A Salmonella Small Non-Coding RNA Facilitates Bacterial Invasion and Intracellular Replication by Modulating the Expression of Virulence Factors
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{"title"=>"A salmonella small non-coding rna facilitates bacterial invasion and intracellular replication by modulating the expression of virulence factors", "type"=>"journal", "authors"=>[{"first_name"=>"Hao", "last_name"=>"Gong", "scopus_author_id"=>"35847508800"}, {"first_name"=>"Gia Phong", "last_name"=>"Vu", "scopus_author_id"=>"35847823900"}, {"first_name"=>"Yong", "last_name"=>"Bai", "scopus_author_id"=>"55276494400"}, {"first_name"=>"Elton", "last_name"=>"Chan", "scopus_author_id"=>"36087145500"}, {"first_name"=>"Ruobin", "last_name"=>"Wu", "scopus_author_id"=>"55469405300"}, {"first_name"=>"Edward", "last_name"=>"Yang", "scopus_author_id"=>"24548979800"}, {"first_name"=>"Fenyong", "last_name"=>"Liu", "scopus_author_id"=>"35218137200"}, {"first_name"=>"Sangwei", "last_name"=>"Lu", "scopus_author_id"=>"7404227635"}], "year"=>2011, "source"=>"PLoS Pathogens", "identifiers"=>{"sgr"=>"80053458416", "doi"=>"10.1371/journal.ppat.1002120", "pui"=>"362681232", "issn"=>"15537366", "pmid"=>"21949647", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "scopus"=>"2-s2.0-80053458416"}, "id"=>"1534606e-2ad8-33f2-adba-47f890ef2974", "abstract"=>"Small non-coding RNAs (sRNAs) that act as regulators of gene expression have been identified in all kingdoms of life, including microRNA (miRNA) and small interfering RNA (siRNA) in eukaryotic cells. Numerous sRNAs identified in Salmonella are encoded by genes located at Salmonella pathogenicity islands (SPIs) that are commonly found in pathogenic strains. Whether these sRNAs are important for Salmonella pathogenesis and virulence in animals has not been reported. In this study, we provide the first direct evidence that a pathogenicity island-encoded sRNA, IsrM, is important for Salmonella invasion of epithelial cells, intracellular replication inside macrophages, and virulence and colonization in mice. IsrM RNA is expressed in vitro under conditions resembling those during infection in the gastrointestinal tract. Furthermore, IsrM is found to be differentially expressed in vivo, with higher expression in the ileum than in the spleen. IsrM targets the mRNAs coding for SopA, a SPI-1 effector, and HilE, a global regulator of the expression of SPI-1 proteins, which are major virulence factors essential for bacterial invasion. Mutations in IsrM result in disregulation of expression of HilE and SopA, as well as other SPI-1 genes whose expression is regulated by HilE. Salmonella with deletion of isrM is defective in bacteria invasion of epithelial cells and intracellular replication/survival in macrophages. Moreover, Salmonella with mutations in isrM is attenuated in killing animals and defective in growth in the ileum and spleen in mice. Our study has shown that IsrM sRNA functions as a pathogenicity island-encoded sRNA directly involved in Salmonella pathogenesis in animals. Our results also suggest that sRNAs may represent a distinct class of virulence factors that are important for bacterial infection in vivo.", "link"=>"http://www.mendeley.com/research/salmonella-small-noncoding-rna-facilitates-bacterial-invasion-intracellular-replication-modulating-e", "reader_count"=>128, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>10, "Researcher"=>23, "Student > Doctoral Student"=>11, "Student > Ph. D. Student"=>40, "Student > Postgraduate"=>6, "Student > Master"=>15, "Student > Bachelor"=>11, "Lecturer > Senior Lecturer"=>1, "Professor"=>7}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>10, "Researcher"=>23, "Student > Doctoral Student"=>11, "Student > Ph. D. Student"=>40, "Student > Postgraduate"=>6, "Student > Master"=>15, "Student > Bachelor"=>11, "Lecturer > Senior Lecturer"=>1, "Professor"=>7}, "reader_count_by_subject_area"=>{"Engineering"=>3, "Unspecified"=>5, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>23, "Agricultural and Biological Sciences"=>84, "Medicine and Dentistry"=>4, "Philosophy"=>1, "Psychology"=>1, "Social Sciences"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>4}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>84}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>23}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>1}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>3, "Germany"=>1, "India"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/735918"], "description"=>"<p>(A) Mortality of the BALB/c mice infected with isogenic strains carrying different constructs. BALB/c mice (5 animals per group) were infected intragastrically with <i>Salmonella</i> (5×10<sup>6</sup> CFU). (B) The numbers of bacteria (CFU) in spleen and ileum of the infected animals. Groups of BALB/c (5 animals per group) mice were infected intragastrically (IG) with 1×10<sup>5</sup> CFU of isogenic strains carrying different constructs, and bacteria were recovered from the organs at 7 days post inoculation. Each sample was analyzed in triplicate and the analysis was repeated at least three times. The CFU of the sample was expressed as the average of the values obtained. The concentrations of bacteria were recorded as CFU/ml of organ homogenate. The limit of bacteria detection in the organ homogenates was 10 CFU/ml.