Dynamics of DNA Methylation in Recent Human and Great Ape Evolution
Publication Date
September 05, 2013
Journal
PLOS Genetics
Authors
Irene Hernando Herraez, Javier Prado Martinez, Paras Garg, Marcos Fernandez Callejo, et al
Volume
9
Issue
9
Pages
e1003763
DOI
https://dx.plos.org/10.1371/journal.pgen.1003763
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1003763
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/24039605
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3764194
Europe PMC
http://europepmc.org/abstract/MED/24039605
Web of Science
000325076600029
Scopus
84884678913
Mendeley
http://www.mendeley.com/research/dynamics-dna-methylation-recent-human-great-ape-evolution-6
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Mendeley | Further Information

{"title"=>"Dynamics of DNA Methylation in Recent Human and Great Ape Evolution", "type"=>"journal", "authors"=>[{"first_name"=>"Irene", "last_name"=>"Hernando-Herraez", "scopus_author_id"=>"55751209700"}, {"first_name"=>"Javier", "last_name"=>"Prado-Martinez", "scopus_author_id"=>"55276465800"}, {"first_name"=>"Paras", "last_name"=>"Garg", "scopus_author_id"=>"55338380600"}, {"first_name"=>"Marcos", "last_name"=>"Fernandez-Callejo", "scopus_author_id"=>"55751636100"}, {"first_name"=>"Holger", "last_name"=>"Heyn", "scopus_author_id"=>"14039019800"}, {"first_name"=>"Christina", "last_name"=>"Hvilsom", "scopus_author_id"=>"24777994500"}, {"first_name"=>"Arcadi", "last_name"=>"Navarro", "scopus_author_id"=>"35477108400"}, {"first_name"=>"Manel", "last_name"=>"Esteller", "scopus_author_id"=>"14719291800"}, {"first_name"=>"Andrew J.", "last_name"=>"Sharp", "scopus_author_id"=>"8553148600"}, {"first_name"=>"Tomas", "last_name"=>"Marques-Bonet", "scopus_author_id"=>"11140868400"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"369904018", "sgr"=>"84884678913", "pmid"=>"24039605", "scopus"=>"2-s2.0-84884678913", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "doi"=>"10.1371/journal.pgen.1003763", "issn"=>"15537390"}, "id"=>"fd6e0880-62de-3165-9cd8-233b8cbd03e7", "abstract"=>"DNA methylation is an epigenetic modification involved in regulatory processes such as cell differentiation during development, X-chromosome inactivation, genomic imprinting and susceptibility to complex disease. However, the dynamics of DNA methylation changes between humans and their closest relatives are still poorly understood. We performed a comparative analysis of CpG methylation patterns between 9 humans and 23 primate samples including all species of great apes (chimpanzee, bonobo, gorilla and orangutan) using Illumina Methylation450 bead arrays. Our analysis identified ∼800 genes with significantly altered methylation patterns among the great apes, including ∼170 genes with a methylation pattern unique to human. Some of these are known to be involved in developmental and neurological features, suggesting that epigenetic changes have been frequent during recent human and primate evolution. We identified a significant positive relationship between the rate of coding variation and alterations of methylation at the promoter level, indicative of co-occurrence between evolution of protein sequence and gene regulation. In contrast, and supporting the idea that many phenotypic differences between humans and great apes are not due to amino acid differences, our analysis also identified 184 genes that are perfectly conserved at protein level between human and chimpanzee, yet show significant epigenetic differences between these two species. We conclude that epigenetic alterations are an important force during primate evolution and have been under-explored in evolutionary comparative genomics.", "link"=>"http://www.mendeley.com/research/dynamics-dna-methylation-recent-human-great-ape-evolution-6", "reader_count"=>161, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>6, "Researcher"=>28, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>56, "Student > Postgraduate"=>8, "Other"=>8, "Student > Master"=>21, "Student > Bachelor"=>24, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>6, "Researcher"=>28, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>56, "Student > Postgraduate"=>8, "Other"=>8, "Student > Master"=>21, "Student > Bachelor"=>24, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>34, "Mathematics"=>3, "Agricultural and Biological Sciences"=>98, "Medicine and Dentistry"=>3, "Neuroscience"=>1, "Chemistry"=>2, "Psychology"=>2, "Social Sciences"=>4, "Computer Science"=>7}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>2}, "Social Sciences"=>{"Social Sciences"=>4}, "Psychology"=>{"Psychology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>98}, "Computer Science"=>{"Computer Science"=>7}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>34}, "Mathematics"=>{"Mathematics"=>3}, "Unspecified"=>{"Unspecified"=>6}}, "reader_count_by_country"=>{"Netherlands"=>1, "Austria"=>1, "Sweden"=>1, "United States"=>7, "Italy"=>1, "Mexico"=>1, "Slovenia"=>1, "Australia"=>1, "France"=>1, "Germany"=>1, "Spain"=>2}, "group_count"=>7}

