HMD", "gene expression", "Gene Body DNA Methylation", "pmd", "Gene Body DNA Methylation Patterns", "opossum extraembryonic membrane", "gene body methylation"], "article_id"=>1502096, "categories"=>["Biological Sciences"], "users"=>["Diane I. Schroeder", "Kartika Jayashankar", "Kory C. Douglas", "Twanda L. Thirkill", "Daniel York", "Pete J. Dickinson", "Lawrence E. Williams", "Paul B. Samollow", "Pablo J. Ross", "Danika L. Bannasch", "Gordon C. Douglas", "Janine M. LaSalle"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005442.g001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genome_wide_methylation_patterns_in_mammalian_placentas_show_both_large_scale_divergence_and_gene_specific_similarities_/1502096", "title"=>"Genome-wide methylation patterns in mammalian placentas show both large-scale divergence and gene-specific similarities.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-08-04 03:39:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/2200466"], "description"=>"<p>(A) Relationship between average gene body percent methylation and gene expression in placentas. Only gene with orthologs were used. The right column shows a density scatterplot with gray and purple show areas of low and high density, respectively. Black lines show the marginal distribution of percent methylation in gene bodies. The left column shows the number of genes in each quadrant above/below what would be expected if gene expression and gene body methylation were independent. Human, mouse, and opossum expression data are from Necsulea et al. [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.ref030\" target=\"_blank\">30</a>] (GSE43520) and horse expression data is from Wang et al. [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.ref031\" target=\"_blank\">31</a>](GSE30243). (B) Comparison of methylation and gene expression patterns at the <i>HECTD1</i> locus. Genes of interest are orange.</p>", "links"=>[], "tags"=>["DNA Methylation Patterns", "preimplantation methylation patterns", "placenta", "methylated domains", "HMD", "gene expression", "Gene Body DNA Methylation", "pmd", "Gene Body DNA Methylation Patterns", "opossum extraembryonic membrane", "gene body methylation"], "article_id"=>1502099, "categories"=>["Biological Sciences"], "users"=>["Diane I. Schroeder", "Kartika Jayashankar", "Kory C. Douglas", "Twanda L. Thirkill", "Daniel York", "Pete J. Dickinson", "Lawrence E. Williams", "Paul B. Samollow", "Pablo J. Ross", "Danika L. Bannasch", "Gordon C. Douglas", "Janine M. LaSalle"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005442.g003", "stats"=>{"downloads"=>3, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regions_of_high_methylation_are_enriched_for_actively_transcribed_genes_/1502099", "title"=>"Regions of high methylation are enriched for actively transcribed genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-08-04 03:39:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/2200476"], "description"=>"<p>(A) Distribution of average methylation in 50 kb windows (first column) and gene bodies (second column) during early human, mouse, and cow development. The third column shows the relationship between average gene body methylation and gene expression in oocytes. Black lines show the marginal distribution of percent methylation in gene bodies. All protein-coding genes from each species were used. Human oocyte and sperm methylation data are from Okae et al. [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.ref027\" target=\"_blank\">27</a>] (JGAS00000000006), human oocyte expression data are from Reich et al. [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.ref034\" target=\"_blank\">34</a>] (GSE32689), mouse oocyte and sperm methylation and expression data are from Wang et al [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.ref024\" target=\"_blank\">24</a>] (GSE56697), and cow oocyte expression data are from Graf et al [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.ref033\" target=\"_blank\">33</a>] (GSE52415). (B) Heatmap of average gene body methylation in human, mouse, and cow oocytes. For a complete list of all GO and KEGG terms for each quadrant, see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.s020\" target=\"_blank\">S3 Table</a>.