Substrate and Inhibitor Specificity of the Type II p21-Activated Kinase, PAK6
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{"title"=>"Substrate and Inhibitor Specificity of the Type II p21-Activated Kinase, PAK6", "type"=>"journal", "authors"=>[{"first_name"=>"Jia", "last_name"=>"Gao", "scopus_author_id"=>"57198100666"}, {"first_name"=>"Byung Hak", "last_name"=>"Ha", "scopus_author_id"=>"36672950500"}, {"first_name"=>"Hua Jane", "last_name"=>"Lou", "scopus_author_id"=>"55343020000"}, {"first_name"=>"Elizabeth M.", "last_name"=>"Morse", "scopus_author_id"=>"35784971400"}, {"first_name"=>"Rong", "last_name"=>"Zhang", "scopus_author_id"=>"57199380889"}, {"first_name"=>"David A.", "last_name"=>"Calderwood", "scopus_author_id"=>"7004645355"}, {"first_name"=>"Benjamin E.", "last_name"=>"Turk", "scopus_author_id"=>"7007002702"}, {"first_name"=>"Titus J.", "last_name"=>"Boggon", "scopus_author_id"=>"6603049539"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84886617114", "sgr"=>"84886617114", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0077818", "pmid"=>"24204982", "pui"=>"370137487"}, "id"=>"132cc167-7640-3405-ad21-ea209407ffb6", "abstract"=>"The p21-activated kinases (PAKs) are important effectors of Rho-family small GTPases. The PAK family consists of two groups, type I and type II, which have different modes of regulation and signaling. PAK6, a type II PAK, influences behavior and locomotor function in mice and has an ascribed role in androgen receptor signaling. Here we show that PAK6 has a peptide substrate specificity very similar to the other type II PAKs, PAK4 and PAK5 (PAK7). We find that PAK6 catalytic activity is inhibited by a peptide corresponding to its N-terminal pseudosubstrate. Introduction of a melanoma-associated mutation, P52L, into this peptide reduces pseudosubstrate autoinhibition of PAK6, and increases phosphorylation of its substrate PACSIN1 (Syndapin I) in cells. Finally we determine two co-crystal structures of PAK6 catalytic domain in complex with ATP-competitive inhibitors. We determined the 1.4 Å co-crystal structure of PAK6 with the type II PAK inhibitor PF-3758309, and the 1.95 Å co-crystal structure of PAK6 with sunitinib. These findings provide new insights into the structure-function relationships of PAK6 and may facilitate development of PAK6 targeted therapies.", "link"=>"http://www.mendeley.com/research/substrate-inhibitor-specificity-type-ii-p21activated-kinase-pak6", "reader_count"=>22, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>10, "Design"=>1, "Neuroscience"=>1, "Chemistry"=>1, "Psychology"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Design"=>{"Design"=>1}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>4}}, "reader_count_by_country"=>{"United Kingdom"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1259531"], "description"=>"<div><p>The p21-activated kinases (PAKs) are important effectors of Rho-family small GTPases. The PAK family consists of two groups, type I and type II, which have different modes of regulation and signaling. PAK6, a type II PAK, influences behavior and locomotor function in mice and has an ascribed role in androgen receptor signaling. Here we show that PAK6 has a peptide substrate specificity very similar to the other type II PAKs, PAK4 and PAK5 (PAK7). We find that PAK6 catalytic activity is inhibited by a peptide corresponding to its N-terminal pseudosubstrate. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0077818#s1\" target=\"_blank\">Introduction</a> of a melanoma-associated mutation, P52L, into this peptide reduces pseudosubstrate autoinhibition of PAK6, and increases phosphorylation of its substrate PACSIN1 (Syndapin I) in cells. Finally we determine two co-crystal structures of PAK6 catalytic domain in complex with ATP-competitive inhibitors. We determined the 1.4 Å co-crystal structure of PAK6 with the type II PAK inhibitor PF-3758309, and the 1.95 Å co-crystal structure of PAK6 with sunitinib. These findings provide new insights into the structure-function relationships of PAK6 and may facilitate development of PAK6 targeted therapies.