Conformational Sampling and Nucleotide-Dependent Transitions of the GroEL Subunit Probed by Unbiased Molecular Dynamics Simulations
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{"title"=>"Conformational sampling and nucleotide-dependent transitions of the GroEL subunit probed by unbiased molecular dynamics simulations", "type"=>"journal", "authors"=>[{"first_name"=>"Lars", "last_name"=>"Skjaerven", "scopus_author_id"=>"19640261400"}, {"first_name"=>"Barry", "last_name"=>"Grant", "scopus_author_id"=>"9843571900"}, {"first_name"=>"Arturo", "last_name"=>"Muga", "scopus_author_id"=>"7003622015"}, {"first_name"=>"Knut", "last_name"=>"Teigen", "scopus_author_id"=>"7004913990"}, {"first_name"=>"J. Andrew", "last_name"=>"McCammon", "scopus_author_id"=>"36050413200"}, {"first_name"=>"Nathalie", "last_name"=>"Reuter", "scopus_author_id"=>"6701534466"}, {"first_name"=>"Aurora", "last_name"=>"Martinez", "scopus_author_id"=>"7404025564"}], "year"=>2011, "source"=>"PLoS Computational Biology", "identifiers"=>{"issn"=>"1553734X", "arxiv"=>"PMC3053311", "scopus"=>"2-s2.0-79953645137", "sgr"=>"79953645137", "pui"=>"361550337", "isbn"=>"1553-7358 (Electronic)\\r1553-734X (Linking)", "pmid"=>"21423709", "doi"=>"10.1371/journal.pcbi.1002004"}, "id"=>"79cbaf36-8594-3133-9f9f-737cdc5793ca", "abstract"=>"GroEL is an ATP dependent molecular chaperone that promotes the folding of a large number of substrate proteins in E. coli. Large-scale conformational transitions occurring during the reaction cycle have been characterized from extensive crystallographic studies. However, the link between the observed conformations and the mechanisms involved in the allosteric response to ATP and the nucleotide-driven reaction cycle are not completely established. Here we describe extensive (in total long) unbiased molecular dynamics (MD) simulations that probe the response of GroEL subunits to ATP binding. We observe nucleotide dependent conformational transitions, and show with multiple 100 ns long simulations that the ligand-induced shift in the conformational populations are intrinsically coded in the structure-dynamics relationship of the protein subunit. Thus, these simulations reveal a stabilization of the equatorial domain upon nucleotide binding and a concomitant \"opening\" of the subunit, which reaches a conformation close to that observed in the crystal structure of the subunits within the ADP-bound oligomer. Moreover, we identify changes in a set of unique intrasubunit interactions potentially important for the conformational transition.", "link"=>"http://www.mendeley.com/research/conformational-sampling-nucleotidedependent-transitions-groel-subunit-probed-unbiased-molecular-dyna", "reader_count"=>65, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Librarian"=>2, "Researcher"=>25, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>23, "Student > Postgraduate"=>1, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Librarian"=>2, "Researcher"=>25, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>23, "Student > Postgraduate"=>1, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>32, "Physics and Astronomy"=>5, "Chemistry"=>13, "Social Sciences"=>1, "Computer Science"=>3}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>13}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>32}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Sweden"=>1, "United States"=>4, "Norway"=>5, "United Kingdom"=>1, "Italy"=>1, "France"=>1, "India"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/791568"], "description"=>"<p>(A) Experimentally obtained structures projected onto the two first principal components (PC). The inset shows the eigenvalue spectrum representing the percentage of the total variance captured by the corresponding eigenvector. Labels besides each point indicate the cumulative sum of the total variance accounted for in all lower number eigenvectors. (B) Visualization of PC1 of the X-ray structures, which consists of a downward tilt and rotation of the apical domain, along with a downward tilt of helix M in the intermediate domain. Internal helix motion is also observed within the equatorial domain along with flapping loop motion (residues 36-51).</p>", "links"=>[], "tags"=>["287", "groel"], "article_id"=>461933, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PCA_of_287_GroEL_subunits_/461933", "title"=>"PCA of 287 GroEL subunits.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:32:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/792615"], "description"=>"<p>The average difference in distance () is shown for each of the three calculations; between X-ray <b>t</b> and <b>r″</b> (column 1), MD simulations of <b>t</b> with and without ATP (column 2), and X-ray <b>t</b> and ATP bound <b>t</b> conformers (column 3). Negative values (above mid rule) depict interactions present (or closer) in the nucleotide free state (unliganded), while positive values (below mid rule) depict interactions closer in the nucleotide bound state.</p>", "links"=>[], "tags"=>["atomic", "interactions", "nucleotide", "binding", "x-ray", "structures", "md"], "article_id"=>462971, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.t002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differential_atomic_interactions_upon_nucleotide_binding_obtained_from_X_ray_structures_and_MD_simulations_/462971", "title"=>"Differential atomic interactions upon nucleotide binding obtained from X-ray structures and MD simulations.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-03-10 00:49:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/791918"], "description"=>"<p>Black bars show the RMSF values obtained from the ATP bound simulations, while red dots represent the unbound simulations. Binding site residues are depicted green, while residues that yield a significant change () between ATP-bound and ATP-free simulations are depicted with blue squares. Residues of particular interest are labeled. RMSF values are shown for the equatorial domain (residues 2-133 (A), 409-525 (B)). Secondary structure elements are indicated schematically with helices in black and strands in gray.