Anthrax Toxin Receptor Drives Protective Antigen Oligomerization and Stabilizes the Heptameric and Octameric Oligomer by a Similar Mechanism
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{"title"=>"Anthrax toxin receptor drives protective antigen oligomerization and stabilizes the heptameric and octameric oligomer by a similar mechanism", "type"=>"journal", "authors"=>[{"first_name"=>"Alexander F.", "last_name"=>"Kintzer", "scopus_author_id"=>"30267724400"}, {"first_name"=>"Harry J.", "last_name"=>"Sterling", "scopus_author_id"=>"7004511248"}, {"first_name"=>"Iok I.", "last_name"=>"Tang", "scopus_author_id"=>"35216602300"}, {"first_name"=>"Evan R.", "last_name"=>"Williams", "scopus_author_id"=>"7403996224"}, {"first_name"=>"Bryan A.", "last_name"=>"Krantz", "scopus_author_id"=>"6701610818"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-78149476014", "doi"=>"10.1371/journal.pone.0013888", "pui"=>"359941851", "issn"=>"19326203", "pmid"=>"21079738", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "sgr"=>"78149476014"}, "id"=>"2a1eb217-89e5-392c-8153-377d1c1b0091", "abstract"=>"BACKGROUND: Anthrax toxin is comprised of protective antigen (PA), lethal factor (LF), and edema factor (EF). These proteins are individually nontoxic; however, when PA assembles with LF and EF, it produces lethal toxin and edema toxin, respectively. Assembly occurs either on cell surfaces or in plasma. In each milieu, PA assembles into a mixture of heptameric and octameric complexes that bind LF and EF. While octameric PA is the predominant form identified in plasma under physiological conditions (pH 7.4, 37°C), heptameric PA is more prevalent on cell surfaces. The difference between these two environments is that the anthrax toxin receptor (ANTXR) binds to PA on cell surfaces. It is known that the extracellular ANTXR domain serves to stabilize toxin complexes containing the PA heptamer by preventing premature PA channel formation--a process that inactivates the toxin. The role of ANTXR in PA oligomerization and in the stabilization of toxin complexes containing octameric PA are not understood.\\n\\nMETHODOLOGY: Using a fluorescence assembly assay, we show that the extracellular ANTXR domain drives PA oligomerization. Moreover, a dimeric ANTXR construct increases the extent of and accelerates the rate of PA assembly relative to a monomeric ANTXR construct. Mass spectrometry analysis shows that heptameric and octameric PA oligomers bind a full stoichiometric complement of ANTXR domains. Electron microscopy and circular dichroism studies reveal that the two different PA oligomers are equally stabilized by ANTXR interactions.\\n\\nCONCLUSIONS: We propose that PA oligomerization is driven by dimeric ANTXR complexes on cell surfaces. Through their interaction with the ANTXR, toxin complexes containing heptameric and octameric PA oligomers are similarly stabilized. Considering both the relative instability of the PA heptamer and extracellular assembly pathway identified in plasma, we propose a means to regulate the development of toxin gradients around sites of infection during anthrax pathogenesis.", "link"=>"http://www.mendeley.com/research/anthrax-toxin-receptor-drives-protective-antigen-oligomerization-stabilizes-heptameric-octameric-oli", "reader_count"=>19, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>2, "Student > Master"=>1, "Student > Bachelor"=>1, "Professor"=>1, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>2, "Student > Master"=>1, "Student > Bachelor"=>1, "Professor"=>1, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>7, "Medicine and Dentistry"=>1, "Neuroscience"=>1, "Chemistry"=>4, "Unspecified"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>7}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/819931"], "description"=>"<p>(<b>A</b>) Representative micrographs (49,000×) of PA-msANTXR2 complexes following a 5-minute exposure to 37°C at either pH 8.0 (left) or pH 5.0 (right). A 20-nm scale bar is shown in white for either micrograph. (inset on left) Class-average images of PA<sub>7</sub>-msANTXR2 and PA<sub>8</sub>-msANTXR2 complexes; a 5-nm scale bar is shown. (<b>B</b>) Quantitative analysis of the number of soluble PA oligomers and the relative proportions of PA<sub>7</sub> and PA<sub>8</sub>, identified from electron micrographs at each pH. (left) A plot of the average number of soluble prechannels versus pH for both free PA complexes (□, data taken from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Kintzer2\" target=\"_blank\">[22]</a>) and msANTXR2-bound PA complexes (▪) complexes. Error bars are propagated from the standard deviations of the mean number of particles obtained from at least 10 micrographs for each pH. (right) A plot of the relative proportions of PA<sub>7</sub> (black ▪) and PA<sub>8</sub> (red •) complexes determined using class-average image analysis for both PA-LF<sub>N</sub> (open symbols, data taken from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Kintzer2\" target=\"_blank\">[22]</a>) and PA-LF<sub>N</sub>-msANTXR2 (filled symbols) complexes.