Enterococcus faecalis Infection Causes Inflammation, Intracellular Oxphos-Independent ROS Production, and DNA Damage in Human Gastric Cancer Cells
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{"title"=>"Enterococcus faecalis Infection Causes Inflammation, Intracellular Oxphos-Independent ROS Production, and DNA Damage in Human Gastric Cancer Cells", "type"=>"journal", "authors"=>[{"first_name"=>"Jesper A B", "last_name"=>"Strickertsson", "scopus_author_id"=>"45561709500"}, {"first_name"=>"Claus", "last_name"=>"Desler", "scopus_author_id"=>"22940305600"}, {"first_name"=>"Tomas", "last_name"=>"Martin-Bertelsen", "scopus_author_id"=>"54387349500"}, {"first_name"=>"Ana Manuel Dantas", "last_name"=>"Machado", "scopus_author_id"=>"8641383300"}, {"first_name"=>"Torkel", "last_name"=>"Wadstrøm", "scopus_author_id"=>"36050694600"}, {"first_name"=>"Ole", "last_name"=>"Winther", "scopus_author_id"=>"6701382702"}, {"first_name"=>"Lene Juel", "last_name"=>"Rasmussen", "scopus_author_id"=>"7201874444"}, {"first_name"=>"Lennart", "last_name"=>"Friis-Hansen", "scopus_author_id"=>"7004483675"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"23646188", "doi"=>"10.1371/journal.pone.0063147", "sgr"=>"84876988604", "scopus"=>"2-s2.0-84876988604", "issn"=>"19326203", "pui"=>"368837452"}, "id"=>"50478524-b4a1-3ac4-8633-481023972f61", "abstract"=>"BACKGROUND Achlorhydria caused by e.g. atrophic gastritis allows for bacterial overgrowth, which induces chronic inflammation and damage to the mucosal cells of infected individuals driving gastric malignancies and cancer. Enterococcus faecalis (E. faecalis) can colonize achlohydric stomachs and we therefore wanted to study the impact of E. faecalis infection on inflammatory response, reactive oxygen species (ROS) formation, mitochondrial respiration, and mitochondrial genetic stability in gastric mucosal cells. METHODS To separate the changes induced by bacteria from those of the inflammatory cells we established an in vitro E. faecalis infection model system using the gastric carcinoma cell line MKN74. Total ROS and superoxide was measured by fluorescence microscopy. Cellular oxygen consumption was characterized non-invasively using XF24 microplate based respirometry. Gene expression was examined by microarray, and response pathways were identified by Gene Set Analysis (GSA). Selected gene transcripts were verified by quantitative real-time polymerase chain reaction (qRT-PCR). Mitochondrial mutations were determined by sequencing. RESULTS Infection of MKN74 cells with E. faecalis induced intracellular ROS production through a pathway independent of oxidative phosphorylation (oxphos). Furthermore, E. faecalis infection induced mitochondrial DNA instability. Following infection, genes coding for inflammatory response proteins were transcriptionally up-regulated while DNA damage repair and cell cycle control genes were down-regulated. Cell growth slowed down when infected with viable E. faecalis and responded in a dose dependent manner to E. faecalis lysate. CONCLUSIONS Infection by E. faecalis induced an oxphos-independent intracellular ROS response and damaged the mitochondrial genome in gastric cell culture. Finally the bacteria induced an NF-κB inflammatory response as well as impaired DNA damage response and cell cycle control gene expression. TRANSCRIPT PROFILING Array Express accession number E-MEXP-3496.", "link"=>"http://www.mendeley.com/research/enterococcus-faecalis-infection-causes-inflammation-intracellular-oxphosindependent-ros-production-d", "reader_count"=>23, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Librarian"=>1, "Student > Doctoral Student"=>1, "Researcher"=>2, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>4, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Librarian"=>1, "Student > Doctoral Student"=>1, "Researcher"=>2, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>4, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>13, "Medicine and Dentistry"=>1, "Chemistry"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Republic of Singapore"=>1, "United States"=>1, "Brazil"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1048357"], "description"=>"<p>MKN74 cells infected with <i>E. faecalis</i> for 30 minutes at MOI50. (A) Representative