Inhibition of Type VI Secretion by an Anti-TssM Llama Nanobody
Publication Date
March 26, 2015
Journal
PLOS ONE
Authors
Van Son Nguyen, Laureen Logger, Silvia Spinelli, Aline Desmyter, et al
Volume
10
Issue
3
Pages
e0122187
DOI
https://dx.plos.org/10.1371/journal.pone.0122187
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0122187
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/25811612
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4374921
Europe PMC
http://europepmc.org/abstract/MED/25811612
Web of Science
000356353700174
Scopus
84926344008
Mendeley
http://www.mendeley.com/research/inhibition-type-vi-secretion-antitssm-llama-nanobody
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Mendeley | Further Information

{"title"=>"Inhibition of type VI secretion by an anti-TssM llama nanobody", "type"=>"journal", "authors"=>[{"first_name"=>"Van Son", "last_name"=>"Nguyen", "scopus_author_id"=>"56548025400"}, {"first_name"=>"Laureen", "last_name"=>"Logger", "scopus_author_id"=>"56041864700"}, {"first_name"=>"Silvia", "last_name"=>"Spinelli", "scopus_author_id"=>"7005124414"}, {"first_name"=>"Aline", "last_name"=>"Desmyter", "scopus_author_id"=>"6602069524"}, {"first_name"=>"Thi Thu Hang", "last_name"=>"Le", "scopus_author_id"=>"56548056700"}, {"first_name"=>"Christine", "last_name"=>"Kellenberger", "scopus_author_id"=>"56216907600"}, {"first_name"=>"Badreddine", "last_name"=>"Douzi", "scopus_author_id"=>"35091005400"}, {"first_name"=>"Eric", "last_name"=>"Durand", "scopus_author_id"=>"7005193843"}, {"first_name"=>"Alain", "last_name"=>"Roussel", "scopus_author_id"=>"7102748214"}, {"first_name"=>"Eric", "last_name"=>"Cascales", "scopus_author_id"=>"6603332760"}, {"first_name"=>"Christian", "last_name"=>"Cambillau", "scopus_author_id"=>"7006765066"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"doi"=>"10.1371/journal.pone.0122187", "pmid"=>"25811612", "issn"=>"19326203", "sgr"=>"84926344008", "scopus"=>"2-s2.0-84926344008", "pui"=>"603466554"}, "id"=>"fea53bde-5265-3c3b-ad32-0ea0eb89ce23", "abstract"=>"The type VI secretion system (T6SS) is a secretion pathway widespread in Gram-negative bacteria that targets toxins in both prokaryotic and eukaryotic cells. Although most T6SSs identified so far are involved in inter-bacterial competition, a few are directly required for full virulence of pathogens. The T6SS comprises 13 core proteins that assemble a large complex structurally and functionally similar to a phage contractile tail structure anchored to the cell envelope by a trans-membrane spanning stator. The central part of this stator, TssM, is a 1129-amino-acid protein anchored in the inner membrane that binds to the TssJ outer membrane lipoprotein. In this study, we have raised camelid antibodies against the purified TssM periplasmic domain. We report the crystal structure of two specific nanobodies that bind to TssM in the nanomolar range. Interestingly, the most potent nanobody, nb25, competes with the TssJ lipoprotein for TssM binding in vitro suggesting that TssJ and the nb25 CDR3 loop share the same TssM binding site or causes a steric hindrance preventing TssM-TssJ complex formation. Indeed, periplasmic production of the nanobodies displacing the TssM-TssJ interaction inhibits the T6SS function in vivo. This study illustrates the power of nanobodies to specifically target and inhibit bacterial secretion systems.", "link"=>"http://www.mendeley.com/research/inhibition-type-vi-secretion-antitssm-llama-nanobody", "reader_count"=>20, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Researcher"=>3, "Student > Ph. D. Student"=>6, "Other"=>1, "Student > Master"=>3, "Student > Bachelor"=>3, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Researcher"=>3, "Student > Ph. D. Student"=>6, "Other"=>1, "Student > Master"=>3, "Student > Bachelor"=>3, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>7, "Physics and Astronomy"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>7}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>2}}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1990958"], "description"=>"<p>Kinetic and thermodynamic parameters of the interactions between anti-TssM nanobodies with TssMp.