</p></div>", "links"=>[], "tags"=>["inhibitor", "specificity", "ii", "p21-activated"], "article_id"=>833484, "categories"=>["Biological Sciences"], "users"=>["Jia Gao", "Byung Hak Ha", "Hua Jane Lou", "Elizabeth M. Morse", "Rong Zhang", "David A. Calderwood", "Benjamin E. Turk", "Titus J. Boggon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077818", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Substrate_and_Inhibitor_Specificity_of_the_Type_II_p21_Activated_Kinase_PAK6_/833484", "title"=>"Substrate and Inhibitor Specificity of the Type II p21-Activated Kinase, PAK6", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-10-28 02:51:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1259528"], "description"=>"<p>PAK6 in complex with PF-3758309 is shown with the surface of PAK6 protein colored blue for residues identical between human PAK4, PAK5 and PAK6, and white for non-conserved residues. PF-3758309 is shown in stick format with carbons shown yellow. The co-crystal structures of PAK6 with sunitinib and PAK4 in complex with its autoinhibitory pseudosubstrate <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0077818#pone.0077818-Ha1\" target=\"_blank\">[9]</a> (PDB ID: 4FII) were superposed onto the PAK6/PF-3758309 structure and both sunitinib and the autoinhibitory pseudosubstrate inhibitor are shown. The carbon atoms of sunitinib are colored orange and the carbon atoms of the PAK4 autoinhibitory pseudosubstrate are colored pink. Residues adjacent to the kinase linker display differences between the type II PAK family, and are labeled and colored green. Kinase N- and C-lobes are indicated.</p>", "links"=>[], "tags"=>["ii"], "article_id"=>833481, "categories"=>["Biological Sciences"], "users"=>["Jia Gao", "Byung Hak Ha", "Hua Jane Lou", "Elizabeth M. Morse", "Rong Zhang", "David A. Calderwood", "Benjamin E. Turk", "Titus J. Boggon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077818.g005", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Surface_conservation_of_the_type_II_PAKs_/833481", "title"=>"Surface conservation of the type II PAKs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-28 02:51:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1259526"], "description"=>"<p><b>A)</b> Overall structure of PAK6 in complex with PF-3758309. PAK6 shown in cartoon format in cyan, PF-3758309 shown in stick format with carbons shown yellow. PAK6 N-lobe, C-lobe, activation loop, C-helix and P-loop are labeled. N- and C- termini are indicated. Phosphorylated activation loop serine, pS560, is shown in stick format and labeled. <b>B)</b> Overall structure of PAK6 in complex with sunitinib. PAK6 is colored purple and carbon atoms of sunitinib are colored orange. Global structural features are as indicated in <b>A</b>. <b>C)</b> Superposition of PAK6 with PF-3758309 and PAK6 with sunitinib. Slight conformational differences are observed in the glycine-rich P-loop, the C-helix and the orientation of the N-lobe. Superposition is of the kinase domain the C-lobes. <b>D)</b> Superposition of PAK6 with PF-3758309, PAK6 with sunitinib and apo PAK6. Crystal structure of Apo PAK6 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0077818#pone.0077818-Eswaran3\" target=\"_blank\">[29]</a> (PDB ID: 2C30) superposed onto the two inhibitor-bound PAK6 structures. Significant conformational movements are observed in the N-lobe particularly around the glycine-rich P-loop and the C-helix. Boxed area indicates the zoomed region shown in <b>E</b>. <b>E)</b> Close up highlighting the conformational differences between the PAK6 structures. A kink in the C-helix is clearly visible for the PF-3758309 and sunitinib-bound structures, indicated with an arrow. All structural figures generated using CCP4mg <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0077818#pone.0077818-McNicholas1\" target=\"_blank\">[46]</a>.</p>", "links"=>[], "tags"=>["structures", "pak6", "pf-3758309"], "article_id"=>833479, "categories"=>["Biological Sciences"], "users"=>["Jia Gao", "Byung Hak Ha", "Hua Jane Lou", "Elizabeth M. Morse", "Rong Zhang", "David A. Calderwood", "Benjamin E. Turk", "Titus J. Boggon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077818.g003", "stats"=>{"downloads"=>2, "page_views"=>49, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Crystal_structures_of_PAK6_with_PF_3758309_and_with_sunitinib_/833479", "title"=>"Crystal structures of PAK6 with PF-3758309 and with sunitinib.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-28 02:51:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1259527"], "description"=>"<p><b>A)</b> Overview showing the interactions of PF-3758309 with PAK6. Residues are shown in stick format and labeled. PF-3758309 shown in stick format with carbons shown yellow. Hydrogen-bonds shown as red dashed lines. Unbiased <i>F</i><sub>obs</sub>-<i>F</i><sub>calc</sub> electron density is shown for PF-37508309 in green at 3 σ. Electron density is from the final round of refinement prior to building PF-3758309. The mode of binding is clearly visible and compatible with the final refined orientation of PF-3758309. For clarity the map is clipped at 3 Å from PF-3758309. M481 is observed in two conformations, which are both shown. Waters indicated by red spheres. <b>B)</b> Ligplot+ <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0077818#pone.0077818-Laskowski1\" target=\"_blank\">[47]</a> schematic showing the