IL-17RA Signaling Reduces Inflammation and Mortality during Trypanosoma cruzi Infection by Recruiting Suppressive IL-10-Producing Neutrophils
Publication Date
April 26, 2012
Journal
PLOS Pathogens
Authors
Jimena Tosello Boari, María Carolina Amezcua Vesely, Daniela Andrea Bermejo, Maria Cecilia Ramello, et al
Volume
8
Issue
4
Pages
e1002658
DOI
https://dx.plos.org/10.1371/journal.ppat.1002658
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1002658
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/22577359
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3343119
Europe PMC
http://europepmc.org/abstract/MED/22577359
Web of Science
000303444200047
Scopus
84861204482
Mendeley
http://www.mendeley.com/research/il17ra-signaling-reduces-inflammation-mortality-during-trypanosoma-cruzi-infection-recruiting-suppre
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Mendeley | Further Information

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/333458"], "description"=>"<div><p>Members of the IL-17 cytokine family play an important role in protection against pathogens through the induction of different effector mechanisms. We determined that IL-17A, IL-17E and IL-17F are produced during the acute phase of <em>T. cruzi</em> infection. Using IL-17RA knockout (KO) mice, we demonstrate that IL-17RA, the common receptor subunit for many IL-17 family members, is required for host resistance during <em>T. cruzi</em> infection. Furthermore, infected IL-17RA KO mice that lack of response to several IL-17 cytokines showed amplified inflammatory responses with exuberant IFN-γ and TNF production that promoted hepatic damage and mortality. Absence of IL-17RA during <em>T. cruzi</em> infection resulted in reduced CXCL1 and CXCL2 expression in spleen and liver and limited neutrophil recruitment. <em>T. cruzi</em>-stimulated neutrophils secreted IL-10 and showed an IL-10-dependent suppressive phenotype <em>in vitro</em> inhibiting T-cell proliferation and IFN-γ production. Specific depletion of Ly-6G+ neutrophils <em>in vivo</em> during <em>T. cruzi</em> infection raised parasitemia and serum IFN-γ concentration and resulted in increased liver pathology in WT mice and overwhelming wasting disease in IL-17RA KO mice. Adoptively transferred neutrophils were unable to migrate to tissues and to restore resistant phenotype in infected IL-17RA KO mice but migrated to spleen and liver of infected WT mice and downregulated IFN-γ production and increased survival in an IL-10 dependent manner. Our results underscore the role of IL-17RA in the modulation of IFN-γ-mediated inflammatory responses during infections and uncover a previously unrecognized regulatory mechanism that involves the IL-17RA-mediated recruitment of suppressive IL-10-producing neutrophils.</p> </div>", "links"=>[], "tags"=>["il-17ra", "signaling", "reduces", "inflammation", "recruiting", "suppressive", "il-10-producing", "neutrophils"], "article_id"=>125853, "categories"=>["Cancer"], "users"=>["Jimena Tosello Boari", "María Carolina Amezcua Vesely", "Daniela Andrea Bermejo", "Maria Cecilia Ramello", "Carolina Lucía Montes", "Hugo Cejas", "Adriana Gruppi", "Eva Virginia Acosta Rodríguez"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002658"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/IL_17RA_Signaling_Reduces_Inflammation_and_Mortality_during_Trypanosoma_cruzi_Infection_by_Recruiting_Suppressive_IL_10_Producing_Neutrophils/125853", "title"=>"IL-17RA Signaling Reduces Inflammation and Mortality during <em>Trypanosoma cruzi</em> Infection by Recruiting Suppressive IL-10-Producing Neutrophils", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-04-26 01:37:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/646726"], "description"=>"<p>A) IL-17A and IL-17F concentration determined in the culture supernatants of spleen and lymph node cells obtained from mice at different times post <i>T. cruzi</i> infection and stimulated during 48 h in the presence of CD3/PdBU. Data are shown as mean ± SD, n = 5 mice per group. B) Plasma IL-17A concentration in non-infected (NI) or 20-day <i>T. cruzi</i>-infected (I) mice. Data are shown as mean ± SD, n = 5 mice per group. C) Percentage