A Common Variant Associated with Dyslexia Reduces Expression of the KIAA0319 Gene
Publication Date
March 27, 2009
Journal
PLOS Genetics
Authors
Megan Y. Dennis, Silvia Paracchini, Thomas S. Scerri, Ludmila Prokunina Olsson, et al
Volume
5
Issue
3
Pages
e1000436
DOI
https://dx.plos.org/10.1371/journal.pgen.1000436
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1000436
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/19325871
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2653637
Europe PMC
http://europepmc.org/abstract/MED/19325871
Web of Science
000266320100042
Scopus
63449106260
Mendeley
http://www.mendeley.com/research/common-variant-associated-dyslexia-reduces-expression-kiaa0319-gene
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Mendeley | Further Information

{"title"=>"A common variant associated with dyslexia reduces expression of the KIAA0319 gene", "type"=>"journal", "authors"=>[{"first_name"=>"Megan Y.", "last_name"=>"Dennis", "scopus_author_id"=>"15130981100"}, {"first_name"=>"Silvia", "last_name"=>"Paracchini", "scopus_author_id"=>"6602812326"}, {"first_name"=>"Thomas S.", "last_name"=>"Scerri", "scopus_author_id"=>"7801657283"}, {"first_name"=>"Ludmila", "last_name"=>"Prokunina-Olsson", "scopus_author_id"=>"16426739500"}, {"first_name"=>"Julian C.", "last_name"=>"Knight", "scopus_author_id"=>"7401751812"}, {"first_name"=>"Richard", "last_name"=>"Wade-Martins", "scopus_author_id"=>"6603463193"}, {"first_name"=>"Penny", "last_name"=>"Coggill", "scopus_author_id"=>"6507375211"}, {"first_name"=>"Stephan", "last_name"=>"Beck", "scopus_author_id"=>"7201824644"}, {"first_name"=>"Eric D.", "last_name"=>"Green", "scopus_author_id"=>"7201576916"}, {"first_name"=>"Anthony P.", "last_name"=>"Monaco", "scopus_author_id"=>"55704771100"}], "year"=>2009, "source"=>"PLoS Genetics", "identifiers"=>{"isbn"=>"1553-7404 (Electronic)", "pmid"=>"19325871", "doi"=>"10.1371/journal.pgen.1000436", "pui"=>"354404854", "issn"=>"15537390", "sgr"=>"63449106260", "scopus"=>"2-s2.0-63449106260"}, "id"=>"2be531e0-ab06-3d59-93a0-f755efa89902", "abstract"=>"Numerous genetic association studies have implicated the KIAA0319 gene on human chromosome 6p22 in dyslexia susceptibility. The causative variant(s) remains unknown but may modulate gene expression, given that (1) a dyslexia-associated haplotype has been implicated in the reduced expression of KIAA0319, and (2) the strongest association has been found for the region spanning exon 1 of KIAA0319. Here, we test the hypothesis that variant(s) responsible for reduced KIAA0319 expression resides on the risk haplotype close to the gene's transcription start site. We identified seven single-nucleotide polymorphisms on the risk haplotype immediately upstream of KIAA0319 and determined that three of these are strongly associated with multiple reading-related traits. Using luciferase-expressing constructs containing the KIAA0319 upstream region, we characterized the minimal promoter and additional putative transcriptional regulator regions. This revealed that the minor allele of rs9461045, which shows the strongest association with dyslexia in our sample (max p-value = 0.0001), confers reduced luciferase expression in both neuronal and non-neuronal cell lines. Additionally, we found that the presence of this rs9461045 dyslexia-associated allele creates a nuclear protein-binding site, likely for the transcriptional silencer OCT-1. Knocking down OCT-1 expression in the neuronal cell line SHSY5Y using an siRNA restores KIAA0319 expression from the risk haplotype to nearly that seen from the non-risk haplotype. Our study thus pinpoints a common variant as altering the function of a dyslexia candidate gene and provides an illustrative example of the strategic approach needed to dissect the molecular basis of complex genetic traits.", "link"=>"http://www.mendeley.com/research/common-variant-associated-dyslexia-reduces-expression-kiaa0319-gene", "reader_count"=>70, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>5, "Researcher"=>18, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>16, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>8, "Lecturer"=>1, "Professor"=>8, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>5, "Researcher"=>18, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>16, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>8, "Lecturer"=>1, "Professor"=>8, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Engineering"=>3, "Biochemistry, Genetics and Molecular Biology"=>9, "Medicine and Dentistry"=>4, "Agricultural and Biological Sciences"=>34, "Neuroscience"=>3, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Business, Management and Accounting"=>1, "Psychology"=>11, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Neuroscience"=>{"Neuroscience"=>3}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>11}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>34}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Netherlands"=>2, "United States"=>3, "United Kingdom"=>3, "South Africa"=>1}, "group_count"=>4}

