The Danger Signal S100B Integrates Pathogen– and Danger–Sensing Pathways to Restrain Inflammation
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{"title"=>"The danger signal S100B integrates pathogen- and danger-sensing pathways to restrain inflammation", "type"=>"journal", "authors"=>[{"first_name"=>"Guglielmo", "last_name"=>"Sorci", "scopus_author_id"=>"7004744909"}, {"first_name"=>"Gloria", "last_name"=>"Giovannini", "scopus_author_id"=>"56240037500"}, {"first_name"=>"Francesca", "last_name"=>"Riuzzi", "scopus_author_id"=>"6507906497"}, {"first_name"=>"Pierluigi", "last_name"=>"Bonifazi", "scopus_author_id"=>"56266285100"}, {"first_name"=>"Teresa", "last_name"=>"Zelante", "scopus_author_id"=>"6504233929"}, {"first_name"=>"Silvia", "last_name"=>"Zagarella", "scopus_author_id"=>"35070753500"}, {"first_name"=>"Francesco", "last_name"=>"Bistoni", "scopus_author_id"=>"7102412384"}, {"first_name"=>"Rosario", "last_name"=>"Donato", "scopus_author_id"=>"7004951519"}, {"first_name"=>"Luigina", "last_name"=>"Romani", "scopus_author_id"=>"7101824161"}], "year"=>2011, "source"=>"PLoS Pathogens", "identifiers"=>{"pui"=>"361538250", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "issn"=>"15537366", "doi"=>"10.1371/journal.ppat.1001315", "scopus"=>"2-s2.0-79953281711", "pmid"=>"21423669", "sgr"=>"79953281711"}, "id"=>"20974d95-583f-3d2c-bed0-0c266e471de5", "abstract"=>"Humans inhale hundreds of Aspergillus conidia without adverse consequences. Powerful protective mechanisms may ensure prompt control of the pathogen and inflammation. Here we reveal a previously unknown mechanism by which the danger molecule S100B integrates pathogen- and danger-sensing pathways to restrain inflammation. Upon forming complexes with TLR2 ligands, S100B inhibited TLR2 via RAGE, through a paracrine epithelial cells/neutrophil circuit that restrained pathogen-induced inflammation. However, upon binding to nucleic acids, S100B activated intracellular TLRs eventually resolve danger-induced inflammation via transcriptional inhibition of S100B. Thus, the spatiotemporal regulation of TLRs and RAGE by S100B provides evidence for an evolving braking circuit in infection whereby an endogenous danger protects against pathogen-induced inflammation and a pathogen-sensing mechanism resolves danger-induced inflammation.", "link"=>"http://www.mendeley.com/research/danger-signal-s100b-integrates-pathogen-dangersensing-pathways-restrain-inflammation", "reader_count"=>60, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>16, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>3, "Other"=>4, "Student > Master"=>3, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>16, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>3, "Other"=>4, "Student > Master"=>3, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>32, "Medicine and Dentistry"=>11, "Neuroscience"=>3, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Veterinary Science and Veterinary Medicine"=>2, "Chemistry"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>4}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>11}, "Neuroscience"=>{"Neuroscience"=>3}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>32}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>2}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>2, "Brazil"=>1, "United Kingdom"=>1, "France"=>1}, "group_count"=>1}