fluorescence microscope image of MKN74 cells stained with ROS detecting probes (green) and superoxide detecting probes (orange) Scale bars  = 50 µm. (B) Quantification of fluorescence intensity using the LSM 510 software. A statistically significant increased intracellular production of ROS (p<0.01) and superoxide (p<0.02) in the infected cells compared to uninfected control cells was observed. * denotes significant difference. (C) Fluorescence image showing MKN74 plasma membrane (red) and <i>E. faecalis</i> (green) after 4 hours of infection. Flanking images show the YZ and XZ plane. (D) Split image of C. No evidence for bacterial invasion of the cells was observed.</p>", "links"=>[], "tags"=>["Molecular cell biology", "Cellular types", "Epithelial cells", "Eukaryotic cells", "Nucleic acids", "rna", "Cellular stress responses", "gene expression", "Gastroenterology and hepatology", "Bacterial and foodborne illness", "Gastrointestinal cancers", "Gastrointestinal infections", "oncology", "Basic cancer research", "Cancer risk factors", "induced", "intracellular", "ros"], "article_id"=>693783, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Jesper A. B. Strickertsson", "Claus Desler", "Tomas Martin-Bertelsen", "Ana Manuel Dantas Machado", "Torkel Wadstrøm", "Ole Winther", "Lene Juel Rasmussen", "Lennart Friis-Hansen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0063147.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_E_faecalis_infection_induced_intracellular_ROS_production_/693783", "title"=>"<i>E. faecalis</i> infection induced intracellular ROS production.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-30 01:03:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/1048359"], "description"=>"<p>MKN74 cells were incubated with or without <i>E. faecalis</i> for 4, 8 or 24 hours. Bacteria were removed and oxygen consumption rate was measured in an XF24 Extracellular Flux Analyzer. (A) ATP turnover, (B) respiratory capacity and (C) oxphos-independant oxygen consumption was determined as described in the text. <b>▪</b> =  Control cells, <b>ο</b>  =  <i>E. faecalis</i> infected cells. (n = 3–6, error bars indicate S.D. ** and *** denotes significant difference p<0.01 and p<0.001 respectively).</p>", "links"=>[], "tags"=>["Molecular cell biology", "Cellular types", "Epithelial cells", "Eukaryotic cells", "Nucleic acids", "rna", "Cellular stress responses", "gene expression", "Gastroenterology and hepatology", "Bacterial and foodborne illness", "Gastrointestinal cancers", "Gastrointestinal infections", "oncology", "Basic cancer research", "Cancer risk factors", "mkn74", "cells", "oxidative", "phosphorylation"], "article_id"=>693785, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Jesper A. B. Strickertsson", "Claus Desler", "Tomas Martin-Bertelsen", "Ana Manuel Dantas Machado", "Torkel Wadstrøm", "Ole Winther", "Lene Juel Rasmussen", "Lennart Friis-Hansen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0063147.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Intracellular_oxygen_consumption_in_MKN74_cells_was_independent_of_oxidative_phosphorylation_after_infection_/693785", "title"=>"Intracellular oxygen consumption in MKN74 cells was independent of oxidative phosphorylation after infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-30 01:03:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/1048362"], "description"=>"<p>Mutations detected in the mtDNA D-loop region after infection. MKN74 cells were infected with <i>E. faecalis</i> at MOI 10 for 5 days. Infected MKN74 cell cultures had a significantly higher number of total mutations and transition mutations than non-infected control cell cultures. * denotes significantly different from untreated cells p<0.05.</p>", "links"=>[], "tags"=>["Molecular cell biology", "Cellular types", "Epithelial cells", "Eukaryotic cells", "Nucleic acids", "rna", "Cellular stress responses", "gene expression", "Gastroenterology and hepatology", "Bacterial and foodborne illness", "Gastrointestinal cancers", "Gastrointestinal infections", "oncology", "Basic cancer research", "Cancer risk factors", "mitochondrial", "mutations", "mkn74"], "article_id"=>693788, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Jesper A. B. Strickertsson", "Claus Desler", "Tomas Martin-Bertelsen", "Ana Manuel Dantas Machado", "Torkel Wadstrøm", "Ole Winther", "Lene Juel Rasmussen", "Lennart Friis-Hansen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0063147.