CrossRef

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/446742", "https://ndownloader.figshare.com/files/446801", "https://ndownloader.figshare.com/files/446857", "https://ndownloader.figshare.com/files/446884", "https://ndownloader.figshare.com/files/446914", "https://ndownloader.figshare.com/files/446984", "https://ndownloader.figshare.com/files/447051"], "description"=>"<div><p>Numerous genetic association studies have implicated the <em>KIAA0319</em> gene on human chromosome 6p22 in dyslexia susceptibility. The causative variant(s) remains unknown but may modulate gene expression, given that (1) a dyslexia-associated haplotype has been implicated in the reduced expression of <em>KIAA0319</em>, and (2) the strongest association has been found for the region spanning exon 1 of <em>KIAA0319</em>. Here, we test the hypothesis that variant(s) responsible for reduced <em>KIAA0319</em> expression resides on the risk haplotype close to the gene's transcription start site. We identified seven single-nucleotide polymorphisms on the risk haplotype immediately upstream of <em>KIAA0319</em> and determined that three of these are strongly associated with multiple reading-related traits. Using luciferase-expressing constructs containing the <em>KIAA0319</em> upstream region, we characterized the minimal promoter and additional putative transcriptional regulator regions. This revealed that the minor allele of rs9461045, which shows the strongest association with dyslexia in our sample (max <em>p</em>-value = 0.0001), confers reduced luciferase expression in both neuronal and non-neuronal cell lines. Additionally, we found that the presence of this rs9461045 dyslexia-associated allele creates a nuclear protein-binding site, likely for the transcriptional silencer OCT-1. Knocking down <em>OCT-1</em> expression in the neuronal cell line SHSY5Y using an siRNA restores <em>KIAA0319</em> expression from the risk haplotype to nearly that seen from the non-risk haplotype. Our study thus pinpoints a common variant as altering the function of a dyslexia candidate gene and provides an illustrative example of the strategic approach needed to dissect the molecular basis of complex genetic traits.</p></div>", "links"=>[], "tags"=>["variant", "dyslexia", "reduces"], "article_id"=>148064, "categories"=>["Genetics", "Neuroscience"], "users"=>["Megan Y. Dennis", "Silvia Paracchini", "Thomas S. Scerri", "Ludmila Prokunina-Olsson", "Julian C. Knight", "Richard Wade-Martins", "Penny Coggill", "Stephan Beck", "Eric D. Green", "Anthony P. Monaco"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000436.s001", "https://dx.doi.org/10.1371/journal.pgen.1000436.s002", "https://dx.doi.org/10.1371/journal.pgen.1000436.s003", "https://dx.doi.org/10.1371/journal.pgen.1000436.s004", "https://dx.doi.org/10.1371/journal.pgen.1000436.s005", "https://dx.doi.org/10.1371/journal.pgen.1000436.s006", "https://dx.doi.org/10.1371/journal.pgen.1000436.s007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Common_Variant_Associated_with_Dyslexia_Reduces_Expression_of_the_KIAA0319_Gene/148064", "title"=>"A Common Variant Associated with Dyslexia Reduces Expression of the <em>KIAA0319</em> Gene", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-03-27 02:14:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/903062"], "description"=>"<p>(A) Graphical representation of the location of the seven SNPs (corresponding to SNPs 1–7) on the RD-associated risk haplotype within the genomic region 4,028 bp upstream and 77 bp downstream of the <i>KIAA0319</i> TSS. The asterisk within <i>TTRAP</i> depicts the location of rs2143340, the risk haplotype-tagging SNP. (B) Associations of each SNP variant with the six indicated quantitative reading-related measures, as assessed by genotyping sample 1 (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000436#s2\" target=\"_blank\">Methods</a> for details). (C) Representation of LD across the genomic region harboring these variants (calculated from the same genotyping data as in B), evaluated by Haploview version 4.0. The indicated numbers represent absolute D prime (D') between two loci. An empty red box represents complete LD, while an empty blue box indicates low LD. (D) MultiPip (percent identity plot) alignment of genomic sequence from the indicated vertebrate species across the region containing SNPs 1–7 compared to the human sequence derived from the