BMP Inhibition in Seminomas Initiates Acquisition of Pluripotency via NODAL Signaling Resulting in Reprogramming to an Embryonal Carcinoma
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{"title"=>"BMP Inhibition in Seminomas Initiates Acquisition of Pluripotency via NODAL Signaling Resulting in Reprogramming to an Embryonal Carcinoma", "type"=>"journal", "authors"=>[{"first_name"=>"Daniel", "last_name"=>"Nettersheim", "scopus_author_id"=>"22958210100"}, {"first_name"=>"Sina", "last_name"=>"Jostes", "scopus_author_id"=>"56768235500"}, {"first_name"=>"Rakesh", "last_name"=>"Sharma", "scopus_author_id"=>"56767332700"}, {"first_name"=>"Simon", "last_name"=>"Schneider", "scopus_author_id"=>"56331005900"}, {"first_name"=>"Andrea", "last_name"=>"Hofmann", "scopus_author_id"=>"39561091900"}, {"first_name"=>"Humberto J.", "last_name"=>"Ferreira", "scopus_author_id"=>"55266632000"}, {"first_name"=>"Per", "last_name"=>"Hoffmann", "scopus_author_id"=>"35242500200"}, {"first_name"=>"Glen", "last_name"=>"Kristiansen", "scopus_author_id"=>"24169060100"}, {"first_name"=>"Manel B.", "last_name"=>"Esteller", "scopus_author_id"=>"14719291800"}, {"first_name"=>"Hubert", "last_name"=>"Schorle", "scopus_author_id"=>"55977834700"}], "year"=>2015, "source"=>"PLoS Genetics", "identifiers"=>{"scopus"=>"2-s2.0-84938777512", "doi"=>"10.1371/journal.pgen.1005415", "sgr"=>"84938777512", "pmid"=>"26226633", "issn"=>"15537404", "pui"=>"605567960"}, "id"=>"c7353b20-6154-383e-842f-729555ea399d", "abstract"=>"Type II germ cell cancers (GCC) can be subdivided into seminomas and non-seminomas. Seminomas are similar to carcinoma in situ (CIS) cells, the common precursor of type II GCCs, with regard to epigenetics and expression, while embryonal carcinomas (EC) are totipotent and differentiate into teratomas, yolk-sac tumors and choriocarcinomas. GCCs can present as seminomas with a non-seminoma component, raising the question if a CIS gives rise to seminomas and ECs at the same time or whether seminomas can be reprogrammed to ECs. In this study, we utilized the seminoma cell line TCam-2 that acquires an EC-like status after xenografting into the murine flank as a model for a seminoma to EC transition and screened for factors initiating and driving this process. Analysis of expression and DNA methylation dynamics during transition of TCam-2 revealed that many pluripotency- and reprogramming-associated genes were upregulated while seminoma-markers were downregulated. Changes in expression level of 53 genes inversely correlated to changes in DNA methylation. Interestingly, after xenotransplantation 6 genes (GDF3, NODAL, DNMT3B, DPPA3, GAL, AK3L1) were rapidly induced, followed by demethylation of their genomic loci, suggesting that these 6 genes are poised for expression driving the reprogramming. We demonstrate that inhibition of BMP signaling is the initial event in reprogramming, resulting in activation of the pluripotency-associated genes and NODAL signaling. We propose that reprogramming of seminomas to ECs is a multi-step process. Initially, the microenvironment causes inhibition of BMP signaling, leading to induction of NODAL signaling. During a maturation phase, a fast acting NODAL loop stimulates its own activity and temporarily inhibits BMP signaling. During the stabilization phase, a slow acting NODAL loop, involving WNTs re-establishes BMP signaling and the pluripotency circuitry. In parallel, DNMT3B-driven de novo methylation silences seminoma-associated genes and epigenetically fixes the EC state.", "link"=>"http://www.mendeley.com/research/bmp-inhibition-seminomas-initiates-acquisition-pluripotency-via-nodal-signaling-resulting-reprogramm", "reader_count"=>24, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>3, "Researcher"=>4, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>2, "Student > Master"=>1, "Other"=>1, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>3, "Researcher"=>4, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>2, "Student > Master"=>1, "Other"=>1, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>10, "Medicine and Dentistry"=>2, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2195094", "https://ndownloader.figshare.com/files/2195095", "https://ndownloader.figshare.com/files/2195096", "https://ndownloader.figshare.com/files/2195097", "https://ndownloader.figshare.com/files/2195098", "https://ndownloader.figshare.com/files/2195099", "https://ndownloader.figshare.com/files/2195100", "https://ndownloader.figshare.com/files/2195101", "https://ndownloader.figshare.com/files/2195102", "https://ndownloader.figshare.com/files/2195103"], "description"=>"<div><p>Type II germ cell cancers (GCC) can be subdivided into seminomas and non-seminomas. Seminomas are similar to carcinoma in situ (CIS) cells, the common precursor of type II GCCs, with regard to epigenetics and expression, while embryonal carcinomas (EC) are totipotent and differentiate into teratomas, yolk-sac tumors and choriocarcinomas. GCCs can present as seminomas with a non-seminoma component, raising the question if a CIS gives rise to seminomas and ECs at the same time or whether seminomas can be reprogrammed to ECs. In this study, we utilized the seminoma cell line TCam-2 that acquires an EC-like status after xenografting into the murine flank as a model for a seminoma to EC transition and screened for factors initiating and driving this process. Analysis of expression and DNA methylation dynamics during transition of TCam-2 revealed that many pluripotency- and reprogramming-associated genes were upregulated while seminoma-markers were downregulated. Changes in expression level of 53 genes inversely correlated to changes in DNA methylation. Interestingly, after xenotransplantation 6 genes (<i>GDF3</i>, <i>NODAL</i>, <i>DNMT3B</i>, <i>DPPA3</i>, <i>GAL</i>, <i>AK3L1</i>) were rapidly induced, followed by demethylation of their genomic loci, suggesting that these 6 genes are poised for expression driving the reprogramming. We demonstrate that inhibition of BMP signaling is the initial event in reprogramming, resulting in activation of the pluripotency-associated genes and NODAL signaling. We propose that reprogramming of seminomas to ECs is a multi-step process. Initially, the microenvironment causes inhibition of BMP signaling, leading to induction of NODAL signaling. During a maturation phase, a fast acting NODAL loop stimulates its own activity and temporarily inhibits BMP signaling. During the stabilization phase, a slow acting NODAL loop, involving WNTs re-establishes BMP signaling and the pluripotency circuitry. In parallel, DNMT3B-driven de novo methylation silences seminoma-associated genes and epigenetically fixes the EC state.</p></div>", "links"=>[], "tags"=>["Reprogramming", "Embryonal Carcinoma Type II germ cell cancers", "type II GCCs", "microenvironment causes inhibition", "3l", "3b", "bmp", "wnt", "DNA Methylation Dynamics", "ec", "dnmt", "expression", "xenotransplantation 6 genes", "seminoma", "gdf", "cis", "NODAL Signaling Resulting", "DPPA", "ak", "Seminomas Initiates Acquisition", "gal", "NODAL loop"], "article_id"=>1498080, "categories"=>["Uncategorised"], "users"=>["Daniel Nettersheim", "Sina Jostes", "Rakesh Sharma", "Simon Schneider", "Andrea Hofmann", "Humberto J. Ferreira", "Per Hoffmann", "Glen Kristiansen", "Manel B. Esteller", "Hubert