</p>", "links"=>[], "tags"=>["DNA Methylation Patterns", "preimplantation methylation patterns", "placenta", "methylated domains", "HMD", "gene expression", "Gene Body DNA Methylation", "pmd", "Gene Body DNA Methylation Patterns", "opossum extraembryonic membrane", "gene body methylation"], "article_id"=>1502100, "categories"=>["Biological Sciences"], "users"=>["Diane I. Schroeder", "Kartika Jayashankar", "Kory C. Douglas", "Twanda L. Thirkill", "Daniel York", "Pete J. Dickinson", "Lawrence E. Williams", "Paul B. Samollow", "Pablo J. Ross", "Danika L. Bannasch", "Gordon C. Douglas", "Janine M. LaSalle"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005442.g004", "stats"=>{"downloads"=>2, "page_views"=>40, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gene_methylation_and_expression_in_oocytes_compared_to_placenta_in_mouse_and_cow_/1502100", "title"=>"Gene methylation and expression in oocytes compared to placenta in mouse and cow.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-08-04 03:39:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/2200457"], "description"=>"<p>(A) Heatmap of average methylation in the gene bodies (introns and exons, excluding CpG islands and promoters) of orthologous genes. Only the top few GO biological processes with Benjamini p-values below 1.0E-3 are shown. For a complete list see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005442#pgen.1005442.s020\" target=\"_blank\">S3 Table</a>. Branches A and B were combined because they contain similar GO terms. (B) Comparison of percent methylation between human placenta (red curve) and rhesus placenta (purple curve). Rhesus methylation data was lifted over to the human genome. Vertical purple lines show large chromosomal breaks in synteny between the two species. The fourth ring in shows regions of higher (blue) and lower (red) methylation in human placenta compared to rhesus. The fourth circle in shows the locations of human genes in black. (C) Spinograms showing the probability that a 5 kb window is in a gene given that window's average percent methylation. Bars are color-coded by percent methylation and bar widths show the percentage of windows with that methylation level. Bars furthest from the 0.5 blue line marker show the most information about gene location.</p>", "links"=>[], "tags"=>["DNA Methylation Patterns", "preimplantation methylation patterns", "placenta", "methylated domains", "HMD", "gene expression", "Gene Body DNA Methylation", "pmd", "Gene Body DNA Methylation Patterns", "opossum extraembryonic membrane", "gene body methylation"], "article_id"=>1502097, "categories"=>["Biological Sciences"], "users"=>["Diane I. Schroeder", "Kartika Jayashankar", "Kory C. Douglas", "Twanda L. Thirkill", "Daniel York", "Pete J. Dickinson", "Lawrence E. Williams", "Paul B. Samollow", "Pablo J. Ross", "Danika L. Bannasch", "Gordon C. Douglas", "Janine M. LaSalle"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005442.g002", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regions_of_high_methylation_in_placentas_cover_gene_bodies_/1502097", "title"=>"Regions of high methylation in placentas cover gene bodies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-08-04 03:39:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/2200500", "https://ndownloader.figshare.com/files/2200501", "https://ndownloader.figshare.com/files/2200502", "https://ndownloader.figshare.com/files/2200503", "https://ndownloader.figshare.com/files/2200504", "https://ndownloader.figshare.com/files/2200505", "https://ndownloader.figshare.com/files/2200506", "https://ndownloader.figshare.com/files/2200507", "https://ndownloader.figshare.com/files/2200509", "https://ndownloader.figshare.com/files/2200510", "https://ndownloader.figshare.com/files/2200511", "https://ndownloader.figshare.com/files/2200512", "https://ndownloader.figshare.com/files/2200513", "https://ndownloader.figshare.com/files/2200514", "https://ndownloader.figshare.com/files/2200515", "https://ndownloader.figshare.com/files/2200516", "https://ndownloader.figshare.com/files/2200517", "https://ndownloader.figshare.com/files/2200518", "https://ndownloader.figshare.com/files/2200519", "https://ndownloader.figshare.com/files/2200520"], "description"=>"<div><p>Over