non-risk BAC. Red indicates >75% identity between that species' sequence and the human sequence over 100 nucleotides; green indicates >50% identity between that species' sequence and the human sequence over 100 nucleotides; grey corresponds to sequence missing in that species; white corresponds to no sequence from that species aligning with the human sequence for the indicated interval. At the bottom, the nucleotide-level alignments are provided for the immediate regions encompassing SNPs 2, 4, and 5 (with the position of the SNP highlighted in each case; note that the depicted human sequence reflects the non-risk haplotype). A dot indicates that the corresponding base in that species matches the base in the human reference sequence.</p>", "links"=>[], "tags"=>["promoter", "snps", "residing", "rd-associated"], "article_id"=>573509, "categories"=>["Genetics", "Neuroscience"], "users"=>["Megan Y. Dennis", "Silvia Paracchini", "Thomas S. Scerri", "Ludmila Prokunina-Olsson", "Julian C. Knight", "Richard Wade-Martins", "Penny Coggill", "Stephan Beck", "Eric D. Green", "Anthony P. Monaco"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000436.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_KIAA0319_promoter_region_SNPs_residing_on_the_RD_associated_risk_haplotype_/573509", "title"=>"<i>KIAA0319</i> promoter region SNPs residing on the RD-associated risk haplotype.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-27 00:58:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/903152"], "description"=>"<p>(A) Luciferase-expressing constructs containing different portions of the <i>KIAA0319</i> promoter region from the non-risk haplotype were generated. Restriction sites relevant to the creation of the depicted “deletion series” of constructs are shown, as are the locations of SNPs 1–7 (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000436#pgen-1000436-g001\" target=\"_blank\">Figure 1A</a>). Each construct was transfected into SHSY5Y and SK-N-MC neuronal cell lines and subsequent luciferase expression measured; all assays were performed in quadruplicate and repeated at least three times. RLA for each construct was scaled such that pGL3-Basic activity equaled 1.0. Error bars represent the standard error of the mean. The green box in each construct represents the proximal end of <i>KIAA0319</i>, with the arrow indicating the TSS. (B) Additional studies were performed with constructs containing disrupted RFX1- or ETF-binding sites (represented by a red triangle and red square, respectively).</p>", "links"=>[], "tags"=>["putative", "promoter"], "article_id"=>573601, "categories"=>["Genetics", "Neuroscience"], "users"=>["Megan Y. Dennis", "Silvia Paracchini", "Thomas S. Scerri", "Ludmila Prokunina-Olsson", "Julian C. Knight", "Richard Wade-Martins", "Penny Coggill", "Stephan Beck", "Eric D. Green", "Anthony P. Monaco"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000436.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luciferase_based_expression_analysis_of_the_putative_KIAA0319_promoter_region_/573601", "title"=>"Luciferase-based expression analysis of the putative <i>KIAA0319</i> promoter region.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-27 01:00:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/903255"], "description"=>"<p>(A) Luciferase expression from constructs containing the risk versus non-risk variants of SNPs 2, 4, and 5 was measured in SHSY5Y, SK-N-MC, and HEK293T cells. White and red circles represent the non-risk and risk variants, respectively (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000436#pgen-1000436-g002\" target=\"_blank\">Figure 2</a> for additional features of the depicted constructs). All assays were performed in quadruplicate and repeated at least three times. Error bars represent the standard error of the mean. The vertical dashed line represents the RLA measured for the construct containing the non-risk haplotype (set at 1.0 RLA); note that this reflects a different scale than the RLA depicted in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000436#pgen-1000436-g002\" target=\"_blank\">Figure 2</a>. For all three cell lines, only the construct containing the SNP 2 risk variant (denoted with a red arrow) yielded a significant RLA difference compared to the construct containing the non-risk haplotype, as analyzed using an unpaired two-sided t-test (P = 8.32×10<sup>−10</sup>, SHSY5Y; P = 3.92×10<sup>−7</sup>, SK-N-MC; P = 4.02×10<sup>−8</sup>, HEK293T). (B) EMSA testing the binding of SHSY5Y nuclear protein(s) to probes containing the SNP 2 risk versus non-risk variant. The presence of a competitor is denoted above each lane: -, no competitor; R, risk competitor; N, non-risk competitor; AP2, competitor containing an AP2-binding site (negative control); and *, 10-fold and **, 100-fold excess of competitor, respectively. (C) EMSA testing the binding of SHSY5Y nuclear protein(s) to probes containing the SNP 2 risk variant in the presence of competitors containing binding sites for CRX, OCT-1, and AP2 (negative control). (D) Supershift EMSA testing the binding of SHSY5Y nuclear protein(s) to probes containing the SNP 2 risk variant in the presence of anti-CRX or -OCT-1 antibody or general rabbit antiserum.