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_E_faecalis_infection_increased_mitochondrial_mutations_in_MKN74_cells_/693788", "title"=>"<i>E. faecalis</i> infection increased mitochondrial mutations in MKN74 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-30 01:03:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/1048363"], "description"=>"<p>(A) A section of the GSA result. From the portion of gene sets significantly enriched in MKN74 cells infected for 24 hours, a subset of gene sets were manually selected by association with inflammatory response and response to ROS. The numbers in hard brackets indicate effective number of genes in the gene set. The title of each gene set corresponds to the title given on the MSigDB website. Numbers in colored boxes are adjusted p-values (q-values), black indicate statistical significance at 1% Fdr. (B) Characterization by qRT-PCR of transcripts coding for important cytokines and chemokines after <i>E. faecalis</i> infection for 24 hours (MOI50) and 5 days (MOI10). * denotes significantly different from untreated cells p<0.05.</p>", "links"=>[], "tags"=>["Molecular cell biology", "Cellular types", "Epithelial cells", "Eukaryotic cells", "Nucleic acids", "rna", "Cellular stress responses", "gene expression", "Gastroenterology and hepatology", "Bacterial and foodborne illness", "Gastrointestinal cancers", "Gastrointestinal infections", "oncology", "Basic cancer research", "Cancer risk factors", "stimulated", "up-regulation", "transcripts", "inflammatory", "ros"], "article_id"=>693789, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Jesper A. B. Strickertsson", "Claus Desler", "Tomas Martin-Bertelsen", "Ana Manuel Dantas Machado", "Torkel Wadstrøm", "Ole Winther", "Lene Juel Rasmussen", "Lennart Friis-Hansen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0063147.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Infection_stimulated_an_up_regulation_of_several_transcripts_involved_in_inflammatory_and_ROS_response_pathways_/693789", "title"=>"Infection stimulated an up-regulation of several transcripts involved in inflammatory and ROS response pathways.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-30 01:03:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1048365"], "description"=>"<p>(A) A section of the GSA result after 24 hours of infection. Gene sets associated with DNA damage repair with same setup as <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0063147#pone-0063147-g004\" target=\"_blank\">figure 4</a> A. (B) Characterization of transcripts coding for important genes involved in MMR after <i>E. faecalis</i> infection for 24 hours (MOI50) and 5 days (MOI10). * denotes significantly different from untreated cells p<0.05.</p>", "links"=>[], "tags"=>["Molecular cell biology", "Cellular types", "Epithelial cells", "Eukaryotic cells", "Nucleic acids", "rna", "Cellular stress responses", "gene expression", "Gastroenterology and hepatology", "Bacterial and foodborne illness", "Gastrointestinal cancers", "Gastrointestinal infections", "oncology", "Basic cancer research", "Cancer risk factors", "stimulated", "up-regulation", "transcripts", "dna"], "article_id"=>693791, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Jesper A. B. Strickertsson", "Claus Desler", "Tomas Martin-Bertelsen", "Ana Manuel Dantas Machado", "Torkel Wadstrøm", "Ole Winther", "Lene Juel Rasmussen", "Lennart Friis-Hansen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0063147.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Infection_stimulated_an_up_regulation_of_several_transcripts_involved_in_DNA_damage_response_pathways_/693791", "title"=>"Infection stimulated an up-regulation of several transcripts involved in DNA damage response pathways.