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1193419"], "description"=>"<p>Differentially methylated sites we identified using whole blood of human and chimpanzee were compared to a previous study that used the Illumina HumanMethylation27 DNA Analysis BeadChip to study liver, kidney and heart tissue in an independent population of humans and chimpanzees <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003763#pgen.1003763-Gertz1\" target=\"_blank\">[19]</a>. We found a significant trend for sites that are differentially methylated in blood to also show higher human-chimpanzee divergence in these other tissues (yellow box plot, n = 457) suggesting a conservation across other somatic tissues compared to non-differentially methylated sites in blood (grey box plot, n = 7,942).</p>", "links"=>[], "tags"=>["human-chimpanzee", "differentially", "methylated", "sites", "somatic"], "article_id"=>790523, "categories"=>["Biological Sciences"], "users"=>["Irene Hernando-Herraez", "Javier Prado-Martinez", "Paras Garg", "Marcos Fernandez-Callejo", "Holger Heyn", "Christina Hvilsom", "Arcadi Navarro", "Manel Esteller", "Andrew J. Sharp", "Tomàs Marques-Bonet"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003763.g007", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conservation_of_human_chimpanzee_differentially_methylated_sites_among_multiple_somatic_tissues_/790523", "title"=>"Conservation of human-chimpanzee differentially methylated sites among multiple somatic tissues.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:46:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193418"], "description"=>"<p><i>BRCA1</i> provides an example of co-occurrence between protein sequence evolution and gene regulation. The <i>BRCA1</i> gene shows changes in DNA methylation in a regulatory region upstream of the TSS <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003763#pgen.1003763-Rice1\" target=\"_blank\">[40]</a> and a K<sub>A</sub>/K<sub>I</sub> ratio of 0.69 between human and chimpanzee.</p>", "links"=>[], "tags"=>["methylation", "differences", "chimpanzee", "promoter"], "article_id"=>790522, "categories"=>["Biological Sciences"], "users"=>["Irene Hernando-Herraez", "Javier Prado-Martinez", "Paras Garg", "Marcos Fernandez-Callejo", "Holger Heyn", "Christina Hvilsom", "Arcadi Navarro", "Manel Esteller", "Andrew J. Sharp", "Tomàs Marques-Bonet"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003763.g006", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Example_gene_showing_methylation_differences_between_human_and_chimpanzee_at_promoter_level_/790522", "title"=>"Example gene showing methylation differences between human and chimpanzee at promoter level.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:46:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193412"], "description"=>"<p>Heat maps showing genus specific differentially methylated CpG sites. We found 2,284 human-specific differentially methylated CpGs, 1,245 specific to <i>Pan</i> species, 1,374 specific to <i>Gorilla</i> species and 5,501 changes specific to <i>Pongo</i> species. Each vertical line represents a single CpG, with each row showing the β-value obtained in each individual tested.</p>", "links"=>[], "tags"=>["methylated", "cpg", "sites", "ape"], "article_id"=>790516, "categories"=>["Biological Sciences"], "users"=>["Irene Hernando-Herraez", "Javier Prado-Martinez", "Paras Garg", "Marcos Fernandez-Callejo", "Holger Heyn", "Christina Hvilsom", "Arcadi Navarro", "Manel Esteller", "Andrew J. Sharp", "Tomàs Marques-Bonet"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003763.g002", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differentially_methylated_CpG_sites_in_each_great_ape_genus_/790516", "title"=>"Differentially methylated CpG sites in each great ape genus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:46:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193409"], "description"=>"<p>(A) Methylation changes correlate with DNA sequence changes. x-axis shows the number of nucleotide substitutions between two species per kb, y-axis shows the changes in methylation based on β-values. (B) Neighbor-joining tree based on methylation data from probes with a perfect match in all reference genomes (31,853 autosomal CpGs). Bootstrap values (1,000 permutations) are shown for each node.