</p>", "links"=>[], "tags"=>["TssM periplasmic domain", "membrane", "nb 25 CDR 3 loop share", "stator", "type VI secretion", "nanobodie", "phage contractile tail structure", "13 core proteins", "T 6SS", "tssj", "TssM binding site", "T 6SS function", "type VI secretion system", "lipoprotein"], "article_id"=>1357708, "categories"=>["Biological Sciences"], "users"=>["Van Son Nguyen", "Laureen Logger", "Silvia Spinelli", "Aline Desmyter", "Thi Thu Hang Le", "Christine Kellenberger", "Badreddine Douzi", "Eric Durand", "Alain Roussel", "Eric Cascales", "Christian Cambillau"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122187.t002", "stats"=>{"downloads"=>6, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Kinetic_and_thermodynamic_parameters_of_the_interactions_between_anti_TssM_nanobodies_with_TssMp_/1357708", "title"=>"Kinetic and thermodynamic parameters of the interactions between anti-TssM nanobodies with TssMp.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-03-26 04:48:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1990955"], "description"=>"<p><b>(A)</b> Hcp release assay. HA-epitope-tagged Hcp (Hcp<sub>HA</sub>) release was assessed by separating whole cells (C) and supernatant (S) fractions from wild-type (WT), Δ<i>tssM c</i>ells or WT cells producing 6His-tagged nanobodies as indicated. 2×10<sup>8</sup> cells and the TCA-precipitated material of the supernatant from 5×10<sup>8</sup> cells were loaded on a 12.5%-acrylamide SDS-PAGE and the nanobodies (lower panel), Hcp (middle panel) and periplasmic TolB (cell integrity control, upper panel) proteins were immunodetected using anti-5His, anti-HA and anti-TolB antibodies respectively. <b>(B)</b> Anti-bacterial assay. The Sci-1 T6SS-dependent anti-bacterial activity was assessed by mixing prey cells (W3110 <i>gfp</i><sup>+</sup>, kan<sup>R</sup>) with the indicated attacker cell (K-12, W3110; WT, EAEC 17–2; Δ<i>tssM</i>, 17–2Δ<i>tssM</i> or WT cells producing the indicated nanobody) for 16 hours at 37°C in <i>sci-1</i>-inducing medium (SIM). The recovered fluorescent level (in arbitrary units) is shown in the upper graph (mean of fluorescence levels per OD<sub>600nm</sub> obtained from four independent experiments). The number of recovered viable prey cells, expressed in colony forming unit (cfu) is shown in the lower graph (the triangles indicate values from four independent assays, and the average is indicated by the bar).</p>", "links"=>[], "tags"=>["TssM periplasmic domain", "membrane", "nb 25 CDR 3 loop share", "stator", "type VI secretion", "nanobodie", "phage contractile tail structure", "13 core proteins", "T 6SS", "tssj", "TssM binding site", "T 6SS function", "type VI secretion system", "lipoprotein"], "article_id"=>1357705, "categories"=>["Biological Sciences"], "users"=>["Van Son Nguyen", "Laureen Logger", "Silvia Spinelli", "Aline Desmyter", "Thi Thu Hang Le", "Christine Kellenberger", "Badreddine Douzi", "Eric Durand", "Alain Roussel", "Eric Cascales", "Christian Cambillau"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122187.g005", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TssM_specific_nanobodies_nb25_and_nb42_specifically_affect_T6SS_function_/1357705", "title"=>"TssM-specific nanobodies nb25 and nb42 specifically affect T6SS function.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-26 04:48:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1990953"], "description"=>"<p>The pre-formed TssM-TssJ complex was analyzed by size exclusion chromatography before (dash line) and after incubation with an excess of nb25 (plain line). The composition of the different complexes, eluting at different volumes, was analysed by SDS-PAGE and Coomassie blue staining (inset). The fractions corresponding to peak 1–3 are indicated on the top. The molecular masses of the protein markers (in kDa) are indicated on the left. According to the calibration of the column, the apparent molecular weights for peak 1 (9.72 ml), peak 2 (13.02 ml) and peak 3 (14.43 ml) are about 90, 18 and 14 kDa, respectively. The faint band at the position of TssMp in peaks 2 and 3 of the SDS gel arise from contamination by the large main TssMp peak 1.