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  • {"files"=>["https://ndownloader.figshare.com/files/792454"], "description"=>"<p>(<b>A</b>) Levels of p38 phosphorylation on purified epithelial cells from C57BL6 mice or TLR KO mice, unexposed (–) or exposed to <i>Aspergillus</i> resting (RC) or swollen (SC) conidia, 5 µg/ml MALP–2, 10 µg/ml Poly(I:C) or 10 µg/ml ODN–CpG for 8 h. (<b>B</b>) <i>Ifnb1</i> or <i>Ifna1</i> gene expression by real time RT–PCR on epithelial cells from C57BL6 mice exposed to Poly(I:C) in the presence of siS100B or 4 nM S100B. *<i>P</i><0.05, siRNA –treated <i>vs</i> untreated cells. Representative of 2 experiments. (<b>C</b>) S100B co-localization with fungal RNA in HEK293 cells pulsed with fungal RNA and stained with Syto17 red fluorescent nucleic acid stain and anti-S100B antibody followed by FITC-conjugated goat anti–rabbit. Mock-pulsed (control) and pulsed cells were analyzed on confocal microscope. (<b>D</b>) Fungal RNA stimulates epithelial cells via TLR3. Levels of IRF3 phosphorylation on lung epithelial cells exposed to Poly(I:C) or fungal RNA. Data are presented as immunoblots of cell lysates and fold increases (pixel density) in the phosphorylated to total protein ratios. (<b>E</b>) Immunoblots and pixel density of IKKβ and IKKα phosphorylation in epithelial cells from C57BL6 mice exposed as in (<b>A</b>). (<b>F</b>) Results from an ELISA procedure to monitor activation of p65, p52, and RelB in nuclear extract from epithelial cells exposed as in (<b>A</b>) for different lengths of time. Time 0 indicates untreated cells. Relative activities (A<sub>450</sub>) are mean±SE of two experiments, each in triplicate. *<i>P</i><0.05, treated vs untreated cells. (<b>G</b>) <i>s100b</i> gene expression by real time RT–PCR upon canonical/noncanonical NF–κB inhibition by siRNA in epithelial cells exposed to MALP–2 or Poly(I:C), as above. SB202190 (5 µM) was used as p38 inhibitor. *<i>P</i><0.05, siRNA–treated or p38–inhibited cells <i>vs</i> MALP–2 or Poly(I:C)–exposed cells. Representative of 2 experiments.</p>", "links"=>[], "tags"=>["tlr9", "inhibit"], "article_id"=>462811, "categories"=>["Immunology", "Microbiology", "Medicine"], "users"=>["Guglielmo Sorci", "Gloria Giovannini", "Francesca Riuzzi", "Pierluigi Bonifazi", "Teresa Zelante", "Silvia Zagarella", "Francesco Bistoni", "Rosario Donato", "Luigina Romani"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001315.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TLR3_and_TLR9_inhibit_s100b_expression_via_TRIF_noncanonical_NF_B_/462811", "title"=>"TLR3 and TLR9 inhibit <i>s100b</i> expression via TRIF/noncanonical NF–κB.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:46:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/792614"], "description"=>"<p>The figure shows that TLR2 activation on epithelial cells by the fungus resulted in the release of the Ca<sup>2+</sup>–binding protein, S100B, that paracrinally binds to RAGE, on polymorphonuclear neutrophils, and mediates its association with TLR2 with subsequent inhibition. However, S100B, upon binding to nucleic acids, also activates an intracellular TLR3/TLR9/TRIF–dependent pathway culminating in the transcriptional down-regulation of S100B. The transcriptional regulation of S100B by the sequential action of downstream MyD88– and TRIF–dependent NF–κB signalling pathways provides the molecular basis for an evolving braking circuit in infection whereby the endogenous danger protects the host against pathogen–induced inflammation and a nucleic acid–sensing mechanism resolves danger–induced chronic inflammation.</p>", "links"=>[], "tags"=>["signals", "tlrs", "s100b", "limits"], "article_id"=>462970, "categories"=>["Immunology", "Microbiology", "Medicine"], "users"=>["Guglielmo Sorci", "Gloria Giovannini", "Francesca Riuzzi", "Pierluigi Bonifazi", "Teresa Zelante", "Silvia Zagarella", "Francesco Bistoni", "Rosario Donato", "Luigina Romani"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001315.g007", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spatiotemporal_integration_of_signals_from_TLRs_and_RAGE_by_S100B_limits_pathogen_8211_and_danger_8211_induced_inflammation_/462970", "title"=>"Spatiotemporal