Biochemical Warfare on the Reef: The Role of Glutathione Transferases in Consumer Tolerance of Dietary Prostaglandins
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{"title"=>"Biochemical warfare on the reef: The role of glutathione transferases in consumer tolerance of dietary prostaglandins", "type"=>"journal", "authors"=>[{"first_name"=>"Kristen E.", "last_name"=>"Whalen", "scopus_author_id"=>"24545001800"}, {"first_name"=>"Amy L.", "last_name"=>"Lane", "scopus_author_id"=>"14017960500"}, {"first_name"=>"Julia", "last_name"=>"Kubanek", "scopus_author_id"=>"6603812071"}, {"first_name"=>"Mark E.", "last_name"=>"Hahn", "scopus_author_id"=>"7201578361"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-77649102859", "pui"=>"358372371", "doi"=>"10.1371/journal.pone.0008537", "isbn"=>"1932-6203", "sgr"=>"77649102859", "pmid"=>"20052279"}, "id"=>"b3ca5c9d-53b4-3be6-9875-5e0c9c9f2a59", "abstract"=>"Despite the profound variation among marine consumers in tolerance for allelochemically-rich foods, few studies have examined the biochemical adaptations underlying diet choice. Here we examine the role of glutathione S-transferases (GSTs) in the detoxification of dietary allelochemicals in the digestive gland of the predatory gastropod Cyphoma gibbosum, a generalist consumer of gorgonian corals. Controlled laboratory feeding experiments were used to investigate the influence of gorgonian diet on Cyphoma GST activity and isoform expression. Gorgonian extracts and semi-purified fractions were also screened to identify inhibitors and possible substrates of Cyphoma GSTs. In addition, we investigated the inhibitory properties of prostaglandins (PGs) structurally similar to antipredatory PGs found in high concentrations in the Caribbean gorgonian Plexaura homomalla.", "link"=>"http://www.mendeley.com/research/biochemical-warfare-reef-role-glutathione-transferases-consumer-tolerance-dietary-prostaglandins", "reader_count"=>19, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>7, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>7, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>12, "Chemistry"=>1, "Social Sciences"=>1, "Linguistics"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Linguistics"=>{"Linguistics"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Mexico"=>1, "United Kingdom"=>1, "Portugal"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/868330"], "description"=>"<p>Bars represent the mean GST activity (±SE) of snails feeding on the control diet (n = 12 snails) or one of six gorgonian diets – <i>B. asbestinum</i> (n = 4), <i>E. mammosa</i> (n = 4), <i>G. ventalina</i> (n = 4), <i>P. acerosa</i> (n = 4), <i>P. americana</i> (n = 7) and <i>P. homomalla</i> (n = 4). The reaction mixture contained 2 µg of cytosolic protein in 0.1 M KPO<sub>4</sub> buffer, pH 7.5, containing 1 mM GSH and 1 mM CDNB at 25°C. GST activity did not differ among snail diets (ANOVA, <i>P</i> = 0.687) or among snails feeding on the control diet collected from different reefs (ANOVA, <i>P</i> = 0.109).</p>", "links"=>[], "tags"=>["gland", "gst", "snail"], "article_id"=>538784, "categories"=>["Ecology", "Physiology", "Biochemistry"], "users"=>["Kristen E. Whalen", "Amy L. Lane", "Julia Kubanek", "Mark E. Hahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008537.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Digestive_gland_GST_activity_does_not_differ_with_snail_diet_/538784", "title"=>"Digestive gland GST activity does not differ with snail diet.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-06 02:26:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/431335", "https://ndownloader.figshare.com/files/431380", "https://ndownloader.figshare.com/files/431512", "https://ndownloader.figshare.com/files/431656", "https://ndownloader.figshare.com/files/431744", "https://ndownloader.figshare.com/files/431808"], "description"=>"<div><h3>Background</h3><p>Despite the profound variation among marine consumers in tolerance for allelochemically-rich foods, few studies have examined the biochemical adaptations underlying diet choice. Here we examine the role of glutathione <em>S</em>-transferases (GSTs) in the detoxification of dietary allelochemicals in the digestive gland of the predatory gastropod <em>Cyphoma gibbosum</em>, a generalist consumer of gorgonian corals. Controlled laboratory feeding experiments were used to investigate the influence of gorgonian diet on <em>Cyphoma</em> GST activity and isoform expression. Gorgonian extracts and semi-purified fractions were also screened to identify inhibitors and possible substrates of <em>Cyphoma</em> GSTs. In addition, we investigated the inhibitory properties of prostaglandins (PGs) structurally similar to antipredatory PGs found in high concentrations in the Caribbean gorgonian <em>Plexaura homomalla</em>.