</p>", "links"=>[], "tags"=>["complexes", "ph"], "article_id"=>490304, "categories"=>["Microbiology", "Biophysics"], "users"=>["Alexander F. Kintzer", "Harry J. Sterling", "Iok I. Tang", "Evan R. Williams", "Bryan A. Krantz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0013888.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_EM_analysis_of_the_stability_of_PA_7_msANTXR2_and_PA_8_msANTXR2_complexes_from_pH_8_0_to_5_0_/490304", "title"=>"EM analysis of the stability of PA<sub>7</sub>-msANTXR2 and PA<sub>8</sub>-msANTXR2 complexes from pH 8.0 to 5.0.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:29:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/820316"], "description"=>"a<p>Molecular masses are measured using nanoelectrospray MS according to the method described in Kintzer et al. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Kintzer1\" target=\"_blank\">[21]</a>.</p>b<p>Theoretical molecular masses are derived using the amino acid sequences of msANTXR, PA<sub>63</sub>, and LF<sub>N</sub>.</p>", "links"=>[], "tags"=>["molecular", "masses"], "article_id"=>490687, "categories"=>["Microbiology", "Biophysics"], "users"=>["Alexander F. Kintzer", "Harry J. Sterling", "Iok I. Tang", "Evan R. Williams", "Bryan A. Krantz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0013888.t001", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Measured_a_and_theoretical_b_molecular_masses_for_msANTXR_PA_LF_N_complexes_/490687", "title"=>"Measured<sup>a</sup> and theoretical<sup>b</sup> molecular masses for msANTXR-PA-LF<sub>N</sub> complexes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 22:31:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/820355"], "description"=>"a<p>Negative-stain electron micrographs using uranyl acetate stain, 2%.</p>b<p>A pre-assembled population of PA-msANTXR2 complexes (containing 78% PA<sub>7</sub> and 22% PA<sub>8</sub>) was incubated for 5 minutes at 37°C at the specified pH.</p>c<p>The mean number of particles per micrograph (<i>n</i> of 10 micrographs) given as ±s.d.</p>d<p>Oligomeric composition is determined using crystal-structure-referenced alignment and classification analysis <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Kintzer1\" target=\"_blank\">[21]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Kintzer2\" target=\"_blank\">[22]</a>. The percentage reported is computed from the total number of particles, <i>N</i>, comprising all PA<sub>7</sub> and PA<sub>8</sub> classes, where oligomeric composition is equal to the total number of PA<sub>7</sub> or PA<sub>8</sub> particles divided by <i>N</i>.</p>e<p>n.d., not determined. Class-average image analyses of these pH conditions are not shown due to the low particle counts observed. The low particle counts are attributed to severe aggregation (as shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone-0013888-g003\" target=\"_blank\">Fig. 3A</a>).</p>", "links"=>[], "tags"=>["em", "pa-msantxr2", "co-complexes"], "article_id"=>490719, "categories"=>["Microbiology", "Biophysics"], "users"=>["Alexander F. Kintzer", "Harry J. Sterling", "Iok I. Tang", "Evan R. Williams", "Bryan A. Krantz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0013888.t002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Negative_stain_a_EM_analysis_PA_msANTXR2_co_complexes_following_an_exposure_at_37_C_b_/490719", "title"=>"Negative-stain<sup>a</sup> EM analysis PA-msANTXR2 co-complexes following an exposure at 37°C<sup>b</sup>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 22:31:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/819852"], "description"=>"<p>Nanoelectrospray MS of sANTXR-PA-LF<sub>N</sub> complexes (∼2 µM) in 200 mM ammonium acetate, 2 mM ammonium bicarbonate, 0.2 mM magnesium acetate, pH 7.8. The <i>y</i>-axis is scaled 10× in the range <i>m</i>/<i>z</i> 6000–13,000, and the <i>x</i>-axis is expanded in the range <i>m</i>/<i>z</i> 10,000–13,000 to aid viewing low relative abundance and closely spaced peaks in these regions. See also <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone-0013888-t001\" target=\"_blank\">Table 1</a> for the respective molecular mass values for each complex.