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-30 01:03:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/1048367"], "description"=>"<p>(A) A section of the GSA result after 24 hours of infection. Gene sets associated with cell cycle control with same setup as <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0063147#pone-0063147-g004\" target=\"_blank\">figure 4</a> A. (B) MKN74 growth assay. The fold change in number of cells relative to day zero is shown. The growth of MKN74 cells, infected with viable <i>E. faecalis</i> at a MOI of 10 or with different concentrations of bacterial lysate, was followed for a period of five days. Uninfected cells served as controls. Cell density was measured by crystal violet absorbance. ** and *** denotes significant difference p<0.01 and p<0.001 respectively.</p>", "links"=>[], "tags"=>["Molecular cell biology", "Cellular types", "Epithelial cells", "Eukaryotic cells", "Nucleic acids", "rna", "Cellular stress responses", "gene expression", "Gastroenterology and hepatology", "Bacterial and foodborne illness", "Gastrointestinal cancers", "Gastrointestinal infections", "oncology", "Basic cancer research", "Cancer risk factors", "caused", "down-regulation", "transcripts", "lysate", "slowed"], "article_id"=>693793, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Jesper A. B. Strickertsson", "Claus Desler", "Tomas Martin-Bertelsen", "Ana Manuel Dantas Machado", "Torkel Wadstrøm", "Ole Winther", "Lene Juel Rasmussen", "Lennart Friis-Hansen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0063147.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Infection_caused_a_down_regulation_of_transcripts_involved_in_cell_cycle_control_pathways_and_E_faecalis_lysate_slowed_down_cell_proliferation_/693793", "title"=>"Infection caused a down-regulation of transcripts involved in cell cycle control pathways, and <i>E. faecalis</i> lysate slowed down cell proliferation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-30 01:03:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/1048369"], "description"=>"<p>Proposed model for how chronic infection by pathogenic bacteria affects gastric epithelial cells.</p>", "links"=>[], "tags"=>["Molecular cell biology", "Cellular types", "Epithelial cells", "Eukaryotic cells", "Nucleic acids", "rna", "Cellular stress responses", "gene expression", "Gastroenterology and hepatology", "Bacterial and foodborne illness", "Gastrointestinal cancers", "Gastrointestinal infections", "oncology", "Basic cancer research", "Cancer risk factors", "pathogenic", "gastric", "epithelial"], "article_id"=>693795, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Jesper A. B. Strickertsson", "Claus Desler", "Tomas Martin-Bertelsen", "Ana Manuel Dantas Machado", "Torkel Wadstrøm", "Ole Winther", "Lene Juel Rasmussen", "Lennart Friis-Hansen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0063147.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proposed_model_for_how_chronic_infection_by_pathogenic_bacteria_affects_gastric_epithelial_cells_/693795", "title"=>"Proposed model for how chronic infection by pathogenic bacteria affects gastric epithelial cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-30 01:03:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/1048370"], "description"=>"<p>Selected genes are shown. The table shows expressional fold change of selected genes in MKN74 cells infected with <i>E. faecalis</i> for 24 hours and 5 days. Difference of means  =  difference in arbitrary expressional level of control cells and infected cells. *  =  P value <0.05.</p>", "links"=>[], "tags"=>["Molecular cell biology", "Cellular types", "Epithelial cells", "Eukaryotic cells", "Nucleic acids", "rna", "Cellular stress responses", "gene expression", "Gastroenterology and hepatology", "Bacterial and foodborne illness", "Gastrointestinal cancers", "Gastrointestinal infections", "oncology", "Basic cancer research", "Cancer risk factors", "inflammatory", "mkn74", "cells", "microarray"], "article_id"=>693796, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Jesper A. B. Strickertsson", "Claus Desler", "Tomas Martin-Bertelsen", "Ana Manuel Dantas Machado", "Torkel Wadstrøm", "Ole Winther", "Lene Juel Rasmussen", "Lennart Friis-Hansen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0063147.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genes_involved_in_the_inflammatory_response_of_MKN74_cells_identified_by_microarray_analysis_/693796", "title"=>"Genes involved in the inflammatory response of MKN74 cells identified by microarray analysis.