</p><h3>Principal Findings</h3><p><em>Cyphoma</em> GST subunit composition was invariant and activity was constitutively high regardless of gorgonian diet. Bioassay-guided fractionation of gorgonian extracts revealed that moderately hydrophobic fractions from all eight gorgonian species examined contained putative GST substrates/inhibitors. LC-MS and NMR spectral analysis of the most inhibitory fraction from <em>P. homomalla</em> subsequently identified prostaglandin A<sub>2</sub> (PGA<sub>2</sub>) as the dominant component. A similar screening of commercially available prostaglandins in series A, E, and F revealed that those prostaglandins most abundant in gorgonian tissues (e.g., PGA<sub>2</sub>) were also the most potent inhibitors. <em>In vivo</em> estimates of PGA<sub>2</sub> concentration in digestive gland tissues calculated from snail grazing rates revealed that <em>Cyphoma</em> GSTs would be saturated with respect to PGA<sub>2</sub> and operating at or near physiological capacity.</p><h3>Significance</h3><p>The high, constitutive activity of <em>Cyphoma</em> GSTs is likely necessitated by the ubiquitous presence of GST substrates and/or inhibitors in this consumer's gorgonian diet. This generalist's GSTs may operate as ‘all-purpose’ detoxification enzymes, capable of conjugating or sequestering a broad range of lipophilic gorgonian compounds, thereby allowing this predator to exploit a range of chemically-defended prey, resulting in a competitive dietary advantage for this species.</p></div>", "links"=>[], "tags"=>["biochemical", "warfare", "glutathione", "transferases", "dietary", "prostaglandins"], "article_id"=>145121, "categories"=>["Ecology", "Physiology", "Biochemistry"], "users"=>["Kristen E. Whalen", "Amy L. Lane", "Julia Kubanek", "Mark E. Hahn"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0008537.s001", "https://dx.doi.org/10.1371/journal.pone.0008537.s002", "https://dx.doi.org/10.1371/journal.pone.0008537.s003", "https://dx.doi.org/10.1371/journal.pone.0008537.s004", "https://dx.doi.org/10.1371/journal.pone.0008537.s005", "https://dx.doi.org/10.1371/journal.pone.0008537.s006"], "stats"=>{"downloads"=>11, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Biochemical_Warfare_on_the_Reef_The_Role_of_Glutathione_Transferases_in_Consumer_Tolerance_of_Dietary_Prostaglandins/145121", "title"=>"Biochemical Warfare on the Reef: The Role of Glutathione Transferases in Consumer Tolerance of Dietary Prostaglandins", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-01-06 01:25:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/868636"], "description"=>"a<p>Enzyme activity in the presence of prostaglandin inhibitors was determined at pH 7.5 and 25°C, with 1 mM CDNB and 1 mM GSH and 4% (v/v) DMSO. The mean percent inhibition from five affinity-purified GST concentrates was used to calculate IC<sub>50</sub> values.</p>b<p>K<sub>i</sub> values were calculated using the Cheng-Prusoff equation with an K<sub>m</sub> value of 0.41 mM for CDNB obtained from the average of two independent experiments; a CDNB substrate concentration of 1 mM; and IC<sub>50</sub> values listed in the table above.</p>c<p>In an attempt to constrain the likely range of calculated K<sub>i</sub> values, test calculations using K<sub>m</sub> values for CDNB ranging from 0.1 mM to 1.0 mM resulted in K<sub>i</sub> values for 15(<i>S</i>)-PGA<sub>2</sub> of 6.0 to 37.7 µM.</p>", "links"=>[], "tags"=>["inhibition", "constants", "prostaglandin"], "article_id"=>539090, "categories"=>["Ecology", "Physiology", "Biochemistry"], "users"=>["Kristen E. Whalen", "Amy L. Lane", "Julia Kubanek", "Mark E. Hahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008537.t001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IC_50_values_and_inhibition_constants_K_i_of_prostaglandin_inhibitors_/539090", "title"=>"IC<sub>50</sub> values and inhibition constants (K<sub>i</sub>) of prostaglandin inhibitors.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-01-06 02:31:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/868566"], "description"=>"<p>Points represent the mean (±SE) GST activity remaining compared to solvent controls after incubation with various concentrations (0.2–2000 µM) of 15(R)-15-methyl PGA<sub>2</sub> (•), 15(S)-PGE<sub>2</sub> (▪), 15(S)-PGA<sub>2</sub> (▴), 15(S)-PGF<sub>2α</sub> (▾). The reaction mixture consisted of 3.3–6.4 ng of affinity-purified GST protein in 0.1 M potassium phosphate buffer, pH 7.5, containing 1 mM GSH, 1 mM CDNB at 25°C with 5% (v/v) DMSO. Affinity-purified GST preparations from five snails were used as the enzyme source with specific activities of ranging from 290–582 µmol min<sup>−1</sup> mg protein<sup>−1</sup>. Plots were used to obtain the IC<sub>50</sub> value for each prostaglandin and are listed in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0008537#pone-0008537-t001\" target=\"_blank\">Table 1</a>.</p>", "links"=>[], "tags"=>["affinity-purified", "gst"], "article_id"=>539030, "categories"=>["Ecology", "Physiology", "Biochemistry"], "users"=>["Kristen E. Whalen", "Amy L. Lane", "Julia Kubanek", "Mark E. Hahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008537.g004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inhibition_of_Cyphoma_affinity_purified_GST_activity_by_select_prostaglandins_/539030", "title"=>"Inhibition of <i>Cyphoma</i> affinity-purified GST activity by select prostaglandins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-06 02:30:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/868510"], "description"=>"<p>Eight commercially available prostaglandin compounds, representing a diversity of prostaglandin series present in gorgonian tissues, were screened for their ability to inhibit GST activity at 600 µM. Bars represent the mean (±SE) percent GST activity remaining after prostaglandin exposure compared to solvent controls. The reaction mixture consisted of 2 µg of cytosolic GST protein in 0.1 M potassium phosphate buffer, pH 7.5, containing 1 mM GSH, 1 mM CDNB at 25°C with 5% (v/v) DMSO. Digestive gland cytosolic preparations from two snails were used as the enzyme source with specific activities of 5.8 and 5.1 µmol min<sup>−1</sup> mg protein<sup>−1</sup>, respectively.