</p>", "links"=>[], "tags"=>["spectrometry", "oligomer"], "article_id"=>490225, "categories"=>["Microbiology", "Biophysics"], "users"=>["Alexander F. Kintzer", "Harry J. Sterling", "Iok I. Tang", "Evan R. Williams", "Bryan A. Krantz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0013888.g002", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nanoelectrospray_mass_spectrometry_analysis_of_PA_LF_N_msANTXR2_oligomer_complexes_/490225", "title"=>"Nanoelectrospray mass spectrometry analysis of PA-LF<sub>N</sub>-msANTXR2 oligomer complexes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:29:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/820267"], "description"=>"<p>The assembly of LT complexes with different lifetimes may serve as a means to regulate toxin activity in plasma during infection. The reduced lifetime of PA<sub>7</sub> complexes in plasma may limit their cytotoxic effects to local areas in close proximity to the site of <i>B. anthracis</i> infection. By contrast, PA<sub>8</sub>, which is produced at lower levels, has a longer lifetime, thereby allowing it to exert cytotoxic effects over longer distances.</p>", "links"=>[], "tags"=>["toxin"], "article_id"=>490642, "categories"=>["Microbiology", "Biophysics"], "users"=>["Alexander F. Kintzer", "Harry J. Sterling", "Iok I. Tang", "Evan R. Williams", "Bryan A. Krantz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0013888.g007", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_model_for_the_regulation_of_toxin_activity_in_plasma_/490642", "title"=>"A model for the regulation of toxin activity in plasma.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:31:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/820180"], "description"=>"<p>A model for anthrax toxin assembly in plasma and at cells surfaces. (<b>A</b>) In principle, PA components may assemble into a 70∶30 PA<sub>7</sub>:PA<sub>8</sub> mixture of toxin complexes in plasma. However, PA<sub>7</sub> readily converts to the channel state and aggregates within 5 minutes under these conditions, leaving PA<sub>8</sub> as the predominant soluble toxin complex capable of infecting cells <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Kintzer2\" target=\"_blank\">[22]</a>. By contrast, both oligomeric forms are equally stable at the cell surface, where binding to ANTXR2 serves to prevent premature channel formation until PA<sub>7</sub> or PA<sub>8</sub> complexes are properly internalized and the endosomal compartment is acidified to pH values <6. On cell surfaces, PA may also oligomerize into a 70∶30 PA<sub>7</sub>:PA<sub>8</sub> mixture <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Kintzer1\" target=\"_blank\">[21]</a>, where assembly is driven through interactions with dimeric ANTXR complexes. These complexes are then able to bind LF and become internalized into cells.</p>", "links"=>[], "tags"=>["anthrax", "toxin"], "article_id"=>490550, "categories"=>["Microbiology", "Biophysics"], "users"=>["Alexander F. Kintzer", "Harry J. Sterling", "Iok I. Tang", "Evan R. Williams", "Bryan A. Krantz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0013888.g006", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_model_for_anthrax_toxin_assembly_/490550", "title"=>"A model for anthrax toxin assembly.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:30:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/819782"], "description"=>"<p>(<b>A</b>) A manually constructed model of dsANTXR2 bound to two adjacent PA<sub>63</sub> subunits in a PA<sub>7</sub> oligomer. The surface rendering is colored according to the legend on the right. The model is based upon the crystal structures of GST (PDB 5GST<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Ji1\" target=\"_blank\">[31]</a>) and PA<sub>7</sub>(msANTXR2)<sub>7</sub> (PDB 1TZN<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Lacy1\" target=\"_blank\">[17]</a>). A flexible linker is shown in black that links the carboxy-terminus of GST to the amino-terminus of msANTXR2. (<b>B</b>) FRET-probed PA-assembly kinetics at pH 7.4. A 1∶1 mixture of <sub>n</sub>PA K563C*AF<sub>555</sub> and <sub>n</sub>PA K563C*AF<sub>647</sub> monomers (100 nM total monomer) was either allowed to assemble on its own (black ▪) or mixed with 100 nM of the following assembly co-factors, dsANTXR2 (blue ▾), msANTXR2 (green ▴), or LF<sub>N</sub> (red •), and allowed to assemble. To track