of IL-17A positive cells after 5 h PMA/Ionomycin stimulation of liver cell suspensions obtained from 20-day <i>T. cruzi</i>-infected mice. Plot representative of one out of five mice. D) Percentage of IL-17A positive cells within CD3 positive and CD3 negative cell population after 5 h PMA/Ionomycin stimulation of spleen, lymph nodes and liver cells from 20-day <i>T. cruzi</i>-infected mice. Data are shown as mean ± SEM, n = 5 mice per group. E) IL-17A concentration determined in the culture supernatants of NK1.1+ cells, CD4+ and CD8+ T cells, Gr-1+ cells and the remaining negative fraction (NF) sorted from the spleen and liver of 20-day <i>T. cruzi</i> infected mice and stimulated during 48 h. Data are shown as mean ± SD of triplicates cultures. F) Plasma IL-17E concentration in non-infected (NI) or 20-day <i>T. cruzi</i>-infected (I) mice. Data are shown as mean ± SD, n = 5 mice per group. Data in A, E and F and in B–D are representative of two and three independent experiments, respectively.</p>", "links"=>[], "tags"=>["il-17e", "il-17f"], "article_id"=>317212, "categories"=>["Infectious Diseases"], "users"=>["Jimena Tosello Boari", "María Carolina Amezcua Vesely", "Daniela Andrea Bermejo", "Maria Cecilia Ramello", "Carolina Lucía Montes", "Hugo Cejas", "Adriana Gruppi", "Eva Virginia Acosta Rodríguez"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002658.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IL_17A_IL_17E_and_IL_17F_production_during_T_cruzi_infection_/317212", "title"=>"IL-17A, IL-17E and IL-17F production during <i>T. cruzi</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-26 02:00:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/646906"], "description"=>"<p>A) Survival of WT and IL-17RA KO mice after <i>T. cruzi</i> infection, P value calculated with a Gehan-Breslow-Wilcoxon test, n = 20 per group. B) Parasitemia determined at different time post <i>T. cruzi</i> infection in WT and IL-17RA KO mice, n = 10 per group. P values calculated using two-tailed T test. C) Plasma activity of ALT and AST in WT and IL-17RA KO mice at different times post <i>T. cruzi</i> infection. Data are shown as mean ± SD, n = 5 mice per group. P values calculated using two-way ANOVA followed by Bonferroni's posttest. D) Photographs of Hematoxilin/Eosin stained liver sections from 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice. 200× micrographs allow panoramic evaluation of the lesions. An extensive necrotic area is demarcated in the liver from KO mice. 1000× micrograph show details about the cellular alterations and the nature of inflammatory infiltrate (P: polymorphonuclear cells, M: mononuclear cells, A: amastigote nest). Photographs are representative of one out of five mice. Data in A–C and in D are representative of three and two independent experiments, respectively.</p>", "links"=>[], "tags"=>["parasitism", "hepatic", "il-17ra", "ko", "mice"], "article_id"=>317390, "categories"=>["Infectious Diseases"], "users"=>["Jimena Tosello Boari", "María Carolina Amezcua Vesely", "Daniela Andrea Bermejo", "Maria Cecilia Ramello", "Carolina Lucía Montes", "Hugo Cejas", "Adriana Gruppi", "Eva Virginia Acosta Rodríguez"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002658.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_mortality_tissue_parasitism_and_hepatic_damage_in_IL_17RA_KO_mice_during_T_cruzi_infection_/317390", "title"=>"Increased mortality, tissue parasitism and hepatic damage in IL-17RA KO mice during <i>T. cruzi</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-26 02:03:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/647044"], "description"=>"<p>A) Plasma IFN-γ and TNF concentration in 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice. Data are shown as mean ± SD, n = 6 mice per group. P values calculated using two-tailed T test. B) Plasma IFN-γ concentration in 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice treated with anti-IFN-γ. P values calculated using two-tailed T test. C) Parasitemia determined in 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice treated with anti-IFN-γ. Data are shown as mean ± SD, n = 6 mice per group. P values calculated using two-tailed T test. D) Activity of ALT and AST determined in the plasma of 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice treated with anti-IFN-γ. Data are shown as mean ± SD, n = 6 mice per group. P values calculated using two-tailed T test. E) Survival of <i>T. cruzi</i> infected WT and IL-17RA KO mice treated with anti-IFN-γ. P value calculated with a Gehan-Breslow-Wilcoxon test, n = 12 per group. Data in A and in B–E are representative of four and two independent experiments, respectively.