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-04-30 01:03:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1048374", "https://ndownloader.figshare.com/files/1048376", "https://ndownloader.figshare.com/files/1048383", "https://ndownloader.figshare.com/files/1048384", "https://ndownloader.figshare.com/files/1048386", "https://ndownloader.figshare.com/files/1048389", "https://ndownloader.figshare.com/files/1048391"], "description"=>"<div><p>Background</p><p>Achlorhydria caused by e.g. atrophic gastritis allows for bacterial overgrowth, which induces chronic inflammation and damage to the mucosal cells of infected individuals driving gastric malignancies and cancer. <i>Enterococcus faecalis</i> (<i>E. faecalis</i>) can colonize achlohydric stomachs and we therefore wanted to study the impact of <i>E. faecalis</i> infection on inflammatory response, reactive oxygen species (ROS) formation, mitochondrial respiration, and mitochondrial genetic stability in gastric mucosal cells.</p><p>Methods</p><p>To separate the changes induced by bacteria from those of the inflammatory cells we established an <i>in vitro E. faecalis</i> infection model system using the gastric carcinoma cell line MKN74. Total ROS and superoxide was measured by fluorescence microscopy. Cellular oxygen consumption was characterized non-invasively using XF24 microplate based respirometry. Gene expression was examined by microarray, and response pathways were identified by Gene Set Analysis (GSA). Selected gene transcripts were verified by quantitative real-time polymerase chain reaction (qRT-PCR). Mitochondrial mutations were determined by sequencing.</p><p>Results</p><p>Infection of MKN74 cells with <i>E. faecalis</i> induced intracellular ROS production through a pathway independent of oxidative phosphorylation (oxphos). Furthermore, <i>E. faecalis</i> infection induced mitochondrial DNA instability. Following infection, genes coding for inflammatory response proteins were transcriptionally up-regulated while DNA damage repair and cell cycle control genes were down-regulated. Cell growth slowed down when infected with viable <i>E. faecalis</i> and responded in a dose dependent manner to <i>E. faecalis</i> lysate.</p><p>Conclusions</p><p>Infection by <i>E. faecalis</i> induced an oxphos-independent intracellular ROS response and damaged the mitochondrial genome in gastric cell culture. Finally the bacteria induced an NF-κB inflammatory response as well as impaired DNA damage response and cell cycle control gene expression.</p><p>Transcript profiling</p><p>Array Express accession number E-MEXP-3496.</p></div>", "links"=>[], "tags"=>["Molecular cell biology", "Cellular types", "Epithelial cells", "Eukaryotic cells", "Nucleic acids", "rna", "Cellular stress responses", "gene expression", "Gastroenterology and hepatology", "Bacterial and foodborne illness", "Gastrointestinal cancers", "Gastrointestinal infections", "oncology", "Basic cancer research", "Cancer risk factors", "causes", "intracellular", "oxphos-independent", "ros", "dna", "gastric", "cancer", "cells"], "article_id"=>693800, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Jesper A. B. Strickertsson", "Claus Desler", "Tomas Martin-Bertelsen", "Ana Manuel Dantas Machado", "Torkel Wadstrøm", "Ole Winther", "Lene Juel Rasmussen", "Lennart Friis-Hansen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0063147.s001", "https://dx.doi.org/10.1371/journal.pone.0063147.s002", "https://dx.doi.org/10.1371/journal.pone.0063147.s003", "https://dx.doi.org/10.1371/journal.pone.0063147.s004", "https://dx.doi.org/10.1371/journal.pone.0063147.s005", "https://dx.doi.org/10.1371/journal.pone.0063147.s006", "https://dx.doi.org/10.1371/journal.pone.0063147.s007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Enterococcus_faecalis_Infection_Causes_Inflammation_Intracellular_Oxphos_Independent_ROS_Production_and_DNA_Damage_in_Human_Gastric_Cancer_Cells/693800", "title"=>"<i>Enterococcus faecalis</i> Infection Causes Inflammation, Intracellular Oxphos-Independent ROS Production, and DNA Damage in Human Gastric Cancer Cells", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-04-30 01:03:20"}

PMC Usage Stats | Further Information

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Relative Metric

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