</p>", "links"=>[], "tags"=>["colonization"], "article_id"=>406270, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002120.g007", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Virulence_and_colonization_of_Salmonella_in_mice_/406270", "title"=>"Virulence and colonization of <i>Salmonella</i> in mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:44:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/735719"], "description"=>"<p>(A–B) Schematic representation of the proposed interactions of IsrM sRNA to <i>hilE</i> (A) and <i>sopA</i> mRNAs (B), and of compensatory base-pair changes. Numbers indicate relative position to the translational start site of <i>hilE</i> and <i>sopA</i> or position downstream of the transcriptional start site of <i>isrM</i>. Arrows denote nucleotide substitutions (in box) introduced to IsrM, and <i>hilE</i> and <i>sopA</i> mRNAs. The SD and AUG sequences are highlighted in blue and red, respectively. (C–D) Western blot analysis of <i>E. coli</i> carrying pLaco-IsrM, pLaco-H-IsrM and pLaco-S-IsrM, in combination with either wild type or mutant target plasmids, as indicated. The expression of the tagged HilE (C) and SopA (D) proteins was determined using that of GroEL as the internal control.</p>", "links"=>[], "tags"=>["targeting"], "article_id"=>406074, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002120.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Post_transcriptional_targeting_of_hilE_and_sopA_by_IsrM_/406074", "title"=>"Post-transcriptional targeting of <i>hilE</i> and <i>sopA</i> by IsrM.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:41:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/736150"], "description"=>"<p>Plasmid constructs used in the study.</p>", "links"=>[], "tags"=>["constructs"], "article_id"=>406503, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002120.t002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Plasmid_constructs_used_in_the_study_/406503", "title"=>"Plasmid constructs used in the study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-15 01:48:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/735585"], "description"=>"<p><i>Salmonella</i> was grown either <i>in vitro</i> (A–C) or in mice (D). Effect of pH values (A), osmolarity (B), and limitation of oxygen (C). Cultures of ST14028s were grown in culture media at different pH, at various concentrations of NaCl, or in the presence and limitation of oxygen. The values of the relative expression, which are the means from triplicate experiments, represent the ratios of the levels of IsrM under each pH condition to that under the control pH7.0 condition (A), the ratios of the levels of IsrM under different osmolarity conditions to that under the control condition of 170 mM NaCl as in regular LB broth (B), or the ratios of the level of IsrM under oxygen limitation to that under the control condition (i.e. in the presence of oxygen) (C). The analyses were repeated three times. The standard deviation is indicated by the error bars. (D) Level of IsrM from <i>Salmonella</i> recovered from the spleen and ileum of infected mice. SCID mice were intraperitoneally (IP) or intragastrically (IG) infected with ST14028s, and bacteria were recovered from the organs at 18 hours or 7 days post inoculation, respectively. The values in the IP and IG experiments, which are the means from triplicate experiments, represent the relative level of IsrM in ST14028s recovered from the spleen and ileum, as compared to the level of IsrM in <i>Salmonella</i> recovered from the spleen of the IP- and IG-infected mice at 18 hours post inoculation, respectively.</p>", "links"=>[], "tags"=>["isrm", "rna"], "article_id"=>405931, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002120.g002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_IsrM_RNA_in_Salmonella_/405931", "title"=>"Expression of IsrM RNA in <i>Salmonella</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:38:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/736080"], "description"=>"<p>Bacterial strains used in this study.