</p>", "links"=>[], "tags"=>["caused", "hepatic", "infected", "il-17ra", "ko"], "article_id"=>317526, "categories"=>["Infectious Diseases"], "users"=>["Jimena Tosello Boari", "María Carolina Amezcua Vesely", "Daniela Andrea Bermejo", "Maria Cecilia Ramello", "Carolina Lucía Montes", "Hugo Cejas", "Adriana Gruppi", "Eva Virginia Acosta Rodríguez"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002658.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Augmented_production_of_IFN_caused_increased_hepatic_damage_and_mortality_in_T_cruzi_infected_IL_17RA_KO_mice_/317526", "title"=>"Augmented production of IFN-γ caused increased hepatic damage and mortality in <i>T. cruzi</i> infected IL-17RA KO mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-26 02:05:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/647251"], "description"=>"<p>A) Cell numbers in spleen, lymph nodes and liver of WT and IL-17RA KO mice determined at different times after <i>T. cruzi</i> infection. Data are shown as mean ± SD, n = 5 mice per group. P values calculated using two-way ANOVA followed by Bonferroni's posttest. B) Percentage of CD11b+ Gr-1+ neutrophils in spleen and liver of 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice. Plots are representative one out of five mice. C) Absolute numbers of CD11b+ Gr-1+ neutrophils in spleen (left) and liver (right) of 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice. Each symbol represents a different mouse and horizontal line indicates the mean. P values calculated with two-tailed T test. D) Concentration of CXCL1, CXCL2 and CXCL10 in spleen and liver homogenates obtained from WT and IL-17RA KO mice at different times post <i>T. cruzi</i> infection. Data are shown as mean ± SD of biological triplicates, normalized to total protein concentration, n = 5 mice per group. P values calculated with two-way ANOVA followed by Bonferroni's posttest. (* p: spleen WT vs spleen KO; # p: liver WT vs liver KO). E) Absolute number or frequency of transferred WT and IL-17RA KO neutrophils detected in bone marrow, blood, spleen and liver of non-infected (NI) and infected (I) WT and IL-17RA KO mice 3 h after i.v. injection. Data are shown as mean ± SD, n = 5 per group. P values calculated with two-tailed T test. Data in A–C and D–E are representative of four and two independent experiments, respectively.</p>", "links"=>[], "tags"=>["neutrophil", "chemoattractant", "recruitment", "spleen", "infected", "il-17ra", "ko"], "article_id"=>317727, "categories"=>["Infectious Diseases"], "users"=>["Jimena Tosello Boari", "María Carolina Amezcua Vesely", "Daniela Andrea Bermejo", "Maria Cecilia Ramello", "Carolina Lucía Montes", "Hugo Cejas", "Adriana Gruppi", "Eva Virginia Acosta Rodríguez"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002658.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reduced_neutrophil_chemoattractant_production_and_neutrophil_recruitment_in_the_spleen_and_liver_of_T_cruzi_infected_IL_17RA_KO_mice_/317727", "title"=>"Reduced neutrophil chemoattractant production and neutrophil recruitment in the spleen and liver of <i>T. cruzi</i> infected IL-17RA KO mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-26 02:08:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/647416"], "description"=>"<p>A–B) Concentration of IL-10 and TNF determined in 48 h culture supernatants of Ly-6G+ neutrophils purified from bone marrow of WT and IL-17RA KO mice (A) and of CD11b+Ly-6G+ neutrophils sorted from spleen 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice (B) and stimulated as indicated. Data are shown as mean ± SD of cuatriplicates. C) Proliferation and percentage of IFN-γ-producing CD3 positive splenocytes from normal mice after 5 day stimulation in anti-CD3 and anti-CD28 coated plates in the presence of CD11b+Ly-6G+ neutrophils obtained from 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice and of a blocking anti-IL10R Ab. Data are shown as mean ± SD of triplicates. P values calculated using two-tailed T test. Data in A–C are representative of two independent experiments.