Androgen Receptor Function Links Human Sexual Dimorphism to DNA Methylation
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{"title"=>"Androgen Receptor Function Links Human Sexual Dimorphism to DNA Methylation", "type"=>"journal", "authors"=>[{"first_name"=>"Ole", "last_name"=>"Ammerpohl", "scopus_author_id"=>"14633018000"}, {"first_name"=>"Susanne", "last_name"=>"Bens", "scopus_author_id"=>"12771570500"}, {"first_name"=>"Mahesh", "last_name"=>"Appari", "scopus_author_id"=>"26427992000"}, {"first_name"=>"Ralf", "last_name"=>"Werner", "scopus_author_id"=>"7202442526"}, {"first_name"=>"Bernhard", "last_name"=>"Korn", "scopus_author_id"=>"7003711262"}, {"first_name"=>"Stenvert L.S.", "last_name"=>"Drop", "scopus_author_id"=>"7006009743"}, {"first_name"=>"Frans", "last_name"=>"Verheijen", "scopus_author_id"=>"7004193085"}, {"first_name"=>"Yvonne", "last_name"=>"van der Zwan", "scopus_author_id"=>"54279651300"}, {"first_name"=>"Trevor", "last_name"=>"Bunch", "scopus_author_id"=>"35093673700"}, {"first_name"=>"Ieuan", "last_name"=>"Hughes", "scopus_author_id"=>"56365856800"}, {"first_name"=>"Martine", "last_name"=>"Cools", "scopus_author_id"=>"9943745400"}, {"first_name"=>"Felix G.", "last_name"=>"Riepe", "scopus_author_id"=>"6602835953"}, {"first_name"=>"Olaf", "last_name"=>"Hiort", "scopus_author_id"=>"7005258062"}, {"first_name"=>"Reiner", "last_name"=>"Siebert", "scopus_author_id"=>"7006769106"}, {"first_name"=>"Paul Martin", "last_name"=>"Holterhus", "scopus_author_id"=>"6603926014"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84883358312", "sgr"=>"84883358312", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0073288", "pmid"=>"24023855", "pui"=>"369736930"}, "id"=>"60c3d547-a724-3610-afa7-94044013c8da", "abstract"=>"Sex differences are well known to be determinants of development, health and disease. Epigenetic mechanisms are also known to differ between men and women through X-inactivation in females. We hypothesized that epigenetic sex differences may also result from sex hormone functions, in particular from long-lasting androgen programming. We aimed at investigating whether inactivation of the androgen receptor, the key regulator of normal male sex development, is associated with differences of the patterns of DNA methylation marks in genital tissues. To this end, we performed large scale array-based analysis of gene methylation profiles on genomic DNA from labioscrotal skin fibroblasts of 8 males and 26 individuals with androgen insensitivity syndrome (AIS) due to inactivating androgen receptor gene mutations. By this approach we identified differential methylation of 167 CpG loci representing 162 unique human genes. These were significantly enriched for androgen target genes and low CpG content promoter genes. Additional 75 genes showed a significant increase of heterogeneity of methylation in AIS compared to a high homogeneity in normal male controls. Our data show that normal and aberrant androgen receptor function is associated with distinct patterns of DNA-methylation marks in genital tissues. These findings support the concept that transcription factor binding to the DNA has an impact on the shape of the DNA methylome. These data which derived from a rare human model suggest that androgen programming of methylation marks contributes to sexual dimorphism in the human which might have considerable impact on the manifestation of sex-associated phenotypes and diseases.", "link"=>"http://www.mendeley.com/research/androgen-receptor-function-links-human-sexual-dimorphism-dna-methylation-2", "reader_count"=>26, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>2, "Researcher"=>4, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>2, "Student > Master"=>6, "Student > Bachelor"=>4, "Lecturer > Senior Lecturer"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>2, "Researcher"=>4, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>2, "Student > Master"=>6, "Student > Bachelor"=>4, "Lecturer > Senior Lecturer"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>12, "Medicine and Dentistry"=>6, "Arts and Humanities"=>1, "Neuroscience"=>1, "Psychology"=>2, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Neuroscience"=>{"Neuroscience"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}, "Arts and Humanities"=>{"Arts and Humanities"=>1}}, "reader_count_by_country"=>{"Japan"=>1, "United