the time course of PA assembly, the ratio of acceptor to donor fluorescence (F<sub>668</sub>/F<sub>566</sub>) was measured every five minutes for one hour at room temperature. The resulting records are normalized to the largest signal obtained for the dsANTXR co-assembly reaction. Solid lines are best-fit lines obtained using a second-order rate model (Eq. 1). The rate constants, <i>k</i>, are 0.19 (±0.01) s<sup>−1</sup> for dsANTXR2, 0.031 (±0.003) s<sup>−1</sup> for LF<sub>N</sub>, and 0.05 (±0.03) s<sup>−1</sup> for msANTXR2, and the amplitudes, <i>A</i>, are −1.12 (±0.02) for dsANTXR2, −1.29 (±0.04) for LF<sub>N</sub>, and −0.15 (±0.02) for msANTXR2. Note due to the lack of an observable change in FRET signal, no kinetic parameters were obtained for the assembly of <sub>n</sub>PA alone, and the data were fit to a straight line.</p>", "links"=>[], "tags"=>["dimerization", "stimulates", "pa"], "article_id"=>490139, "categories"=>["Microbiology", "Biophysics"], "users"=>["Alexander F. Kintzer", "Harry J. Sterling", "Iok I. Tang", "Evan R. Williams", "Bryan A. Krantz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0013888.g001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ANTXR2_dimerization_stimulates_PA_assembly_/490139", "title"=>"ANTXR2 dimerization stimulates PA assembly.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:28:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/820121"], "description"=>"<p>SDS-resistance assays <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Miller1\" target=\"_blank\">[25]</a> were performed with PA<sub>7</sub>(LF<sub>N</sub>)<sub>3</sub>(msANTXR2)<sub>7</sub> complexes, which were incubated at the indicated pH at either 25°C or 37°C. The two species of interest on the SDS-PAGE gels are indicated as either the high-molecular-weight, SDS-resistant PA oligomer band (*) or low-molecular-weight SDS-soluble, PA<sub>63</sub> monomer band (PA<sub>63</sub>).</p>", "links"=>[], "tags"=>["sds-resistant", "complexes"], "article_id"=>490492, "categories"=>["Microbiology", "Biophysics"], "users"=>["Alexander F. Kintzer", "Harry J. Sterling", "Iok I. Tang", "Evan R. Williams", "Bryan A. Krantz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0013888.g005", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_formation_of_SDS_resistant_PA_7_LF_N_3_msANTXR2_7_complexes_is_temperature_independent_/490492", "title"=>"The formation of SDS-resistant PA<sub>7</sub>(LF<sub>N</sub>)<sub>3</sub>(msANTXR2)<sub>7</sub> complexes is temperature-independent.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:30:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/820040"], "description"=>"<p>(<b>A</b>) Time-course records of the CD signal at 222 nm (CD<sub>222</sub>) for either an acid pulse (pH 5.0 final, red trace) or a control with no pH pulse (pH 8.0 final, black trace). (<b>B</b>) The pH-dependence of the CD<sub>222</sub>-signal change for PA<sub>7</sub>(LF<sub>N</sub>)<sub>3</sub> (black □, data taken from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Kintzer2\" target=\"_blank\">[22]</a>), PA<sub>8</sub>(LF<sub>N</sub>)<sub>4</sub> (red ○, data taken from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013888#pone.0013888-Kintzer2\" target=\"_blank\">[22]</a>), PA<sub>7</sub>(LF<sub>N</sub>)<sub>3</sub>(msANTXR2)<sub>7</sub> (black ▪), PA<sub>8</sub>(LF<sub>N</sub>)<sub>3</sub>(msANTXR2)<sub>8</sub> (red •) complexes. Traces were normalized to the initial and final CD<sub>222</sub> signals obtained.</p>", "links"=>[], "tags"=>["ph", "dependence", "cd-signal", "changes"], "article_id"=>490399, "categories"=>["Microbiology", "Biophysics"], "users"=>["Alexander F. Kintzer", "Harry J. Sterling", "Iok I. Tang", "Evan R. Williams", "Bryan A. Krantz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0013888.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_pH_dependence_of_CD_signal_changes_for_PA_7_and_PA_8_msANTXR2_complexes_/490399", "title"=>"The pH dependence of CD-signal changes for PA<sub>7</sub>- and PA<sub>8</sub>-msANTXR2 complexes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:29:58"}

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  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
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  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
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  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
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Relative Metric

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