integration of signals from TLRs and RAGE by S100B limits pathogen– and danger–induced inflammation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:49:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/792541"], "description"=>"<p>Fungal growth (CFU±SE) (<b>A</b>) and (<b>B</b>) <i>Mpo</i> expression by real time RT–PCR in the lung of TLR–deficient mice infected with <i>Aspergillus</i> conidia and treated with 50 ng/ml S100B as in legend to <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1001315#ppat-1001315-g003\" target=\"_blank\"><b>Fig. 3</b></a>. Data were obtained at 3 days postinfection. Representative of 4 experiments. <i>P</i>, treated vs untreated (None) mice.</p>", "links"=>[], "tags"=>["contingent", "tlr"], "article_id"=>462901, "categories"=>["Immunology", "Microbiology", "Medicine"], "users"=>["Guglielmo Sorci", "Gloria Giovannini", "Francesca Riuzzi", "Pierluigi Bonifazi", "Teresa Zelante", "Silvia Zagarella", "Francesco Bistoni", "Rosario Donato", "Luigina Romani"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001315.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_S100B_activity_in_vivo_is_contingent_upon_TLR_signaling_/462901", "title"=>"S100B activity <i>in vivo</i> is contingent upon TLR signaling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:48:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/791849"], "description"=>"<p>Expression of RAGE, HMGB1, S100B, S100A8 and S100A9 by RT–PCR (<b>A</b>), western blotting (<b>B, C</b>) and immunoistochemical staining (<b>D</b>) on the lungs of C57BL6 mice infected with <i>Aspergillus</i> conidia intranasally at different days postinfection (dpi). In <b>C</b>, S100B was assessed on BAL by western blotting. For immunohistochemistry, lung sections were incubated overnight with anti–S100B or anti–RAGE antibody followed by the secondary antibodies. Nuclei were counter–stained with DAPI. (<b>E</b>) Lung sections from transgenic mice expressing <i>s100b</i>–EGFP+ at different days postinfection. Bars, 100 µm. Microscopy was performed on a DM Rb epifluorescence microscope equipped with a digital camera. Representative of 2 experiments.</p>", "links"=>[], "tags"=>["damps", "pulmonary"], "article_id"=>462214, "categories"=>["Immunology", "Microbiology", "Medicine"], "users"=>["Guglielmo Sorci", "Gloria Giovannini", "Francesca Riuzzi", "Pierluigi Bonifazi", "Teresa Zelante", "Silvia Zagarella", "Francesco Bistoni", "Rosario Donato", "Luigina Romani"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001315.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RAGE_and_DAMPs_expression_in_pulmonary_aspergillosis_/462214", "title"=>"RAGE and DAMPs expression in pulmonary aspergillosis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:36:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/396341", "https://ndownloader.figshare.com/files/396374", "https://ndownloader.figshare.com/files/396403", "https://ndownloader.figshare.com/files/396426", "https://ndownloader.figshare.com/files/396457"], "description"=>"<div><p>Humans inhale hundreds of <em>Aspergillus</em> conidia without adverse consequences. Powerful protective mechanisms may ensure prompt control of the pathogen and inflammation. Here we reveal a previously unknown mechanism by which the danger molecule S100B integrates pathogen– and danger–sensing pathways to restrain inflammation. Upon forming complexes with TLR2 ligands, S100B inhibited TLR2 via RAGE, through a paracrine epithelial cells/neutrophil circuit that restrained pathogen-induced inflammation. However, upon binding to nucleic acids, S100B activated intracellular TLRs eventually resolve danger-induced inflammation via transcriptional inhibition of S100B. Thus, the spatiotemporal regulation of TLRs and RAGE by S100B provides evidence for an evolving braking circuit in infection whereby an endogenous danger protects against pathogen–induced inflammation and a pathogen–sensing mechanism resolves danger–induced inflammation.