Kingdom"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1190781", "https://ndownloader.figshare.com/files/1190782", "https://ndownloader.figshare.com/files/1190783", "https://ndownloader.figshare.com/files/1190784", "https://ndownloader.figshare.com/files/1190785", "https://ndownloader.figshare.com/files/1190786", "https://ndownloader.figshare.com/files/1190787"], "description"=>"<div><p>Sex differences are well known to be determinants of development, health and disease. Epigenetic mechanisms are also known to differ between men and women through X-inactivation in females. We hypothesized that epigenetic sex differences may also result from sex hormone functions, in particular from long-lasting androgen programming. We aimed at investigating whether inactivation of the androgen receptor, the key regulator of normal male sex development, is associated with differences of the patterns of DNA methylation marks in genital tissues. To this end, we performed large scale array-based analysis of gene methylation profiles on genomic DNA from labioscrotal skin fibroblasts of 8 males and 26 individuals with androgen insensitivity syndrome (AIS) due to inactivating androgen receptor gene mutations. By this approach we identified differential methylation of 167 CpG loci representing 162 unique human genes. These were significantly enriched for androgen target genes and low CpG content promoter genes. Additional 75 genes showed a significant increase of heterogeneity of methylation in AIS compared to a high homogeneity in normal male controls. Our data show that normal and aberrant androgen receptor function is associated with distinct patterns of DNA-methylation marks in genital tissues. These findings support the concept that transcription factor binding to the DNA has an impact on the shape of the DNA methylome. These data which derived from a rare human model suggest that androgen programming of methylation marks contributes to sexual dimorphism in the human which might have considerable impact on the manifestation of sex-associated phenotypes and diseases.</p></div>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Sexual differentiation", "Evolutionary developmental biology", "Pattern formation", "genetics", "epigenetics", "DNA modification", "gene expression", "Gene networks", "Genetic mutation", "Global health", "pediatrics", "receptor", "links", "dimorphism", "dna"], "article_id"=>788631, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Ole Ammerpohl", "Susanne Bens", "Mahesh Appari", "Ralf Werner", "Bernhard Korn", "Stenvert L. S. Drop", "Frans Verheijen", "Yvonne van der Zwan", "Trevor Bunch", "Ieuan Hughes", "Martine Cools", "Felix G. Riepe", "Olaf Hiort", "Reiner Siebert", "Paul-Martin Holterhus"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0073288.s001", "https://dx.doi.org/10.1371/journal.pone.0073288.s002", "https://dx.doi.org/10.1371/journal.pone.0073288.s003", "https://dx.doi.org/10.1371/journal.pone.0073288.s004", "https://dx.doi.org/10.1371/journal.pone.0073288.s005", "https://dx.doi.org/10.1371/journal.pone.0073288.s006", "https://dx.doi.org/10.1371/journal.pone.0073288.s007"], "stats"=>{"downloads"=>10, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Androgen_Receptor_Function_Links_Human_Sexual_Dimorphism_to_DNA_Methylation_/788631", "title"=>"Androgen Receptor Function Links Human Sexual Dimorphism to DNA Methylation", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-09-04 02:33:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1190775"], "description"=>"<p>The bar plots show percentage of loci either located in imprinted genes, genes containing either promoters with high CpG (HCP) or low CpG (LCP) content as well as the percentage of AR target genes as determined by the GATHER tool. Grey bars: percentage of genes present on the array, black bars: percentage of genes hypomethylated and white bars: percentage of genes hypermethylated in AIS patients. p-values have been determined applying χ<sup>2</sup>-test.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Sexual differentiation", "Evolutionary developmental biology", "Pattern formation", "genetics", "epigenetics", "DNA modification", "gene expression", "Gene networks", "Genetic mutation", "Global health", "pediatrics", "genes", "hypo-", "hypermethylated", "ais", "compared"], "article_id"=>788625, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Ole Ammerpohl", "Susanne Bens", "Mahesh Appari", "Ralf Werner", "Bernhard Korn", "Stenvert L. S. Drop", "Frans Verheijen", "Yvonne van der Zwan", "Trevor Bunch", "Ieuan Hughes", "Martine Cools", "Felix G. Riepe", "Olaf Hiort", "Reiner Siebert", "Paul-Martin Holterhus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0073288.g002", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Enrichment_of_genes_either_hypo_or_hypermethylated_in_AIS_as_compared_to_normal_controls_/788625", "title"=>"Enrichment of genes either hypo- or hypermethylated in AIS as compared to normal controls.