Schorle"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1005415.s001", "https://dx.doi.org/10.1371/journal.pgen.1005415.s002", "https://dx.doi.org/10.1371/journal.pgen.1005415.s003", "https://dx.doi.org/10.1371/journal.pgen.1005415.s004", "https://dx.doi.org/10.1371/journal.pgen.1005415.s005", "https://dx.doi.org/10.1371/journal.pgen.1005415.s006", "https://dx.doi.org/10.1371/journal.pgen.1005415.s007", "https://dx.doi.org/10.1371/journal.pgen.1005415.s008", "https://dx.doi.org/10.1371/journal.pgen.1005415.s009", "https://dx.doi.org/10.1371/journal.pgen.1005415.s010"], "stats"=>{"downloads"=>11, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BMP_Inhibition_in_Seminomas_Initiates_Acquisition_of_Pluripotency_via_NODAL_Signaling_Resulting_in_Reprogramming_to_an_Embryonal_Carcinoma_/1498080", "title"=>"BMP Inhibition in Seminomas Initiates Acquisition of Pluripotency via NODAL Signaling Resulting in Reprogramming to an Embryonal Carcinoma", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-07-30 02:56:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2195067"], "description"=>"<p>(A, B) Venn diagrams summarizing commonly up- (A) and downregulated (B) genes between seminoma, TCam-2 xenografted for 1 and 6 weeks and ECs. Corresponding data is given in (E and H in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005415#pgen.1005415.s008\" target=\"_blank\">S1 Data</a>). Genes recorded in duplicates (due to multiple probes on the array) were included only once. (C) Expression intensities of indicated genes in TCam-2 xenografted for 6 weeks and the EC group as fold change versus appropriate controls (TCam-2 in vitro /seminoma tissues). Genes were categorized (color coded) based on [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005415#pgen.1005415.ref048\" target=\"_blank\">48</a>] [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005415#pgen.1005415.ref018\" target=\"_blank\">18</a>] [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005415#pgen.1005415.ref035\" target=\"_blank\">35</a>]. (D) 5mC levels of indicated genes in seminomas, parental and xenografted TCam-2 as well as EC cell lines (2102EP, NEC8, 833KE, SuSa) as found by 450k microarray analysis. (E) BDCP analysis of 5mC data of genes and samples indicated in (D).</p>", "links"=>[], "tags"=>["Reprogramming", "Embryonal Carcinoma Type II germ cell cancers", "type II GCCs", "microenvironment causes inhibition", "3l", "3b", "bmp", "wnt", "DNA Methylation Dynamics", "ec", "dnmt", "expression", "xenotransplantation 6 genes", "seminoma", "gdf", "cis", "NODAL Signaling Resulting", "DPPA", "ak", "Seminomas Initiates Acquisition", "gal", "NODAL loop"], "article_id"=>1498064, "categories"=>["Uncategorised"], "users"=>["Daniel Nettersheim", "Sina Jostes", "Rakesh Sharma", "Simon Schneider", "Andrea Hofmann", "Humberto J. Ferreira", "Per Hoffmann", "Glen Kristiansen", "Manel B. Esteller", "Hubert Schorle"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005415.g003", "stats"=>{"downloads"=>2, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Meta_analysis_of_Gex_and_5mC_data_of_xenografted_TCam_2_and_GCC_tissues_/1498064", "title"=>"Meta-analysis of Gex and 5mC data of xenografted TCam-2 and GCC tissues.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-30 02:56:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2195054"], "description"=>"<p>(A—B) Unsupervised hierarchical clustering illustrates genome-wide changes in Gex (A) and 5mC (B) over time in indicated samples. Dendrograms indicate that during SET TCam-2 cells become more similar to the EC control cells.</p>", "links"=>[], "tags"=>["Reprogramming", "Embryonal Carcinoma Type II germ cell cancers", "type II GCCs", "microenvironment causes inhibition", "3l", "3b", "bmp", "wnt", "DNA Methylation Dynamics", "ec", "dnmt", "expression", "xenotransplantation 6 genes", "seminoma", "gdf", "cis", "NODAL Signaling Resulting", "DPPA", "ak", "Seminomas Initiates Acquisition", "gal", "NODAL loop"], "article_id"=>1498051, "categories"=>["Uncategorised"], "users"=>["Daniel Nettersheim", "Sina Jostes", "Rakesh Sharma", "Simon Schneider", "Andrea Hofmann", "Humberto J. Ferreira", "Per Hoffmann", "Glen Kristiansen", "Manel B. Esteller", "Hubert