interactions of PAK6 and PF-3758309. PAK6 residues that make contact with both PF-3758309 and sunitinib are highlighted in red. Waters indicated by cyan spheres. <b>C)</b> Overview showing the interactions of sunitinib with PAK6. Residues are shown in stick format and labeled. Sunitinib shown in stick format with carbons shown orange. Hydrogen-bonds shown as red dashed lines. Unbiased <i>F</i><sub>obs</sub>-<i>F</i><sub>calc</sub> electron density shown for sunitinib in green at 3 σ. Electron density is from the final round of refinement prior to building sunitinib. The mode of binding is clearly visible and compatible with the final refined orientation of sunitinib. For clarity the map is clipped at 3 Å from sunitinib. Waters indicated by red spheres. <b>D)</b> Ligplot+ <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0077818#pone.0077818-Laskowski1\" target=\"_blank\">[47]</a> schematic showing the interactions of PAK6 and sunitinib. PAK6 residues that make contact with both PF-3758309 and sunitinib are highlighted in red. Waters indicated by cyan spheres.</p>", "links"=>[], "tags"=>["pf-3758309", "sunitinib"], "article_id"=>833480, "categories"=>["Biological Sciences"], "users"=>["Jia Gao", "Byung Hak Ha", "Hua Jane Lou", "Elizabeth M. Morse", "Rong Zhang", "David A. Calderwood", "Benjamin E. Turk", "Titus J. Boggon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077818.g004", "stats"=>{"downloads"=>1, "page_views"=>63, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Interations_of_PF_3758309_and_sunitinib_with_PAK6_/833480", "title"=>"Interations of PF-3758309 and sunitinib with PAK6.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-28 02:51:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1259525"], "description"=>"<p><b>A)</b> Alignment of the pseudosubstrate autoinhibitory domain (AID) of the type II PAK family members is shown. Pseudosubstrate region indicated by a green bar. Peptide used in panel B indicated in red. Conservation shown with “*” indicating identical, “:” indicating highly conserved and “.” Indicating semi-conserved. <b>B–D)</b> Dose-dependent relationship of the inhibition of wild-type (RRPKPVVDP), P52L (RRPK<u>L</u>VVDP) mutant, and control (APRTPGGRR) peptides on PAK6 kinase activity. <b>B)</b> Inhibition of PAK6 by wild-type (WT) peptide shown on a log scale. Data shows a mean and S.E.M error bar with 3 independent experiments. Concentration range from 0.06 mM to 5.85 mM of peptides was tested. <b>C)</b> Inhibition of PAK6 by P52L peptide shown on a log scale. Data shows a mean and S.E.M error bar with 3 independent experiments. Concentration range from 1.8 mM to 5.85 mM of peptides was tested. <b>D)</b> Inhibition of PAK6 by a control peptide. Data show a mean and S.E.M error bar with 3 independent experiments. Concentration range from 0.5 mM to 4.5 mM of peptide was tested. <b>E)</b> Inhibition plots from panels B-D shown on the same graph. <b>F)</b> Co-transfection of PAK6 with PACSIN1. Co-transfection of myc-PACSIN1 and GFP-PAK6 constructs probed for PACSIN1 phosphorylation using a phospho-specific PACSIN1 antibody. M indicates molecular weight marker. <b>G)</b> Quantification of E. Ratio of phosphorylated PACSIN1 to total PACSIN1 expressed is shown, normalized for Phospho PACSIN1/Total PACSIN1 (myc). PACSIN1 shows significantly increased phosphorylation when co-transfected with the P52L mutant compared to the wild-type PAK6 (* indicates p<0.05; ** indicates p<0.01; Student’s t-test). n = 4. Error bars indicate S.E.M.</p>", "links"=>[], "tags"=>["mutation", "pak6"], "article_id"=>833478, "categories"=>["Biological Sciences"], "users"=>["Jia Gao", "Byung Hak Ha", "Hua Jane Lou", "Elizabeth M. Morse", "Rong Zhang", "David A. Calderwood", "Benjamin E. Turk", "Titus J. Boggon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077818.g002", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_P52L_mutation_results_in_loss_of_PAK6_autoinhibition_/833478", "title"=>"P52L mutation results in loss of PAK6 autoinhibition.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-28 02:51:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1259530"], "description"=>"a<p>Parentheses indicate highest resolution shell.</p>", "links"=>[], "tags"=>["refinement"], "article_id"=>833483, "categories"=>["Biological Sciences"], "users"=>["Jia Gao", "Byung Hak Ha", "Hua Jane Lou", "Elizabeth M. Morse", "Rong Zhang", "David A. Calderwood", "Benjamin E. Turk", "Titus J. Boggon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077818.t001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Data_collection_phasing_and_refinement_statistics_/833483", "title"=>"Data collection, phasing, and refinement statistics.