</p>", "links"=>[], "tags"=>["patterns", "mimic", "phylogenetic"], "article_id"=>790513, "categories"=>["Biological Sciences"], "users"=>["Irene Hernando-Herraez", "Javier Prado-Martinez", "Paras Garg", "Marcos Fernandez-Callejo", "Holger Heyn", "Christina Hvilsom", "Arcadi Navarro", "Manel Esteller", "Andrew J. Sharp", "Tomàs Marques-Bonet"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003763.g001", "stats"=>{"downloads"=>1, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Methylation_patterns_mimic_sequence_based_phylogenetic_relationships_/790513", "title"=>"Methylation patterns mimic sequence based phylogenetic relationships.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:46:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193417"], "description"=>"<p>We performed a comparison of alterations in promoter methylation with (A) the frequency of amino-acid alterations and (B) the relative rate of coding to non-coding variation with genes (K<sub>A</sub>/K<sub>I</sub>) between human and chimpanzee. Using both metrics we observed a significant association between the rate of protein evolution and epigenetic regulatory changes. P-values are based on 1,000 permutations (Differentially methylated genes, n = 745; genes without significant changes in methylation, n = 6,507).</p>", "links"=>[], "tags"=>["promoter", "methylation"], "article_id"=>790521, "categories"=>["Biological Sciences"], "users"=>["Irene Hernando-Herraez", "Javier Prado-Martinez", "Paras Garg", "Marcos Fernandez-Callejo", "Holger Heyn", "Christina Hvilsom", "Arcadi Navarro", "Manel Esteller", "Andrew J. Sharp", "Tomàs Marques-Bonet"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003763.g005", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_significant_relationship_between_changes_in_promoter_methylation_and_protein_evolution_between_human_and_chimpanzee_/790521", "title"=>"A significant relationship between changes in promoter methylation and protein evolution between human and chimpanzee.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:46:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193415"], "description"=>"<p>(A) Distribution of 99,191 CpG sites interrogated in all great ape species. Left: Gene-centric functional distribution of methylation changes : 1,500 bp upstream of gene TSSs, 200 bp upstream of TSSs, 5′UTR, 1<sup>st</sup> exon, gene body, 3′ UTR and intergenic. Right: CpG-island centric distribution: CpG island, shore (±2 kb flanking CpG islands), shelf (2–4 kb from CpG islands). (B) A non-random distribution of methylation changes in recent primate evolution. We observe an excess of differential CpG methylation within the first 1,500 bp upstream of gene TSSs, gene bodies, intergenic regions, shore regions flanking CpG islands and non-CpG island regions. In contrast DNA methylation tends to be relatively conserved close to gene transcription start sites (−200 bp of TSS to 1<sup>st</sup> exon), and in the body of CpG islands. Each bar shows the relative enrichment for differential methylation versus that expected under a null distribution. * denotes p<0.0001 (permutation test). (C) Density plot showing the distribution of methylation levels of differentially methylated sites compared to that in the rest of the genome. Sites of evolutionary change among great apes have a significantly different distribution (p = 2.2×10<sup>−16</sup> Kolmogorov-Smirnov test).</p>", "links"=>[], "tags"=>["differential", "methylation", "primate"], "article_id"=>790519, "categories"=>["Biological Sciences"], "users"=>["Irene Hernando-Herraez", "Javier Prado-Martinez", "Paras Garg", "Marcos Fernandez-Callejo", "Holger Heyn", "Christina Hvilsom", "Arcadi Navarro", "Manel Esteller", "Andrew J. Sharp", "Tomàs Marques-Bonet"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003763.g004", "stats"=>{"downloads"=>1, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Location_of_differential_methylation_in_primate_genomes_/790519", "title"=>"Location of differential methylation in primate genomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:46:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193414"], "description"=>"<p>Each data point represents the mean β-value of the group and whiskers show 2 standard deviations above and below the mean. (A) <i>ARTN</i> is a neurotrophic factor and it shows hypermethylation of 3 CpG sites associated with the long isoform specifically in human. (B) <i>COL2A1</i> shows hypermethylation of 4 CpG sites at the promoter specifically in human. This gene encodes the alpha-1 chain of type II collagen, which is found primarily in cartilage, the inner ear and the vitreous humor of the eye. (C) <i>PGAM2</i> shows hypomethylation of CpG sites at the promoter specifically in human. <i>PGAM2</i> is an enzyme involved in the glycolitic pathway, mutations in which are associated with muscle cramping and intolerance for strenuous exercise. (D) <i>GABBR1</i> shows a complex methylation pattern in which human and gorilla shows similar pattern of methylation, orangutan shows relative hypomethylation, while chimpanzees and bonobos show increased methylation levels at TSS and intermediate levels associated with the short isoform of this gene. <i>GABBR1</i> is a neuronal receptor involved in synaptic inhibition, slow wave sleep, muscle relaxation and sensitivity to pain.