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-04 02:33:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1190776"], "description"=>"<p>(A) Unmutated inactive androgen receptor (AR) binds testosterone (T) activating the receptor. Activated AR binds directly (large arrow) to AR response elements on the DNA inducing gene expression which subsequently prevents DNA methylation (“gene1”). Additionally either the activated AR itself or AR induced genes act on suppressor complexes (S; dotted arrow) which repress particular sets of genes (“gene2”) leading finally to DNA methylation of silenced genes. (B) In AIS missing AR activity prevents activation of AR target genes which might subsequently result to (stochastic <i>de novo</i>) DNA methylation of affected genes. In contrast, genes usually silenced by AR (directly or by additional AR-dependent pathways) become expressed preventing DNA methylation. white lollipops: unmethylated DNA, filled lollipops: methylated DNA.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Sexual differentiation", "Evolutionary developmental biology", "Pattern formation", "genetics", "epigenetics", "DNA modification", "gene expression", "Gene networks", "Genetic mutation", "Global health", "pediatrics", "dna", "methylation", "patterns", "ar"], "article_id"=>788626, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Ole Ammerpohl", "Susanne Bens", "Mahesh Appari", "Ralf Werner", "Bernhard Korn", "Stenvert L. S. Drop", "Frans Verheijen", "Yvonne van der Zwan", "Trevor Bunch", "Ieuan Hughes", "Martine Cools", "Felix G. Riepe", "Olaf Hiort", "Reiner Siebert", "Paul-Martin Holterhus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0073288.g003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_of_establishment_of_DNA_methylation_patterns_by_AR_activity_/788626", "title"=>"Model of establishment of DNA methylation patterns by AR activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-04 02:33:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1190774"], "description"=>"<p>(A) Supervised cluster analysis of DNA-methylation data obtained from genital fibroblasts separates individuals with AIS (yellow) from male controls (blue) (q<0.04). DNA-methylation is presented on a relative scale. To demonstrate reproducibility all hybridizations performed in duplicates are shown separately. (B) DNA-methylation of APOD (cg05624196) in fibroblasts lacking induction of APOD upon androgen treatment (non-responder) was significantly higher compared to responding fibroblasts (responder). (C) Variability in the DNA-methylation in AIS (yellow) compared to male controls (blue). Green: low, black: medium, red: high avg-beta values. The right bar indicates p-value (F-test).</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Sexual differentiation", "Evolutionary developmental biology", "Pattern formation", "genetics", "epigenetics", "DNA modification", "gene expression", "Gene networks", "Genetic mutation", "Global health", "pediatrics", "dna", "methylation", "26", "ais", "genital", "fibroblasts"], "article_id"=>788623, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Ole Ammerpohl", "Susanne Bens", "Mahesh Appari", "Ralf Werner", "Bernhard Korn", "Stenvert L. S. Drop", "Frans Verheijen", "Yvonne van der Zwan", "Trevor Bunch", "Ieuan Hughes", "Martine Cools", "Felix G. Riepe", "Olaf Hiort", "Reiner Siebert", "Paul-Martin Holterhus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0073288.g001", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Array_based_DNA_methylation_analysis_of_26_AIS_genital_fibroblasts_and_8_male_control_genital_fibroblasts_/788623", "title"=>"Array-based DNA methylation analysis of 26 AIS genital fibroblasts and 8 male control genital fibroblasts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-04 02:33:43"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"36", "full-text"=>"42", "pdf"=>"21", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"12", "cited-by"=>"0", "year"=>"2013", "month"=>"10"}
  • {"unique-ip"=>"33", "full-text"=>"43", "pdf"=>"22", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2013", "month"=>"11"}