</p>", "links"=>[], "tags"=>["strains"], "article_id"=>406435, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002120.t001", "stats"=>{"downloads"=>3, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bacterial_strains_used_in_this_study_/406435", "title"=>"Bacterial strains used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-15 01:47:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/371214", "https://ndownloader.figshare.com/files/371248", "https://ndownloader.figshare.com/files/371295", "https://ndownloader.figshare.com/files/371344", "https://ndownloader.figshare.com/files/371394"], "description"=>"<div><p>Small non-coding RNAs (sRNAs) that act as regulators of gene expression have been identified in all kingdoms of life, including microRNA (miRNA) and small interfering RNA (siRNA) in eukaryotic cells. Numerous sRNAs identified in <em>Salmonella</em> are encoded by genes located at <em>Salmonella</em> pathogenicity islands (SPIs) that are commonly found in pathogenic strains. Whether these sRNAs are important for <em>Salmonella</em> pathogenesis and virulence in animals has not been reported. In this study, we provide the first direct evidence that a pathogenicity island-encoded sRNA, IsrM, is important for <em>Salmonella</em> invasion of epithelial cells, intracellular replication inside macrophages, and virulence and colonization in mice. IsrM RNA is expressed <em>in vitro</em> under conditions resembling those during infection in the gastrointestinal tract. Furthermore, IsrM is found to be differentially expressed <em>in vivo</em>, with higher expression in the ileum than in the spleen. IsrM targets the mRNAs coding for SopA, a SPI-1 effector, and HilE, a global regulator of the expression of SPI-1 proteins, which are major virulence factors essential for bacterial invasion. Mutations in IsrM result in disregulation of expression of HilE and SopA, as well as other SPI-1 genes whose expression is regulated by HilE. <em>Salmonella</em> with deletion of <em>isrM</em> is defective in bacteria invasion of epithelial cells and intracellular replication/survival in macrophages. Moreover, <em>Salmonella</em> with mutations in <em>isrM</em> is attenuated in killing animals and defective in growth in the ileum and spleen in mice. Our study has shown that IsrM sRNA functions as a pathogenicity island-encoded sRNA directly involved in <em>Salmonella</em> pathogenesis in animals. Our results also suggest that sRNAs may represent a distinct class of virulence factors that are important for bacterial infection <em>in vivo</em>.</p> </div>", "links"=>[], "tags"=>["non-coding", "rna", "facilitates", "bacterial", "intracellular", "replication", "modulating", "virulence", "factors"], "article_id"=>133328, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002120.s001", "https://dx.doi.org/10.1371/journal.ppat.1002120.s002", "https://dx.doi.org/10.1371/journal.ppat.1002120.s003", "https://dx.doi.org/10.1371/journal.ppat.1002120.s004", "https://dx.doi.org/10.1371/journal.ppat.1002120.s005"], "stats"=>{"downloads"=>10, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Salmonella_Small_Non_Coding_RNA_Facilitates_Bacterial_Invasion_and_Intracellular_Replication_by_Modulating_the_Expression_of_Virulence_Factors/133328", "title"=>"A <em>Salmonella</em> Small Non-Coding RNA Facilitates Bacterial Invasion and Intracellular Replication by Modulating the Expression of Virulence Factors", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-15 00:55:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/736117"], "description"=>"<p>Primers used in the study.</p>", "links"=>[], "tags"=>[], "article_id"=>406475, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002120.t003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primers_used_in_the_study_/406475", "title"=>"Primers used in the study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-15 01:47:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/735792"], "description"=>"<p>The tagged proteins were expressed from strains T-hilE and ΔM-T-hilE (A), and T-sopA and ΔM-T-sopA (B). The expression of bacterial DnaK was used as the internal control. Protein samples were separated in SDS-polyacrylamide gels and reacted with antibodies against the FLAG sequence and DnaK. Each lane was loaded with lysate prepared from 5×10<sup>7</sup> CFU bacteria.</p>", "links"=>[], "tags"=>["blot", "tagged", "proteins"], "article_id"=>406140, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002120.g005", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Western_blot_analysis_of_the_expression_of_the_tagged_proteins_from_Salmonella_/406140", "title"=>"Western blot analysis of the expression of the tagged proteins from <i>Salmonella</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:42:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/735469"], "description"=>"<p>The transcription start sites, −10 boxes, −35 boxes, and transcription terminators of isrM genes are boxed and in red <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002120#ppat.1002120-PadalonBrauch1\" target=\"_blank\">[23]</a>. The targeting sequences for SopA and HilE mRNAs that were identified in this study are boxed and in green.