</p>", "links"=>[], "tags"=>["fluctuations", "unbound", "atp", "bound"], "article_id"=>462281, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Residual_fluctuations_of_the_closed_unbound_and_ATP_bound_simulations_/462281", "title"=>"Residual fluctuations of the closed unbound and ATP bound simulations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:38:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/792036"], "description"=>"<p>Hydrogen bond donors and acceptors are labeled below the bars in which the height represents the occupancy in % of the simulation time. Each bar depicts the occupancy of one H-bond in one of the 6 ATP-bound simulations (simulations K-P in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002004#pcbi-1002004-g002\" target=\"_blank\">Figure 2</a>).</p>", "links"=>[], "tags"=>["hydrogen", "bonds"], "article_id"=>462406, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.g005", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_representation_of_potential_hydrogen_bonds_between_protein_and_nucleotide_/462406", "title"=>"Schematic representation of potential hydrogen bonds between protein and nucleotide.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:40:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/792368"], "description"=>"<p>X-ray structures of <b>t</b> and <b>r″</b> are shown in green and cyan colors, respectively. (A) shows the opposite side of the binding site where nucleotide binding increases the distance between Leu134 and Asn475. The closer contact between Lys34 and Glu483 brought about by nucleotide binding is shown in (B). ADP is shown in stick and surface representation.</p>", "links"=>[], "tags"=>["conformational", "changes", "equatorial", "nucleotide"], "article_id"=>462735, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.g008", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Local_conformational_changes_in_the_equatorial_domain_upon_nucleotide_binding_/462735", "title"=>"Local conformational changes in the equatorial domain upon nucleotide binding.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:45:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/792462"], "description"=>"<p>(A) Cross-correlation map of the closed ATP bound simulation reveals residues that fluctuate in the same direction at the same time. The color scale runs from pink (anticorrelated motions) to blue (correlated motions). Red circles mark areas that are consistently found as correlated over all sets of 10 ns intervals of the trajectory. Secondary structure elements are indicated schematically with helices in black and strands in gray. (B) Mapping of the correlated residues onto the GroEL equatorial domain. Red lines link two correlated residues. ATP is colored blue.</p>", "links"=>[], "tags"=>["correlated", "motions", "equatorial"], "article_id"=>462832, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.g009", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Residue_correlated_motions_of_the_equatorial_domain_/462832", "title"=>"Residue correlated motions of the equatorial domain.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:47:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/791679"], "description"=>"<p>Projection of X-ray (contoured grey dots) and MD (blue) structures onto the two most significant principal planes defined by 287 GroEL experimentally obtained structures. The 300 ns simulations are shown in the first row of panels, while the 100 ns simulations are shown in rows 2–4. The distribution of MD structures is depicted with density shaded blue points. Light grey dots represent the first 50 ns of the 100 ns simulations. Orange, red, and green dots represent the closed (<b>t</b>), semi-relaxed (<b>r</b>), and open (<b>r″</b>) X-ray structures, respectively. The conformer plots show a two dimensional representation of the conformational sampling in terms of conformational difference as described by the PC's.</p>", "links"=>[], "tags"=>["plots", "x-ray", "md", "structures", "nucleotide", "conformational"], "article_id"=>462040, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conformer_plots_of_X_ray_and_MD_structures_reveal_the_nucleotide_dependent_conformational_sampling_/462040", "title"=>"Conformer plots of X-ray and MD structures reveal the nucleotide dependent conformational sampling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:34:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/792530"], "description"=>"<p>The RMSd values between the closed and open X-ray structures and the average conformations in each of the clusters in the four simulations of the GroEL subunit are shown. The RMSd between the open and closed X-ray structure (PDB ids: 1SVT and 1XCK, respectively) is 12.30 Å.</p>", "links"=>[], "tags"=>["md", "trajectories", "groel"], "article_id"=>462894, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.t001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Clustering_analysis_of_MD_trajectories_of_the_GroEL_subunit_/462894", "title"=>"Clustering analysis of MD trajectories of the GroEL subunit.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-03-10 00:48:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/396371", "https://ndownloader.figshare.com/files/396390", "https://ndownloader.figshare.com/files/396420", "https://ndownloader.figshare.com/files/396456", "https://ndownloader.figshare.com/files/396487"], "description"=>"<div><p>GroEL is an ATP dependent molecular chaperone that promotes the folding of a large number of substrate proteins in <em>E. coli</em>. Large-scale conformational transitions occurring during the reaction cycle have been characterized from extensive crystallographic studies. However, the link between the observed conformations and the mechanisms involved in the allosteric response to ATP and the nucleotide-driven reaction cycle are not completely established. Here we describe extensive (in total long) unbiased molecular dynamics (MD) simulations that probe the response of GroEL subunits to ATP binding. We observe nucleotide dependent conformational transitions, and show with multiple 100 ns long simulations that the ligand-induced shift in the conformational populations are intrinsically coded in the structure-dynamics relationship of the protein subunit. Thus, these simulations reveal a stabilization of the equatorial domain upon nucleotide binding and a concomitant “opening” of the subunit, which reaches a conformation close to that observed in the crystal structure of the subunits within the ADP-bound oligomer. Moreover, we identify changes in a set of unique intrasubunit interactions potentially important for the conformational transition.