  • {"unique-ip"=>"26", "full-text"=>"32", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"13", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2013", "month"=>"12"}
  • {"unique-ip"=>"29", "full-text"=>"24", "pdf"=>"16", "abstract"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"1"}
  • {"unique-ip"=>"18", "full-text"=>"16", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"2"}
  • {"unique-ip"=>"21", "full-text"=>"27", "pdf"=>"8", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"3"}
  • {"unique-ip"=>"27", "full-text"=>"28", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"5"}
  • {"unique-ip"=>"22", "full-text"=>"25", "pdf"=>"21", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"6"}
  • {"unique-ip"=>"28", "full-text"=>"34", "pdf"=>"16", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"13", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"4"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"2", "cited-by"=>"1", "year"=>"2015", "month"=>"4"}
  • {"unique-ip"=>"29", "full-text"=>"25", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"7", "cited-by"=>"1", "year"=>"2015", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"13", "full-text"=>"16", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"20", "full-text"=>"23", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"3"}
  • {"unique-ip"=>"25", "full-text"=>"28", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"2"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"30", "full-text"=>"28", "pdf"=>"15", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"21", "full-text"=>"20", "pdf"=>"11", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2014", "month"=>"7"}
  • {"unique-ip"=>"21", "full-text"=>"21", "pdf"=>"10", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"2", "cited-by"=>"1", "year"=>"2014", "month"=>"8"}
  • {"unique-ip"=>"28", "full-text"=>"26", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
  • {"unique-ip"=>"32", "full-text"=>"21", "pdf"=>"7", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"17", "full-text"=>"18", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"18", "full-text"=>"14", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"13", "full-text"=>"11", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"25", "full-text"=>"31", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"3", "cited-by"=>"1", "year"=>"2015", "month"=>"1"}
  • {"unique-ip"=>"22", "full-text"=>"22", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"2", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"12", "full-text"=>"15", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"15", "full-text"=>"13", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"15", "full-text"=>"21", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"10", "full-text"=>"12", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"11", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"12", "full-text"=>"10", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"17", "full-text"=>"11", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"3", "cited-by"=>"1", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"9", "full-text"=>"5", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"11", "full-text"=>"9", "pdf"=>"10", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"12", "full-text"=>"15", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"4", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}

Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Anatomy", "average_usage"=>[248, 440, 562, 666, 765, 856, 944, 1028, 1112, 1198, 1282, 1362, 1430]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[272, 472, 600, 713, 815, 911, 1004, 1094, 1185, 1273, 1358, 1441]}, {"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[275, 472, 605, 720, 822, 921, 1013, 1106, 1200, 1289, 1378, 1459, 1531]}, {"subject_area"=>"/Biology and life sciences/Genetics", "average_usage"=>[284, 491, 620, 738, 843, 945, 1043, 1137, 1225, 1315, 1400, 1479, 1555]}, {"subject_area"=>"/Biology and life sciences/Molecular biology", "average_usage"=>[272, 466, 589, 702, 806, 903, 995, 1086, 1176, 1258, 1347, 1422, 1493]}, {"subject_area"=>"/Medicine and health sciences", "average_usage"=>[264, 460, 584, 692, 794, 887, 978, 1067, 1154, 1241, 1328, 1408, 1474]}, {"subject_area"=>"/Medicine and health sciences/Anatomy", "average_usage"=>[248, 441, 564, 668, 769, 859, 948, 1034, 1117, 1202, 1290, 1368, 1437]}]}
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