</p></div>", "links"=>[], "tags"=>["s100b", "integrates", "pathways", "restrain", "inflammation"], "article_id"=>138292, "categories"=>["Immunology", "Microbiology", "Medicine"], "users"=>["Guglielmo Sorci", "Gloria Giovannini", "Francesca Riuzzi", "Pierluigi Bonifazi", "Teresa Zelante", "Silvia Zagarella", "Francesco Bistoni", "Rosario Donato", "Luigina Romani"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1001315.s001", "https://dx.doi.org/10.1371/journal.ppat.1001315.s002", "https://dx.doi.org/10.1371/journal.ppat.1001315.s003", "https://dx.doi.org/10.1371/journal.ppat.1001315.s004", "https://dx.doi.org/10.1371/journal.ppat.1001315.s005"], "stats"=>{"downloads"=>7, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Danger_Signal_S100B_Integrates_Pathogen_and_Danger_Sensing_Pathways_to_Restrain_Inflammation/138292", "title"=>"The Danger Signal S100B Integrates Pathogen– and Danger–Sensing Pathways to Restrain Inflammation", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-03-10 02:18:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/792345"], "description"=>"<p>(<b>A</b>) Binding of S100B to TLR ligands by ELISA. S100B was incubated in microtiter plates coated with 10 µg/ml (as by preliminary experiments) of MALP–2, Zymosan, HSP70, LPS, Poly(I:C), fungal DNA or RNA, mammalian genomic DNA, Class B ODN–CpG (2006), nonstimulatory ODN–CpG (2310) and R–848 with and without 1 mM EGTA. Data indicate the mean ±SE of triplicates from three independent experiments. *<i>P</i><0.05, S100B vs no S100B (–). (<b>B</b>) Levels of ERK1/2 or p38 MAPK (30 min) in purified PMNs exposed to 5 µg/ml MALP–2, nanomolar or micromolar S100B, 20 µg/ml anti–S100B antibody, 5 µM SB202190, 300 nM HMGB1, alone or in combination, for 30 min as described. Data are presented as immunoblots of cell lysates with phosphorylation–specific antibodies and fold increases (pixel density) in the phosphorylated to total protein ratios. Representative of 2 experiments. (<b>C</b>) TLR2-transfected HEK293 cells were stimulated with MALP–2 for 30 min with and without 4 nM or µM S100B or 20 µg/ml anti–S100B antibody. Cell lysates were subjected to immunoprecipitation after overnight incubation with 2 µg/ml polyclonal anti–S100B or anti–RAGE antibody. Immunoprecipitates were probed with antibodies to the corresponding antigens. RT-PCR analysis confirmed that both RAGE and S100B were expressed on tranfected HEK293 cells and experiments in KO cells confirmed the specificity of the anti-RAGE antibody (data not shown). Representative of 2 experiments. (<b>D</b>) Direct visualization of RAGE interaction with TLR2 in the presence of nanomolar S100B by in situ proximity ligation assay (PLA). TLR2-transfected HEK293 cells were transiently transfected with a RAGE expression vector (pcDNA3/RAGE) or empty vector (pcDNA3) and stimulated with MALP–2 for 30 min with or without 4 nM or µM S100B or 20 µg/ml anti–S100B antibody. Cells were stained with anti-RAGE and anti-TLR2 antibodies, and subjected to PLA. (<b>E</b>) <i>s100b</i> gene–expression by real–time RT–PCR in different TLR-deficient mice at different days postinfection (dpi) with <i>Aspergillus</i> conidia intranasally. *<i>P</i><0.05, dpi 1 and 3 <i>vs</i> 0. (<b>F</b>) <i>S100b</i> gene–expression by real–time RT–PCR in lung of C57BL6 mice injected with 2.5 µg MALP–2, 10 µg LPS, 50 µg Poly(I:C), 50 µg Class B ODN–CpG 3 days before. <i>P</i>, treated <i>vs</i> untreated (–) mice. (<b>G</b>) H&E–stained sections from C57BL6 or RAGE KO mice injected as in <b>F</b>, 3 days before. Representative of 2 experiments.