</p>", "links"=>[], "tags"=>["proliferation", "il-10", "secreting", "neutrophils", "infected"], "article_id"=>317898, "categories"=>["Infectious Diseases"], "users"=>["Jimena Tosello Boari", "María Carolina Amezcua Vesely", "Daniela Andrea Bermejo", "Maria Cecilia Ramello", "Carolina Lucía Montes", "Hugo Cejas", "Adriana Gruppi", "Eva Virginia Acosta Rodríguez"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002658.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Suppression_of_T_cell_proliferation_and_IFN_production_by_IL_10_secreting_neutrophils_obtained_from_T_cruzi_infected_mice_/317898", "title"=>"Suppression of T cell proliferation and IFN-γ production by IL-10 secreting neutrophils obtained from <i>T. cruzi</i> infected mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-26 02:11:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/647603"], "description"=>"<p>A) CD11b+Gr-1+ frequency and absolute numbers in blood, spleen and liver of 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice treated with anti-Ly6G mAbs. Data are shown as mean ± SD, n = 6–8 mice per group. P values calculated by two-tailed T test. B) Concentration of IL-10 determined in 48 h unstimulated culture supernatants of spleen and liver cell suspensions obtained from 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice treated with anti-Ly-6G mAbs. Each symbol represents a different mouse and horizontal line indicates the mean. P values calculated with two-tailed T test. C) Plasma IFN-γ and TNF concentration in 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice treated with anti-Ly-6G mAbs. Each symbol represents a different mouse and horizontal line indicates the mean. P values calculated with two-tailed T test. D) Activity of ALT and AST determined in the plasma of 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice treated with anti-Ly-6G. Data are shown as mean ± SD, n = 6–8 mice per group. P values calculated using two-tailed T test. E) Parasitemia determined in 20-day <i>T. cruzi</i> infected WT and IL-17RA KO mice treated with anti-Ly-6G Abs. Data are shown as mean ± SD, n = 6–8 mice per group. P values calculated using two-tailed T test. F) Survival of <i>T. cruzi</i> infected WT and IL-17RA KO mice treated with anti-Ly-6G. P value calculated with a Gehan-Breslow-Wilcoxon test, n = 12 per group. Data in A–D and in E are representative of three and two independent experiments, respectively.</p>", "links"=>[], "tags"=>["hepatic", "transaminases", "infected", "wt", "il-17ra", "ko", "mice", "neutrophil"], "article_id"=>318080, "categories"=>["Infectious Diseases"], "users"=>["Jimena Tosello Boari", "María Carolina Amezcua Vesely", "Daniela Andrea Bermejo", "Maria Cecilia Ramello", "Carolina Lucía Montes", "Hugo Cejas", "Adriana Gruppi", "Eva Virginia Acosta Rodríguez"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002658.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_IFN_production_and_hepatic_transaminases_activity_in_T_cruzi_infected_WT_and_IL_17RA_KO_mice_after_neutrophil_depletion_/318080", "title"=>"Increased IFN-γ production and hepatic transaminases activity in <i>T. cruzi</i> infected WT and IL-17RA KO mice after neutrophil depletion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-26 02:14:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/647770"], "description"=>"<p>A) Parasitemia determined at day 20 post-infection in infected WT and IL-17RA KO mice adoptively transferred with WT neutrophils. Data are shown as mean ± SD, n = 6 per group. P values calculated with two-tailed T test. B) Concentration of IFN-γ in plasma of 20-day <i>T. cruzi</i> infected WT and IL-17R KO mice adoptively transferred with WT neutrophils. Data are shown as mean ± SD, n = 6 per group. P values calculated with two-tailed T