</p> </div>", "links"=>[], "tags"=>["conformational", "sampling", "nucleotide-dependent", "transitions", "groel", "subunit", "probed", "unbiased", "molecular", "simulations"], "article_id"=>138300, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002004.s001", "https://dx.doi.org/10.1371/journal.pcbi.1002004.s002", "https://dx.doi.org/10.1371/journal.pcbi.1002004.s003", "https://dx.doi.org/10.1371/journal.pcbi.1002004.s004", "https://dx.doi.org/10.1371/journal.pcbi.1002004.s005"], "stats"=>{"downloads"=>10, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Conformational_Sampling_and_Nucleotide_Dependent_Transitions_of_the_GroEL_Subunit_Probed_by_Unbiased_Molecular_Dynamics_Simulations/138300", "title"=>"Conformational Sampling and Nucleotide-Dependent Transitions of the GroEL Subunit Probed by Unbiased Molecular Dynamics Simulations", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-03-10 02:18:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/792248"], "description"=>"<p>The differences in side chain contacts are mapped for the MD conformers. Two residues are assumed to be in contact if the minimal distance between them . Only contacts existing in at least half of the structures are considered. Green triangles represent contacts present in the unliganded forms and not in the liganded forms. While blue dots represents contacts which are present in the liganded forms, but not in the unliganded forms. Red circles depict contacts which are found in both the X-ray and MD analysis. Secondary structure elements are indicated schematically with helices in black and strands in gray.</p>", "links"=>[], "tags"=>["atp-bound", "unliganded", "md"], "article_id"=>462617, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.g007", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Difference_contact_map_between_ATP_bound_and_unliganded_MD_simulations_/462617", "title"=>"Difference contact map between ATP-bound and unliganded MD simulations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:43:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/792572"], "description"=>"<p>See <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002004#pcbi-1002004-t002\" target=\"_blank\">Table 2</a> for legend.</p>", "links"=>[], "tags"=>["atomic", "interactions", "stabilization", "equatorial"], "article_id"=>462936, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.t003", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differential_atomic_interactions_potentially_involved_in_the_stabilization_of_the_equatorial_domain_/462936", "title"=>"Differential atomic interactions potentially involved in the stabilization of the equatorial domain.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-03-10 00:48:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/791801"], "description"=>"<p>Black line corresponds to the RMSd with respect to the starting structure (<b>t</b> for A+C, and <b>r″</b> for B+D), while the grey line corresponds the RMSd with respect to the opposite form (<b>r″</b> for A+C, and <b>t</b> for B+D). Each plot corresponds to one specific MD simulation; (A) closed (<b>t</b>) unbound, (B) open (<b>r″</b>) unbound, (C) closed (<b>t</b>) ATP bound, and (D) open (<b>r″</b>) ADP bound. Black dashed line depicts the RMSd value between the open (<b>r″</b>) and closed (<b>t</b>) X-ray structure. Clustering analysis is performed on each of the 4 simulations, and the bar on the top of each RMSd plot is colored according to which cluster the corresponding frame belongs to.</p>", "links"=>[], "tags"=>["300", "ns", "simulations", "groel"], "article_id"=>462166, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.g003", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RMSd_variation_for_the_300_ns_long_simulations_of_the_GroEL_subunit_/462166", "title"=>"RMSd variation for the 300 ns long simulations of the GroEL subunit.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:36:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/792129"], "description"=>"<p>Configurational entropy of the equatorial domain (A) and the whole subunit (B) with respect to the simulation length. The calculation is based upon the 100 ns long simulations of the closed GroEL subunit; unbound (black), and ATP-bound (red).</p>", "links"=>[], "tags"=>["Computational biology", "Biochemistry"], "article_id"=>462497, "categories"=>["Biological Sciences", "Biochemistry"], "users"=>["Lars Skjaerven", "Barry Grant", "Arturo Muga", "Knut Teigen", "J. Andrew McCammon", "Nathalie Reuter", "Aurora Martinez"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002004.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Configurational_entropy_/462497", "title"=>"Configurational entropy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:41:37"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
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  • {"unique-ip"=>"2", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
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  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
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  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"3", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
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  • {"unique-ip"=>"1", "full-text"=>"0", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"1", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"2", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"2", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"3", "full-text"=>"3", "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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  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
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  • {"unique-ip"=>"7", "full-text"=>"4", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"4", "full-text"=>"1", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}

Relative Metric

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