A Complete Pathway Model for Lipid A Biosynthesis in Escherichia coli
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{"title"=>"A complete pathway model for lipid a biosynthesis in Escherichia coli", "type"=>"journal", "authors"=>[{"first_name"=>"Akintunde", "last_name"=>"Emiola", "scopus_author_id"=>"55790978800"}, {"first_name"=>"John", "last_name"=>"George", "scopus_author_id"=>"56882928800"}, {"first_name"=>"Steven S.", "last_name"=>"Andrews", "scopus_author_id"=>"7202524876"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"25919634", "sgr"=>"84928794055", "doi"=>"10.1371/journal.pone.0121216", "scopus"=>"2-s2.0-84928794055", "pui"=>"604027225", "isbn"=>"10.1371/journal.pone.0121216", "issn"=>"19326203"}, "id"=>"1e8577f0-194e-3c0f-900f-e74b442c9cc8", "abstract"=>"Lipid A is a highly conserved component of lipopolysaccharide (LPS), itself a major compo-nent of the outer membrane of Gram-negative bacteria. Lipid A is essential to cells and elicits a strong immune response from humans and other animals. We developed a quanti-tative model of the nine enzyme-catalyzed steps of Escherichia coli lipid A biosynthesis, drawing parameters from the experimental literature. This model accounts for biosynthesis regulation, which occurs through regulated degradation of the LpxC and WaaA (also called KdtA) enzymes. The LpxC degradation signal appears to arise from the lipid A disaccharide concentration, which we deduced from prior results, model results, and new LpxK overex-pression results. The model agrees reasonably well with many experimental findings, in-cluding the lipid A production rate, the behaviors of mutants with defective LpxA enzymes, correlations between LpxC half-lives and cell generation times, and the effects of LpxK overexpression on LpxC concentrations. Its predictions also differ from some experimental results, which suggest modifications to the current understanding of the lipid A pathway, such as the possibility that LpxD can replace LpxA and that there may be metabolic channeling between LpxH and LpxB. The model shows that WaaA regulation may serve to regulate the lipid A production rate when the 3-deoxy-D-manno-oct-2-ulosonic acid (KDO) concentration is low and/or to control the number of KDO residues that get attached to lipid A. Computation of flux control coefficients showed that LpxC is the rate-limiting enzyme if pathway regulation is ignored, but that LpxK is the rate-limiting enzyme if pathway regula-tion is present, as it is in real cells. Control also shifts to other enzymes if the pathway sub-strate concentrations are not in excess. Based on these results, we suggest that LpxK may be a much better drug target than LpxC, which has been pursued most often.", "link"=>"http://www.mendeley.com/research/complete-pathway-model-lipid-biosynthesis-escherichia-coli-1", "reader_count"=>46, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>2, "Researcher"=>5, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>2, "Student > Master"=>10, "Other"=>2, "Student > Bachelor"=>4, "Lecturer > Senior Lecturer"=>1, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>2, "Researcher"=>5, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>2, "Student > Master"=>10, "Other"=>2, "Student > Bachelor"=>4, "Lecturer > Senior Lecturer"=>1, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>2, "Biochemistry, Genetics and Molecular Biology"=>4, "Mathematics"=>1, "Agricultural and Biological Sciences"=>23, "Medicine and Dentistry"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>6, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>6}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>23}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>4}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2043418"], "description"=>"<p>Bars indicate intracellular counts of lipid X and lipid A disaccharide at the end of a single cell generation from preliminary model results. The model used the scheme shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.g002\" target=\"_blank\">Fig 2</a> and parameters listed in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.t001\" target=\"_blank\">Table 1</a>, with the exceptions: the FtsH count was set to zero, the LpxC and WaaA counts were set to their steady-state levels in the absence of FtsH degradation (1540 and 978, respectively), and all metabolites were started with zero molecules. Although not shown here, the lipid X count had stabilised at a constant level, while the lipid A disaccharide count was increasing at a constant rate of 924 molecules/s.</p>", "links"=>[], "tags"=>["Escherichia coli Lipid", "enzyme", "lps", "pathway substrate concentrations", "LpxK overexpression results", "LpxC degradation signal", "cell generation times", "kdo", "flux control coefficients", "Complete Pathway Model", "pathway regulation", "production rate", "model"], "article_id"=>1397260, "categories"=>["Biological Sciences"], "users"=>["Akintunde Emiola", "John George", "Steven S. Andrews"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0121216.g003", "stats"=>{"downloads"=>0, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lipid_A_disaccharide_accumulation_/1397260", "title"=>"Lipid A disaccharide accumulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-28 03:32:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/2043426", "https://ndownloader.figshare.com/files/2043427"], "description"=>"<div><p>Lipid