</p>", "links"=>[], "tags"=>["sequences", "strains", "upstream", "promoter", "searches", "isrm"], "article_id"=>405815, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002120.g001", "stats"=>{"downloads"=>4, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Alignment_of_isrM_sequences_of_different_Salmonella_strains_including_the_upstream_promoter_region_based_on_BLAST_searches_of_the_IsrM_sequences_in_GenBank_/405815", "title"=>"Alignment of <i>isrM</i> sequences of different <i>Salmonella</i> strains including the upstream promoter region, based on BLAST searches of the IsrM sequences in GenBank.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:36:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/735659"], "description"=>"<p>(A–B) Western blot analyses of the expression of the tagged proteins from bacterial strains T-sopA and ΔM-T-sopA (A), and T-sopE2 and ΔM-T-sopE2 (B). The expression of bacterial DnaK was used as the internal control. Protein samples were separated in SDS-polyacrylamide gels and reacted with antibodies against the FLAG sequence and DnaK. Each lane was loaded with lysate prepared from 5×10<sup>7</sup> CFU bacteria. (C) The effect of the deletion of the <i>isrM</i> sequence on the expression of SPI-1 proteins. The values of the relative expression, which are the means of triplicate experiments, represent the ratios of the levels of the tagged proteins in ΔM-T-invJ, ΔM-T-sopE2, ΔM-T-sptP, ΔM-T-spaO, ΔM-T-sipD, ΔM-T-sipC, ΔM-T-sipB, ΔM-T-sipA, ΔM-T-sopB, and ΔM-T-sopA to those in T-invJ, T-sopE2, T-sptP, T-spaO, T-sipD, T-sipC, T-sipB, T-sipA, T-sopB, and T-sopA, respectively.</p>", "links"=>[], "tags"=>["tagged", "proteins"], "article_id"=>406006, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002120.g003", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_the_tagged_proteins_in_Salmonella_/406006", "title"=>"Expression of the tagged proteins in <i>Salmonella</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:40:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/735844"], "description"=>"<p>Isogenic <i>Salmonella</i> strains carrying different constructs were added to HeLa cells at a MOI of 10, and cell invasion was assayed by determining the ratio of the number of intracellular bacteria at 1 hour postinfection to the number of input bacteria. The ratio for wild-type strain ST14028s at 1 h postinfection was arbitrarily defined as 100%, and the ratios for other samples were expressed as relative values. For the intracellular replication assay, <i>Salmonella</i> was added to J774 macrophages at a MOI of 10. Intracellular growth was assayed by determining the ratio of the number of intracellular bacteria at 8 hour postinfection to the initial number of bacteria at time zero. The ratio for wild-type strain ST14028s at 8 h postinfection was arbitrarily defined as 100%, and the ratios for other samples were expressed as relative values. The data are the averages of three experiments performed in triplicate. The error bars indicate standard deviations.</p>", "links"=>[], "tags"=>["intracellular", "replication"], "article_id"=>406194, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Hao Gong", "Gia-Phong Vu", "Yong Bai", "Elton Chan", "Ruobin Wu", "Edward Yang", "Fenyong Liu", "Sangwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002120.g006", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Epithelial_cell_invasion_and_intracellular_replication_in_macrophages_/406194", "title"=>"Epithelial cell invasion and intracellular replication in macrophages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:43:14"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
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  • {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"6"}
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  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"1", "year"=>"2018", "month"=>"10"}
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  • {"unique-ip"=>"13", "full-text"=>"9", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2019", "month"=>"9"}
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  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
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  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"1", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"9", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"13", "full-text"=>"15", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
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Relative Metric

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