</p>", "links"=>[], "tags"=>["non-risk", "variants", "luciferase"], "article_id"=>573692, "categories"=>["Genetics", "Neuroscience"], "users"=>["Megan Y. Dennis", "Silvia Paracchini", "Thomas S. Scerri", "Ludmila Prokunina-Olsson", "Julian C. Knight", "Richard Wade-Martins", "Penny Coggill", "Stephan Beck", "Eric D. Green", "Anthony P. Monaco"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000436.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_risk_versus_non_risk_variants_on_luciferase_expression_and_nuclear_protein_binding_/573692", "title"=>"Effect of risk versus non-risk variants on luciferase expression and nuclear protein binding.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-27 01:01:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/903351"], "description"=>"<p><i>KIAA0319</i> expression from the risk versus non-risk haplotype measured in SHSY5Y neuronal cells transfected with a scrambled versus OCT-1–specific siRNA. Allele-specific <i>KIAA0319</i> expression of all samples was quantified by measurements of the allelic ratios of two heterozygous coding SNPs in <i>KIAA0319</i> (rs807541 and rs4504469). The results are presented as the global mean±the standard error of the mean of the measurements in the six biological replicates (*P = 0.004; **P = 0.0003). The horizontal dashed line at 1.0 represents equal <i>KIAA0319</i> expression from the risk and non-risk haplotypes.</p>", "links"=>[], "tags"=>["oct-1", "knock-down", "shsy5y", "neuronal"], "article_id"=>573799, "categories"=>["Genetics", "Neuroscience"], "users"=>["Megan Y. Dennis", "Silvia Paracchini", "Thomas S. Scerri", "Ludmila Prokunina-Olsson", "Julian C. Knight", "Richard Wade-Martins", "Penny Coggill", "Stephan Beck", "Eric D. Green", "Anthony P. Monaco"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000436.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_OCT_1_knock_down_on_KIAA031_9_expression_in_SHSY5Y_neuronal_cells_/573799", "title"=>"Effect of OCT-1 knock-down on <i>KIAA031</i>9 expression in SHSY5Y neuronal cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-27 01:03:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/903419"], "description"=>"a<p>Uncorrected for multiple testing with only significant P-values<0.05 shown. All associations with low reading scores are with the minor alleles of the SNPs. None of the SNPs were associated with the PA trait in either sample set.</p>", "links"=>[], "tags"=>["associations", "markers", "genotyped"], "article_id"=>573868, "categories"=>["Genetics", "Neuroscience"], "users"=>["Megan Y. Dennis", "Silvia Paracchini", "Thomas S. Scerri", "Ludmila Prokunina-Olsson", "Julian C. Knight", "Richard Wade-Martins", "Penny Coggill", "Stephan Beck", "Eric D. Green", "Anthony P. Monaco"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000436.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genetic_associations_for_markers_genotyped_in_selected_U_K_sample_sets_/573868", "title"=>"Genetic associations for markers genotyped in selected U.K. sample sets.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-03-27 01:04:28"}

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  • {"unique-ip"=>"17", "full-text"=>"12", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
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  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
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  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
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  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
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  • {"unique-ip"=>"11", "full-text"=>"16", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
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  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"12", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"16", "full-text"=>"20", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"19", "full-text"=>"24", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"3", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
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Relative Metric

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