</p>", "links"=>[], "tags"=>["TssM periplasmic domain", "membrane", "nb 25 CDR 3 loop share", "stator", "type VI secretion", "nanobodie", "phage contractile tail structure", "13 core proteins", "T 6SS", "tssj", "TssM binding site", "T 6SS function", "type VI secretion system", "lipoprotein"], "article_id"=>1357704, "categories"=>["Biological Sciences"], "users"=>["Van Son Nguyen", "Laureen Logger", "Silvia Spinelli", "Aline Desmyter", "Thi Thu Hang Le", "Christine Kellenberger", "Badreddine Douzi", "Eric Durand", "Alain Roussel", "Eric Cascales", "Christian Cambillau"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122187.g004", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nanobody_nb25_disrupts_the_TssMp_TssJ_complex_/1357704", "title"=>"Nanobody nb25 disrupts the TssMp:TssJ complex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-26 04:48:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1990949"], "description"=>"<p>Bilayer interferometry recordings representing binding of TssMp alone (blue) or the TssMp:nb02 (red) or TssMp:nb25 (green) complexes to chip coupled to TssJ. The response (in nm) is plotted versus the time (in sec.). The absence of response in the green sensorgram indicates that nb25 prevents attachment of TssMp to TssJ.</p>", "links"=>[], "tags"=>["TssM periplasmic domain", "membrane", "nb 25 CDR 3 loop share", "stator", "type VI secretion", "nanobodie", "phage contractile tail structure", "13 core proteins", "T 6SS", "tssj", "TssM binding site", "T 6SS function", "type VI secretion system", "lipoprotein"], "article_id"=>1357702, "categories"=>["Biological Sciences"], "users"=>["Van Son Nguyen", "Laureen Logger", "Silvia Spinelli", "Aline Desmyter", "Thi Thu Hang Le", "Christine Kellenberger", "Badreddine Douzi", "Eric Durand", "Alain Roussel", "Eric Cascales", "Christian Cambillau"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122187.g003", "stats"=>{"downloads"=>1, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Binding_of_TssMp_nanobody_complexes_to_TssJ_/1357702", "title"=>"Binding of TssMp:nanobody complexes to TssJ.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-26 04:48:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1990956"], "description"=>"<p><sup>a</sup> numbers in brackets refer to the highest resolution bin.</p><p>Data collection and refinement statistics for the nb02 and nb25 anti-TssM nanobodies.</p>", "links"=>[], "tags"=>["TssM periplasmic domain", "membrane", "nb 25 CDR 3 loop share", "stator", "type VI secretion", "nanobodie", "phage contractile tail structure", "13 core proteins", "T 6SS", "tssj", "TssM binding site", "T 6SS function", "type VI secretion system", "lipoprotein"], "article_id"=>1357706, "categories"=>["Biological Sciences"], "users"=>["Van Son Nguyen", "Laureen Logger", "Silvia Spinelli", "Aline Desmyter", "Thi Thu Hang Le", "Christine Kellenberger", "Badreddine Douzi", "Eric Durand", "Alain Roussel", "Eric Cascales", "Christian Cambillau"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122187.t001", "stats"=>{"downloads"=>2, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Data_collection_and_refinement_statistics_for_the_nb02_and_nb25_anti_TssM_nanobodies_/1357706", "title"=>"Data collection and refinement statistics for the nb02 and nb25 anti-TssM nanobodies.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-03-26 04:48:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1990948"], "description"=>"<p>Surface Plasmon Resonance recordings representing binding and release of the purified periplasmic domain of TssM (from bottom to top: 1.95, 3.9, 7.8, 15.6, 31.25, 62.5, 125 and 250 nM) to nanobody nb02 (<b>A</b>), nb25 (<b>B</b>) or nb42 (<b>C</b>) immobilized on the Chip. The variation of the Surface Plasmon Resonance (shown as the experimental and fitting curves) is reported on the <i>y</i> axis (in arbitrary unit, RU) plotted versus the reaction time on the <i>x</i> axis (in sec.). The apparent K<sub><i>D</i></sub>s are indicated on the top of each graph. The kinetic and thermodynamic parameters are indicated in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0122187#pone.0122187.t002\" target=\"_blank\">Table 2</a>.</p>", "links"=>[], "tags"=>["TssM periplasmic domain", "membrane", "nb 25 CDR 3 loop share", "stator", "type VI secretion", "nanobodie", "phage contractile tail structure", "13 core proteins", "T 6SS", "tssj", "TssM binding site", "T 6SS function", "type VI secretion system", "lipoprotein"], "article_id"=>1357701, "categories"=>["Biological Sciences"], "users"=>["Van Son Nguyen", "Laureen Logger", "Silvia Spinelli", "Aline Desmyter", "Thi Thu Hang Le", "Christine Kellenberger", "Badreddine Douzi", "Eric Durand", "Alain Roussel", "Eric Cascales", "Christian Cambillau"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122187.g002", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nanobodies_nb02_and_nb25_bind_TssMp_with_nanomolar_affinity_/1357701", "title"=>"Nanobodies