A is a highly conserved component of lipopolysaccharide (LPS), itself a major component of the outer membrane of Gram-negative bacteria. Lipid A is essential to cells and elicits a strong immune response from humans and other animals. We developed a quantitative model of the nine enzyme-catalyzed steps of <i>Escherichia coli</i> lipid A biosynthesis, drawing parameters from the experimental literature. This model accounts for biosynthesis regulation, which occurs through regulated degradation of the LpxC and WaaA (also called KdtA) enzymes. The LpxC degradation signal appears to arise from the lipid A disaccharide concentration, which we deduced from prior results, model results, and new LpxK overexpression results. The model agrees reasonably well with many experimental findings, including the lipid A production rate, the behaviors of mutants with defective LpxA enzymes, correlations between LpxC half-lives and cell generation times, and the effects of LpxK overexpression on LpxC concentrations. Its predictions also differ from some experimental results, which suggest modifications to the current understanding of the lipid A pathway, such as the possibility that LpxD can replace LpxA and that there may be metabolic channeling between LpxH and LpxB. The model shows that WaaA regulation may serve to regulate the lipid A production rate when the 3-deoxy-D-<i>manno</i>-oct-2-ulosonic acid (KDO) concentration is low and/or to control the number of KDO residues that get attached to lipid A. Computation of flux control coefficients showed that LpxC is the rate-limiting enzyme if pathway regulation is ignored, but that LpxK is the rate-limiting enzyme if pathway regulation is present, as it is in real cells. Control also shifts to other enzymes if the pathway substrate concentrations are not in excess. Based on these results, we suggest that LpxK may be a much better drug target than LpxC, which has been pursued most often.</p></div>", "links"=>[], "tags"=>["Escherichia coli Lipid", "enzyme", "lps", "pathway substrate concentrations", "LpxK overexpression results", "LpxC degradation signal", "cell generation times", "kdo", "flux control coefficients", "Complete Pathway Model", "pathway regulation", "production rate", "model"], "article_id"=>1397268, "categories"=>["Biological Sciences"], "users"=>["Akintunde Emiola", "John George", "Steven S. Andrews"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0121216.s001", "https://dx.doi.org/10.1371/journal.pone.0121216.s002"], "stats"=>{"downloads"=>0, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Complete_Pathway_Model_for_Lipid_A_Biosynthesis_in_Escherichia_coli_/1397268", "title"=>"A Complete Pathway Model for Lipid A Biosynthesis in <i>Escherichia coli</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-04-28 03:32:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/2043423"], "description"=>"<p>(A) Black bars show enzyme control coefficients for the open-loop case, in which wild-type enzyme counts were assumed but FtsH regulation was disabled. Red bars show enzyme control coefficients for the closed-loop case, in which FtsH regulation was enabled. (B) Enzyme abundance reductions that led the model to produce 0.5 million lipid A molecules per cell generation for the open-loop (black bars) and closed-loop (red bars) cases.</p>", "links"=>[], "tags"=>["Escherichia coli Lipid", "enzyme", "lps", "pathway substrate concentrations", "LpxK overexpression results", "LpxC degradation signal", "cell generation times", "kdo", "flux control coefficients", "Complete Pathway Model", "pathway regulation", "production rate", "model"], "article_id"=>1397265, "categories"=>["Biological Sciences"], "users"=>["Akintunde Emiola", "John George", "Steven S. Andrews"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0121216.g006", "stats"=>{"downloads"=>0, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sensitivity_of_lipid_A_production_rate_on_enzyme_abundance_/1397265", "title"=>"Sensitivity of lipid A production rate on enzyme abundance.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-28 03:32:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/2043421"], "description"=>"<p>(A) Effect of CHIR-090 antibiotic on lipid A production. The model (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.g002\" target=\"_blank\">Fig 2</a> plus <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.e007\" target=\"_blank\">Eq 7</a>) was started with all metabolites at their steady-state concentrations without CHIR-090. Then, antibiotic was added and the total amount of lipid A produced over the following 30 minutes was quantified, shown with the solid black line. The free antibiotic concentration, quantified as the average number of uncomplexed CHIR-090 molecules/cell, was kept constant. The black dashed line shows our estimate of the MIC for the intracellular antibiotic concentration and the red dashed line shows the antibiotic inhibition constant <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref009\" target=\"_blank\">9</a>]</b>. (B) Correlation between LpxC half-life and cell generation time. The experimental data (red circles) are from Schäkermann et al. <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref014\" target=\"_blank\">14</a>]</b>, who varied generation times using different growth conditions and then quantified LpxC half-lives. The model data (black diamonds) were collected by varying the LpxC half-lives (and LpxC <i>kcat</i>) and then quantifying the generation times, defined here as the time required to produce 1 million lipid A molecules. Lines are least-difference best-fits to the data using the function <i>y</i> = <i>c</i><sub>1</sub>/<i>x</i> + <i>c</i><sub>2</sub>, primarily to guide the eye. (C) Effect of overexpressing LpxC on the LpxC half-life (black curve, left axis) and on the lipid A production rate, measured relative to the wild-type production rate (blue curve, right axis). The dashed line shows the wild-type condition using the LpxC translation rate from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.t001\" target=\"_blank\">Table 1</a>.