Schorle"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005415.g001", "stats"=>{"downloads"=>3, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Global_dynamics_of_Gex_and_5mC_during_reprogramming_of_TCam_2_cells_/1498051", "title"=>"Global dynamics of Gex and 5mC during reprogramming of TCam-2 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-30 02:56:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2195073"], "description"=>"<p>(A) IF /IHC staining of pSMAD 1 /5 in parental and xenografted TCam-2 at indicated time points. Scale bar: 100 μm. (B, C) qRT-PCR analysis of indicated genes after NOGGIN treatment of TCam-2 cells for 1–8 days. (D) Western blotting of indicated proteins 8 days after NOGGIN treatment of TCam-2 cells.</p>", "links"=>[], "tags"=>["Reprogramming", "Embryonal Carcinoma Type II germ cell cancers", "type II GCCs", "microenvironment causes inhibition", "3l", "3b", "bmp", "wnt", "DNA Methylation Dynamics", "ec", "dnmt", "expression", "xenotransplantation 6 genes", "seminoma", "gdf", "cis", "NODAL Signaling Resulting", "DPPA", "ak", "Seminomas Initiates Acquisition", "gal", "NODAL loop"], "article_id"=>1498070, "categories"=>["Uncategorised"], "users"=>["Daniel Nettersheim", "Sina Jostes", "Rakesh Sharma", "Simon Schneider", "Andrea Hofmann", "Humberto J. Ferreira", "Per Hoffmann", "Glen Kristiansen", "Manel B. Esteller", "Hubert Schorle"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005415.g004", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inhibition_of_BMP_signaling_is_crucial_for_initiation_of_reprogramming_/1498070", "title"=>"Inhibition of BMP signaling is crucial for initiation of reprogramming.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-30 02:56:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2195058"], "description"=>"<p>(A) Histogram showing changes in Gex 1–6 weeks after xenografting compared to TCam-2 in vitro. (B) Violin plot illustrating 5mC level distribution of all differentially methylated genes during SET. (C) Circos diagrams illustrate inverse correlation between Gex and 5mC during SET and in comparison to 2102EP cells in the 53 5mC /Gex-group genes. Gex and 5mC data of each analyzed gene is linked to each analyzed sample—the thicker a connection the higher the Gex /5mC level and vice versa. Thus, genes with high 5mC levels in a certain sample (thick connection) show a small connection in the illustration of Gex data. T i.v. = TCam-2 in vitro, 1w = TCam-2 in vivo 1w, 6w = TCam-2 in vivo 6w, 2102EP = 2102EP in vitro. (D) Volcano plot of Gex and 5mC data of the 5mC /Gex-group 1 and 6 weeks after xenografting. (E) Gex and 5mC dynamis of indicated genes during SET. Red framed black squares = Gex, blue framed black squares = 5mC of averaged data of 2102EP in vivo 4 /8 weeks.</p>", "links"=>[], "tags"=>["Reprogramming", "Embryonal Carcinoma Type II germ cell cancers", "type II GCCs", "microenvironment causes inhibition", "3l", "3b", "bmp", "wnt", "DNA Methylation Dynamics", "ec", "dnmt", "expression", "xenotransplantation 6 genes", "seminoma", "gdf", "cis", "NODAL Signaling Resulting", "DPPA", "ak", "Seminomas Initiates Acquisition", "gal", "NODAL loop"], "article_id"=>1498055, "categories"=>["Uncategorised"], "users"=>["Daniel Nettersheim", "Sina Jostes", "Rakesh Sharma", "Simon Schneider", "Andrea Hofmann", "Humberto J. Ferreira", "Per Hoffmann", "Glen Kristiansen", "Manel B. Esteller", "Hubert Schorle"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005415.g002", "stats"=>{"downloads"=>5, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Detailed_analyses_of_Gex_and_5mC_dynamics_during_reprogramming_of_TCam_2_cells_/1498055", "title"=>"Detailed analyses of Gex and 5mC dynamics during reprogramming of TCam-2 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-30 02:56:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2195077"], "description"=>"<p>(A) cDNA