the last 20-80 million years the mammalian placenta has taken on a variety of morphologies through both divergent and convergent evolution. Recently we have shown that the human placenta genome has a unique epigenetic pattern of large partially methylated domains (PMDs) and highly methylated domains (HMDs) with gene body DNA methylation positively correlating with level of gene expression. In order to determine the evolutionary conservation of DNA methylation patterns and transcriptional regulatory programs in the placenta, we performed a genome-wide methylome (MethylC-seq) analysis of human, rhesus macaque, squirrel monkey, mouse, dog, horse, and cow placentas as well as opossum extraembryonic membrane. We found that, similar to human placenta, mammalian placentas and opossum extraembryonic membrane have globally lower levels of methylation compared to somatic tissues. Higher relative gene body methylation was the conserved feature across all mammalian placentas, despite differences in PMD/HMDs and absolute methylation levels. Specifically, higher methylation over the bodies of genes involved in mitosis, vesicle-mediated transport, protein phosphorylation, and chromatin modification was observed compared with the rest of the genome. As in human placenta, higher methylation is associated with higher gene expression and is predictive of genic location across species. Analysis of DNA methylation in oocytes and preimplantation embryos shows a conserved pattern of gene body methylation similar to the placenta. Intriguingly, mouse and cow oocytes and mouse early embryos have PMD/HMDs but their placentas do not, suggesting that PMD/HMDs are a feature of early preimplantation methylation patterns that become lost during placental development in some species and following implantation of the embryo.</p></div>", "links"=>[], "tags"=>["DNA Methylation Patterns", "preimplantation methylation patterns", "placenta", "methylated domains", "HMD", "gene expression", "Gene Body DNA Methylation", "pmd", "Gene Body DNA Methylation Patterns", "opossum extraembryonic membrane", "gene body methylation"], "article_id"=>1502122, "categories"=>["Biological Sciences"], "users"=>["Diane I. Schroeder", "Kartika Jayashankar", "Kory C. Douglas", "Twanda L. Thirkill", "Daniel York", "Pete J. Dickinson", "Lawrence E. Williams", "Paul B. Samollow", "Pablo J. Ross", "Danika L. Bannasch", "Gordon C. Douglas", "Janine M. LaSalle"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1005442.s001", "https://dx.doi.org/10.1371/journal.pgen.1005442.s002", "https://dx.doi.org/10.1371/journal.pgen.1005442.s003", "https://dx.doi.org/10.1371/journal.pgen.1005442.s004", "https://dx.doi.org/10.1371/journal.pgen.1005442.s005", "https://dx.doi.org/10.1371/journal.pgen.1005442.s006", "https://dx.doi.org/10.1371/journal.pgen.1005442.s007", "https://dx.doi.org/10.1371/journal.pgen.1005442.s008", "https://dx.doi.org/10.1371/journal.pgen.1005442.s009", "https://dx.doi.org/10.1371/journal.pgen.1005442.s010", "https://dx.doi.org/10.1371/journal.pgen.1005442.s011", "https://dx.doi.org/10.1371/journal.pgen.1005442.s012", "https://dx.doi.org/10.1371/journal.pgen.1005442.s013", "https://dx.doi.org/10.1371/journal.pgen.1005442.s014", "https://dx.doi.org/10.1371/journal.pgen.1005442.s015", "https://dx.doi.org/10.1371/journal.pgen.1005442.s016", "https://dx.doi.org/10.1371/journal.pgen.1005442.s017", "https://dx.doi.org/10.1371/journal.pgen.1005442.s018", "https://dx.doi.org/10.1371/journal.pgen.1005442.s019", "https://dx.doi.org/10.1371/journal.pgen.1005442.s020"], "stats"=>{"downloads"=>20, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Early_Developmental_and_Evolutionary_Origins_of_Gene_Body_DNA_Methylation_Patterns_in_Mammalian_Placentas_/1502122", "title"=>"Early Developmental and Evolutionary Origins of Gene Body DNA Methylation Patterns in Mammalian Placentas", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-08-04 03:39:25"}

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{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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