</p>", "links"=>[], "tags"=>["Escherichia coli Lipid", "enzyme", "lps", "pathway substrate concentrations", "LpxK overexpression results", "LpxC degradation signal", "cell generation times", "kdo", "flux control coefficients", "Complete Pathway Model", "pathway regulation", "production rate", "model"], "article_id"=>1397263, "categories"=>["Biological Sciences"], "users"=>["Akintunde Emiola", "John George", "Steven S. Andrews"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0121216.g004", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_model_with_experiment_/1397263", "title"=>"Comparison of model with experiment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-28 03:32:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/2043422"], "description"=>"<p>(A) Lower row shows LpxK bands on an SDS-PAGE gel, arising from overexpression induced with the amount of IPTG shown at the top of each column. The upper row shows the resultant LpxC bands on a Western blot for the same induction levels. (B) Model prediction of LpxC overexpression arising from LpxK overexpression. The model was that shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.g002\" target=\"_blank\">Fig 2</a> but with different LpxK enzyme counts, at steady-state.</p>", "links"=>[], "tags"=>["Escherichia coli Lipid", "enzyme", "lps", "pathway substrate concentrations", "LpxK overexpression results", "LpxC degradation signal", "cell generation times", "kdo", "flux control coefficients", "Complete Pathway Model", "pathway regulation", "production rate", "model"], "article_id"=>1397264, "categories"=>["Biological Sciences"], "users"=>["Akintunde Emiola", "John George", "Steven S. Andrews"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0121216.g005", "stats"=>{"downloads"=>0, "page_views"=>54, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overexpression_of_LpxK_increases_LpxC_concentration_/1397264", "title"=>"Overexpression of LpxK increases LpxC concentration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-28 03:32:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/2043417"], "description"=>"<p>Enzymes and metabolites are shown with three text styles: upright bold indicates that these concentrations are fixed, upright plain indicates that these concentrations vary, and italics indicates that these species are not included in the model explicitly. Black arrows with barbed heads represent chemical reactions in which reactants are converted to products. Red arrows with closed heads represent enzymatic influences on chemical reaction rates, and red arrows with T-bar heads represent inhibitory influences. Variables represent model parameters. Numbers next to black arrows for bi-substrate reactions show which substrate is designated number 1 and number 2.</p>", "links"=>[], "tags"=>["Escherichia coli Lipid", "enzyme", "lps", "pathway substrate concentrations", "LpxK overexpression results", "LpxC degradation signal", "cell generation times", "kdo", "flux control coefficients", "Complete Pathway Model", "pathway regulation", "production rate", "model"], "article_id"=>1397259, "categories"=>["Biological Sciences"], "users"=>["Akintunde Emiola", "John George", "Steven S. Andrews"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0121216.g002", "stats"=>{"downloads"=>3, "page_views"=>32, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_of_the_E_coli_KDO_2_lipid_A_biosynthesis_pathway_/1397259", "title"=>"Model of the <i>E</i>. <i>coli</i> KDO<sub>2</sub>-lipid A biosynthesis pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-28 03:32:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/2043416"], "description"=>"<p>The top two sugars are KDO groups, which are part of the core oligosaccharide, while the remainder of the structure represents lipid A.</p>", "links"=>[], "tags"=>["Escherichia coli Lipid", "enzyme", "lps", "pathway substrate concentrations", "LpxK overexpression results", "LpxC degradation signal", "cell generation times", "kdo", "flux control coefficients", "Complete Pathway Model", "pathway regulation", "production rate", "model"], "article_id"=>1397258, "categories"=>["Biological Sciences"], "users"=>["Akintunde Emiola", "John George", "Steven S. Andrews"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0121216.g001", "stats"=>{"downloads"=>0, "page_views"=>32, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structure_of_KDO_2_lipid_A_/1397258", "title"=>"Structure of KDO<sub>2</sub>-lipid A.