</p>", "links"=>[], "tags"=>["differentially", "methylated"], "article_id"=>790518, "categories"=>["Biological Sciences"], "users"=>["Irene Hernando-Herraez", "Javier Prado-Martinez", "Paras Garg", "Marcos Fernandez-Callejo", "Holger Heyn", "Christina Hvilsom", "Arcadi Navarro", "Manel Esteller", "Andrew J. Sharp", "Tomàs Marques-Bonet"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003763.g003", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Examples_of_differentially_methylated_genes_/790518", "title"=>"Examples of differentially methylated genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:46:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193423", "https://ndownloader.figshare.com/files/1193424", "https://ndownloader.figshare.com/files/1193425", "https://ndownloader.figshare.com/files/1193426", "https://ndownloader.figshare.com/files/1193427", "https://ndownloader.figshare.com/files/1193428", "https://ndownloader.figshare.com/files/1193429", "https://ndownloader.figshare.com/files/1193430", "https://ndownloader.figshare.com/files/1193431", "https://ndownloader.figshare.com/files/1193432", "https://ndownloader.figshare.com/files/1193433", "https://ndownloader.figshare.com/files/1193434", "https://ndownloader.figshare.com/files/1193435", "https://ndownloader.figshare.com/files/1193436"], "description"=>"<div><p>DNA methylation is an epigenetic modification involved in regulatory processes such as cell differentiation during development, X-chromosome inactivation, genomic imprinting and susceptibility to complex disease. However, the dynamics of DNA methylation changes between humans and their closest relatives are still poorly understood. We performed a comparative analysis of CpG methylation patterns between 9 humans and 23 primate samples including all species of great apes (chimpanzee, bonobo, gorilla and orangutan) using Illumina Methylation450 bead arrays. Our analysis identified ∼800 genes with significantly altered methylation patterns among the great apes, including ∼170 genes with a methylation pattern unique to human. Some of these are known to be involved in developmental and neurological features, suggesting that epigenetic changes have been frequent during recent human and primate evolution. We identified a significant positive relationship between the rate of coding variation and alterations of methylation at the promoter level, indicative of co-occurrence between evolution of protein sequence and gene regulation. In contrast, and supporting the idea that many phenotypic differences between humans and great apes are not due to amino acid differences, our analysis also identified 184 genes that are perfectly conserved at protein level between human and chimpanzee, yet show significant epigenetic differences between these two species. We conclude that epigenetic alterations are an important force during primate evolution and have been under-explored in evolutionary comparative genomics.</p></div>", "links"=>[], "tags"=>["dna", "methylation", "ape"], "article_id"=>790527, "categories"=>["Biological Sciences"], "users"=>["Irene Hernando-Herraez", "Javier Prado-Martinez", "Paras Garg", "Marcos Fernandez-Callejo", "Holger Heyn", "Christina Hvilsom", "Arcadi Navarro", "Manel Esteller", "Andrew J. Sharp", "Tomàs Marques-Bonet"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003763.s001", "https://dx.doi.org/10.1371/journal.pgen.1003763.s002", "https://dx.doi.org/10.1371/journal.pgen.1003763.s003", "https://dx.doi.org/10.1371/journal.pgen.1003763.s004", "https://dx.doi.org/10.1371/journal.pgen.1003763.s005", "https://dx.doi.org/10.1371/journal.pgen.1003763.s006", "https://dx.doi.org/10.1371/journal.pgen.1003763.s007", "https://dx.doi.org/10.1371/journal.pgen.1003763.s008", "https://dx.doi.org/10.1371/journal.pgen.1003763.s009", "https://dx.doi.org/10.1371/journal.pgen.1003763.s010", "https://dx.doi.org/10.1371/journal.pgen.1003763.s011", "https://dx.doi.org/10.1371/journal.pgen.1003763.s012", "https://dx.doi.org/10.1371/journal.pgen.1003763.s013", "https://dx.doi.org/10.1371/journal.pgen.1003763.s014"], "stats"=>{"downloads"=>48, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dynamics_of_DNA_Methylation_in_Recent_Human_and_Great_Ape_Evolution_/790527", "title"=>"Dynamics of DNA Methylation in Recent Human and Great Ape Evolution", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-09-05 03:46:09"}

PMC Usage Stats | Further Information

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Relative Metric

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