</p>", "links"=>[], "tags"=>["inhibit", "gst"], "article_id"=>538970, "categories"=>["Ecology", "Physiology", "Biochemistry"], "users"=>["Kristen E. Whalen", "Amy L. Lane", "Julia Kubanek", "Mark E. Hahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008537.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Prostaglandin_A_E_and_F_series_inhibit_Cyphoma_GST_activity_/538970", "title"=>"Prostaglandin A, E and F series inhibit <i>Cyphoma</i> GST activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-06 02:29:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/868406"], "description"=>"<p>Bars represent the mean (±SE) percent GST activity remaining after addition of gorgonian compounds compared to solvent controls. Reaction mixture consisted of 2 µg cytosolic protein in 0.1 M potassium phosphate buffer, pH 7.5, containing 1 mM GSH, 1 mM CDNB at 25°C with <0.01% (v/v) solvent. Reactions were performed in duplicate with digestive gland crude cytosolic preparations from two snails. Crude extracts from eight gorgonian species were tested at 5% natural vol. concentration (NC) for their ability to inhibit crude cytosolic GST activity. Hexane and aqueous soluble extracts were tested at 25% NC. Chloroform soluble fractions were tested at 25% NC with the following exceptions: <i>G. ventalina</i>, <i>P. acerosa</i>, and <i>P. homomalla</i> were tested at 12% NC. A zero indicates complete inhibition of GST activity by the gorgonian extracts and the dotted line indicates no difference from solvent controls.</p>", "links"=>[], "tags"=>["crude", "semi-purified", "extracts", "inhibit", "gst"], "article_id"=>538859, "categories"=>["Ecology", "Physiology", "Biochemistry"], "users"=>["Kristen E. Whalen", "Amy L. Lane", "Julia Kubanek", "Mark E. Hahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008537.g002", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gorgonian_crude_and_semi_purified_extracts_inhibit_Cyphoma_GST_activity_/538859", "title"=>"Gorgonian crude and semi-purified extracts inhibit <i>Cyphoma</i> GST activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-06 02:27:39"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"11", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"2", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"7", "full-text"=>"2", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"6", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
  • {"unique-ip"=>"19", "full-text"=>"16", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2015", "month"=>"11"}
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  • {"unique-ip"=>"5", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"3", "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"=>"5"}
  • {"unique-ip"=>"3", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
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  • {"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"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"3", "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"=>"11"}
  • {"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"=>"2016", "month"=>"12"}
  • {"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"=>"2017", "month"=>"1"}
  • {"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"=>"2"}
  • {"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"=>"3"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"2", "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"=>"5"}
  • {"unique-ip"=>"2", "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"=>"6"}
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  • {"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"=>"8"}
  • {"unique-ip"=>"5", "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"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"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"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"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"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"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"=>"6"}
  • {"unique-ip"=>"16", "full-text"=>"5", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "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"=>"7", "full-text"=>"8", "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"=>"2018", "month"=>"10"}
  • {"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"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "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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