microarray expression data of BMP, NODAL and WNT signaling-associated genes in GCC tissues. <i>SOX2</i> and <i>SOX17</i> were used to determine zero level of expression intensity (black line). (B) Pie diagrams summarizing ID1 IHC data of GCC-TMAs. Stainings were classified as ID1 positive (+), negative (-), mixed with much more positive than negative cells (+ >-) and mixed with much more negative than positive cells (+ <-). (C) ZIC3 protein levels in indicated GCC cell lines and tissues. (D) Pie diagrams summarizing beta-CATENIN IHC data of GCC-TMAs. Beta-CATENIN staining was classified as membraneous (m), cytoplasmic (c) and nuclear (n). (E) IF /IHC staining of beta-CATENIN in in parental and xenografted TCam-2 cells (1, 2 and 6 weeks). Scale bar: 100 μm.</p>", "links"=>[], "tags"=>["Reprogramming", "Embryonal Carcinoma Type II germ cell cancers", "type II GCCs", "microenvironment causes inhibition", "3l", "3b", "bmp", "wnt", "DNA Methylation Dynamics", "ec", "dnmt", "expression", "xenotransplantation 6 genes", "seminoma", "gdf", "cis", "NODAL Signaling Resulting", "DPPA", "ak", "Seminomas Initiates Acquisition", "gal", "NODAL loop"], "article_id"=>1498074, "categories"=>["Uncategorised"], "users"=>["Daniel Nettersheim", "Sina Jostes", "Rakesh Sharma", "Simon Schneider", "Andrea Hofmann", "Humberto J. Ferreira", "Per Hoffmann", "Glen Kristiansen", "Manel B. Esteller", "Hubert Schorle"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005415.g005", "stats"=>{"downloads"=>3, "page_views"=>46, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BMP_NODAL_and_WNT_signaling_in_GCC_tissues_and_cell_lines_/1498074", "title"=>"BMP, NODAL and WNT signaling in GCC tissues and cell lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-30 02:56:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2195078"], "description"=>"<p>(A) Model summarizing the dynamics and events driving acquisition of pluripotency and epigenetic reprogramming of TCam-2 cells to an EC-like cell fate. (B) Models of the fast and slow acting NODAL feedback loop. Arrows indicate 'activation', T-shaped arrows indicate 'inhibition'.</p>", "links"=>[], "tags"=>["Reprogramming", "Embryonal Carcinoma Type II germ cell cancers", "type II GCCs", "microenvironment causes inhibition", "3l", "3b", "bmp", "wnt", "DNA Methylation Dynamics", "ec", "dnmt", "expression", "xenotransplantation 6 genes", "seminoma", "gdf", "cis", "NODAL Signaling Resulting", "DPPA", "ak", "Seminomas Initiates Acquisition", "gal", "NODAL loop"], "article_id"=>1498075, "categories"=>["Uncategorised"], "users"=>["Daniel Nettersheim", "Sina Jostes", "Rakesh Sharma", "Simon Schneider", "Andrea Hofmann", "Humberto J. Ferreira", "Per Hoffmann", "Glen Kristiansen", "Manel B. Esteller", "Hubert Schorle"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005415.g006", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_of_the_dynamics_and_molecular_mechanisms_during_the_SET_/1498075", "title"=>"Model of the dynamics and molecular mechanisms during the SET.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-07-30 02:56:18"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"1", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"11", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"16", "full-text"=>"16", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"47", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"13", "full-text"=>"18", "pdf"=>"12", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"9", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"17", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"25", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"11", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"24", "full-text"=>"9", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}

Relative Metric

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