nb02 and nb25 bind TssMp with nanomolar affinity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-26 04:48:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1990944"], "description"=>"<p>(<b>A</b>) Sequence alignment of nanobodies nb02, nb25 and nb42. Identical amino-acids are in white and underlined in red, similar amino-acids are colored in red, different amino-acids are in black. The CDR1, CDR2 and CDR3 are highlighted in blue, green and yellow, respectively. The green numbers (1 or 2) below the sequence indicate cysteine residues involved in disulphide bridges SS1 (1, Cys22 and Cys96) and SS2 (2, Cys50 and Cys106) disulphide bridges formation. Crystal structure of nanobodies nb02 (<b>B</b>) and nb25 (<b>C</b>), represented as ribbons and colored in rainbow mode. (<b>D</b>) Superimposition of the structures of nb02 (grey) and nb25 (rainbow color). The locations of the CDR1, CDR2 and CDR3 variable regions are indicated as well as the positions of disulphide bridges (SS1 and SS2).</p>", "links"=>[], "tags"=>["TssM periplasmic domain", "membrane", "nb 25 CDR 3 loop share", "stator", "type VI secretion", "nanobodie", "phage contractile tail structure", "13 core proteins", "T 6SS", "tssj", "TssM binding site", "T 6SS function", "type VI secretion system", "lipoprotein"], "article_id"=>1357697, "categories"=>["Biological Sciences"], "users"=>["Van Son Nguyen", "Laureen Logger", "Silvia Spinelli", "Aline Desmyter", "Thi Thu Hang Le", "Christine Kellenberger", "Badreddine Douzi", "Eric Durand", "Alain Roussel", "Eric Cascales", "Christian Cambillau"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122187.g001", "stats"=>{"downloads"=>2, "page_views"=>242, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structure_of_the_anti_TssM_nanobodies_/1357697", "title"=>"Structure of the anti-TssM nanobodies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-26 04:48:59"}

PMC Usage Stats | Further Information

  • {"unique-ip"=>"42", "full-text"=>"52", "pdf"=>"27", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"4"}
  • {"unique-ip"=>"32", "full-text"=>"35", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
  • {"unique-ip"=>"30", "full-text"=>"38", "pdf"=>"12", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"18", "full-text"=>"22", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"18", "full-text"=>"21", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"17", "full-text"=>"17", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"14", "full-text"=>"19", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"18", "full-text"=>"16", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"19", "full-text"=>"17", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"17", "full-text"=>"13", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"13", "full-text"=>"16", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"11", "full-text"=>"37", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"74", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"16", "full-text"=>"17", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"10", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"9", "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"=>"17", "full-text"=>"14", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"18", "full-text"=>"21", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"9", "full-text"=>"11", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"13", "full-text"=>"15", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"11", "full-text"=>"9", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"10", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"4", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"11", "full-text"=>"16", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"12", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"12", "full-text"=>"16", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"13", "full-text"=>"21", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"15", "full-text"=>"11", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"20", "full-text"=>"14", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"12", "full-text"=>"5", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"13", "full-text"=>"11", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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