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-28 03:32:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/2043425"], "description"=>"<p>These values are for <i>E</i>. <i>coli</i> cells in rich media. Location abbreviations are: cyto. for cytoplasm, p.m. for peripheral membrane, and i.m. for integral membrane (locations are not part of the model). Data estimation methods are presented in the main text. Data are from: (a) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref062\" target=\"_blank\">62</a>]</b>, (b) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref013\" target=\"_blank\">13</a>]</b>, (c) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref033\" target=\"_blank\">33</a>]</b>, (d) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref063\" target=\"_blank\">63</a>]</b>, (e) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref041\" target=\"_blank\">41</a>]</b>, (f) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref076\" target=\"_blank\">76</a>]</b>, (g) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref094\" target=\"_blank\">94</a>]</b>, (h) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref032\" target=\"_blank\">32</a>]</b>, (i) <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.g005\" target=\"_blank\">Fig 5</a> in <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref035\" target=\"_blank\">35</a>]</b>, (j) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref040\" target=\"_blank\">40</a>]</b>, (k) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref095\" target=\"_blank\">95</a>]</b>, (l) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref096\" target=\"_blank\">96</a>]</b>, (m) <b>[<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.ref027\" target=\"_blank\">27</a>]</b>. Parameters that do not have citations are discussed in the main text.</p><p>Abundance and kinetic parameters of lipid A biosynthesis model.</p>", "links"=>[], "tags"=>["Escherichia coli Lipid", "enzyme", "lps", "pathway substrate concentrations", "LpxK overexpression results", "LpxC degradation signal", "cell generation times", "kdo", "flux control coefficients", "Complete Pathway Model", "pathway regulation", "production rate", "model"], "article_id"=>1397267, "categories"=>["Biological Sciences"], "users"=>["Akintunde Emiola", "John George", "Steven S. Andrews"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0121216.t001", "stats"=>{"downloads"=>3, "page_views"=>33, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Abundance_and_kinetic_parameters_of_lipid_A_biosynthesis_model_/1397267", "title"=>"Abundance and kinetic parameters of lipid A biosynthesis model.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-04-28 03:32:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/2043424"], "description"=>"<p>(A) The flux control coefficient of WaaA as a function of the CMP-KDO substrate concentration. This is for the open-loop case, in which wild-type enzyme counts were assumed but FtsH regulation was disabled. (B) The ratio of alternate lipid A to normal lipid A (KDO<sub>2</sub>-lipid A) as a function of the number of WaaA proteins. All parameters are the same as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.t001\" target=\"_blank\">Table 1</a>, except that the WaaA proteolysis rate constant was changed in order to alter the WaaA degradation rate and hence the WaaA steady-state copy number. The maximum enzyme count shown arose from no FtsH mediated proteolysis. The dashed line indicates the wild-type count, from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0121216#pone.0121216.t001\" target=\"_blank\">Table 1</a>.</p>", "links"=>[], "tags"=>["Escherichia coli Lipid", "enzyme", "lps", "pathway substrate concentrations", "LpxK overexpression results", "LpxC degradation signal", "cell generation times", "kdo", "flux control coefficients", "Complete Pathway Model", "pathway regulation", "production rate", "model"], "article_id"=>1397266, "categories"=>["Biological Sciences"], "users"=>["Akintunde Emiola", "John George", "Steven S. Andrews"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0121216.g007", "stats"=>{"downloads"=>0, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_WaaA_regulation_/1397266", "title"=>"WaaA regulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-28 03:32:04"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"31", "full-text"=>"26", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"13", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"19", "full-text"=>"23", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"21", "full-text"=>"21", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"16", "full-text"=>"18", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"30", "full-text"=>"36", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"27", "full-text"=>"26", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"17", "full-text"=>"19", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"17", "full-text"=>"22", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"22", "full-text"=>"19", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"17", "full-text"=>"16", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"20", "full-text"=>"17", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"28", "full-text"=>"33", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"14", "supp-data"=>"3", "cited-by"=>"1", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"23", "full-text"=>"21", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"15", "full-text"=>"14", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}

Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[]}
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