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-10-28 02:51:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1259524"], "description"=>"<p>Left panel, relative phosphorylation levels of 201 peptide mixtures within a positional scanning peptide library by PAK6. PAK6 was incubated with the peptide mixtures in the presence of [γ-<sup>33</sup>P]ATP, and radiolabel incorporation was assessed by phosphor imaging. A representative image of two replicates is shown. Right panel, positively selected amino acid residues at each position. Quantified spot intensities from two separate runs were background corrected and then normalized so that the average value within a position was 1.0. Residues with normalized selectivity values greater than 1.6 are shown. Values are the mean of two runs. An asterisk indicates strong apparent selection for Ser that may be an artifact due to peptide mixtures with fixed Ser residues having two potential sites of phosphorylation.</p>", "links"=>[], "tags"=>["pak6", "phosphorylation"], "article_id"=>833477, "categories"=>["Biological Sciences"], "users"=>["Jia Gao", "Byung Hak Ha", "Hua Jane Lou", "Elizabeth M. Morse", "Rong Zhang", "David A. Calderwood", "Benjamin E. Turk", "Titus J. Boggon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0077818.g001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Peptide_library_analysis_of_PAK6_phosphorylation_site_specificity_/833477", "title"=>"Peptide library analysis of PAK6 phosphorylation site specificity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-28 02:51:44"}

PMC Usage Stats | Further Information

  • {"unique-ip"=>"26", "full-text"=>"18", "pdf"=>"12", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"23", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"11"}
  • {"unique-ip"=>"33", "full-text"=>"26", "pdf"=>"12", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"27", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"12"}
  • {"unique-ip"=>"25", "full-text"=>"23", "pdf"=>"12", "abstract"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"16", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"1"}
  • {"unique-ip"=>"25", "full-text"=>"29", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"24", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"2"}
  • {"unique-ip"=>"19", "full-text"=>"14", "pdf"=>"4", "abstract"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"3"}
  • {"unique-ip"=>"15", "full-text"=>"15", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2014", "month"=>"5"}
  • {"unique-ip"=>"13", "full-text"=>"7", "pdf"=>"4", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"6"}
  • {"unique-ip"=>"24", "full-text"=>"60", "pdf"=>"21", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"15", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"4"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"4"}
  • {"unique-ip"=>"22", "full-text"=>"35", "pdf"=>"20", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
  • {"unique-ip"=>"14", "full-text"=>"18", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"15", "full-text"=>"15", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"3"}
  • {"unique-ip"=>"16", "full-text"=>"28", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"67", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"2"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"14", "full-text"=>"10", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"16", "full-text"=>"16", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"20", "full-text"=>"18", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2014", "month"=>"7"}
  • {"unique-ip"=>"11", "full-text"=>"9", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"8"}
  • {"unique-ip"=>"23", "full-text"=>"20", "pdf"=>"6", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"10", "pdf"=>"2", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"28", "full-text"=>"24", "pdf"=>"9", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
  • {"unique-ip"=>"27", "full-text"=>"25", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"15", "full-text"=>"11", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"8", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"9", "full-text"=>"11", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"9", "full-text"=>"6", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"14", "full-text"=>"18", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"17", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"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/Oncology", "average_usage"=>[249, 468, 599, 718, 820, 920, 1008, 1093, 1181, 1281, 1357, 1444, 1517]}, {"subject_area"=>"/Physical sciences/Physics", "average_usage"=>[254, 421, 527, 626, 720, 813, 900, 983, 1063, 1136, 1210, 1283, 1342]}]}
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