test. C) Survival of <i>T. cruzi</i> infected WT and IL-17R KO mice adoptively transferred with WT neutrophils. P value calculated with a Gehan-Breslow-Wilcoxon test, n = 12 per group. D) Parasitemia determined at day 20 postinfection in infected WT mice adoptively transferred with WT and IL-10 KO neutrophils. Data are shown as mean ± SD, n = 12 per group. P values calculated with two-tailed T test. E) Concentration of IFN-γ in plasma of 20-day <i>T. cruzi</i> infected WT mice adoptively transferred with WT and IL-10 KO neutrophils. Data are shown as mean ± SD, n = 12 per group. P values calculated with two-tailed T test. F) Survival of <i>T. cruzi</i> infected WT mice adoptively transferred with WT and IL-10 KO neutrophils. P value calculated with a Gehan-Breslow-Wilcoxon test, n = 12 per group. Data in A–F are representative of two independent experiments.</p>", "links"=>[], "tags"=>["modulation", "adoptively", "transferred", "neutrophils"], "article_id"=>318255, "categories"=>["Infectious Diseases"], "users"=>["Jimena Tosello Boari", "María Carolina Amezcua Vesely", "Daniela Andrea Bermejo", "Maria Cecilia Ramello", "Carolina Lucía Montes", "Hugo Cejas", "Adriana Gruppi", "Eva Virginia Acosta Rodríguez"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002658.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IL_10_dependent_modulation_of_IFN_production_by_adoptively_transferred_neutrophils_during_T_cruzi_infection_/318255", "title"=>"IL-10-dependent modulation of IFN-γ production by adoptively transferred neutrophils during <i>T. cruzi</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-26 02:17:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/647920"], "description"=>"a<p>Scale: +: mild; ++:moderate; +++: severe; ++++: extremely severe.</p>b<p>PMN: Polymorphonuclear cells; Mo/Ly: monocyte/lymphocytes.</p>", "links"=>[], "tags"=>["lesions", "treated", "infected", "wt", "il-17ra", "ko", "mice", "20"], "article_id"=>318403, "categories"=>["Infectious Diseases"], "users"=>["Jimena Tosello Boari", "María Carolina Amezcua Vesely", "Daniela Andrea Bermejo", "Maria Cecilia Ramello", "Carolina Lucía Montes", "Hugo Cejas", "Adriana Gruppi", "Eva Virginia Acosta Rodríguez"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002658.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hepatic_lesions_in_anti_IFN_treated_T_cruzi_infected_WT_and_IL_17RA_KO_mice_at_day_20_post_infection_/318403", "title"=>"Hepatic lesions in anti-IFN-γ treated <i>T. cruzi</i> infected WT and IL-17RA KO mice at day 20 post-infection.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-04-26 02:20:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/647968"], "description"=>"a<p>Scale: +: mild; ++:moderate; +++: severe; ++++: extremely severe.</p>b<p>PMN: Polymorphonuclear cells; Mo/Ly: monocyte/lymphocytes.</p>", "links"=>[], "tags"=>["hepatic", "lesions", "infected", "wt", "il-17ra", "ko"], "article_id"=>318443, "categories"=>["Infectious Diseases"], "users"=>["Jimena Tosello Boari", "María Carolina Amezcua Vesely", "Daniela Andrea Bermejo", "Maria Cecilia Ramello", "Carolina Lucía Montes", "Hugo Cejas", "Adriana Gruppi", "Eva Virginia Acosta Rodríguez"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002658.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_course_study_of_hepatic_lesions_in_T_cruzi_infected_WT_and_IL_17RA_KO_mice_/318443", "title"=>"Time course study of hepatic lesions in <i>T. cruzi</i> infected WT and IL-17RA KO mice.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-04-26 02:20:43"}

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  • {"unique-ip"=>"16", "full-text"=>"23", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
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  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
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  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"19", "full-text"=>"16", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"19", "full-text"=>"16", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
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Relative Metric

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