</p>", "links"=>[], "tags"=>["axis", "restrains"], "article_id"=>462710, "categories"=>["Immunology", "Microbiology", "Medicine"], "users"=>["Guglielmo Sorci", "Gloria Giovannini", "Francesca Riuzzi", "Pierluigi Bonifazi", "Teresa Zelante", "Silvia Zagarella", "Francesco Bistoni", "Rosario Donato", "Luigina Romani"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001315.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_S100B_RAGE_axis_restrains_TLR2_MyD88_8211_dependent_inflammation_/462710", "title"=>"The S100B/RAGE axis restrains TLR2/MyD88–dependent inflammation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:45:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/792002"], "description"=>"<p>Fungal growth (CFU±SE) (<b>A</b>), lung histology (PAS, H&E and Gomori stainings) and BAL morphometry (<b>B</b>), inflammatory chemokines and cytokine gene expression in the lungs by real–time RT–PCR (<b>C</b>), conidiocidal activity (<b>D</b>), oxidant production (<b>E</b>) in mice infected with live <i>Aspergillus</i> conidia intranasally. Note the sustained parenchymal damage (PAS staining in the upper panel of <b>Fig. 2B</b>), fungal growth (Gomori staining in the inset), and inflammatory cell recruitment in lungs (H&E staining in the lower panel) and BAL (May–Grünwald Giemsa–staining in the inset) in RAGE KO mice. Bars indicated magnifications. Dpi, days postinfection. BAL morphometry (numbers refer to % polymorphonuclear (PMN) or mononuclear (MNC) cells), lung RT–PCR, conidiocidal activity and oxidant production were assessed 3 days after the infection. Total lung cells, purified alveolar macrophages and PMNs were incubated with unopsonized resting conidia at 37°C for conidiocidal activity [percentage of colony forming units' inhibition (mean ± SE) at 60 min] or oxidant production by DHR. PMA, phorbol 12–myristate 13–acetate. *<i>P</i>, KO vs WT mice. Data are pooled from 4 experiments or representative of 2 experiments (for histology).</p>", "links"=>[], "tags"=>["mice"], "article_id"=>462367, "categories"=>["Immunology", "Microbiology", "Medicine"], "users"=>["Guglielmo Sorci", "Gloria Giovannini", "Francesca Riuzzi", "Pierluigi Bonifazi", "Teresa Zelante", "Silvia Zagarella", "Francesco Bistoni", "Rosario Donato", "Luigina Romani"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001315.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RAGE_8211_deficient_mice_develop_pathogen_8211_induced_inflammation_/462367", "title"=>"RAGE–deficient mice develop pathogen–induced inflammation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:39:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/792223"], "description"=>"<p>Fungal growth (CFU±SE) (<b>A</b>), lung histology (PAS staining) and BAL morphometry (May–Grünwald Giemsa–staining in the inset) (<b>B</b>) in C57BL6 or RAGE KO mice infected with <i>Aspergillus</i> live conidia intranasally and treated intraperitoneally for 3 consecutive days with different doses (ng/kg) S100B, 1 mg/kg anti–S100B or 0.5 mg/kg anti–RAGE antibodies. <i>P</i>, treated <i>vs</i> untreated (–) mice. NF–κB activation was assessed by western blotting (<b>C</b>) on lung cells from WT and KO mice, untreated (–) or treated with 50 or 500 ng/kg S100B, a day after the last treatment, or by nuclear translocation (indicated by arrowheads in <b>D</b>) on purified PMNs, unexposed (Ct, control) or exposed in vitro for 60 min to <i>Aspergillus</i> conidia alone (–) or in the presence of S100B at 4 nM or 4 µM. Western blotting data are presented as immunoblots of cell lysates with phosphorylation–specific antibodies and fold increases (pixel density) in the phosphorylated to total protein ratios. (<b>E</b>) Oxidant production was assessed PMNs exposed as in D (by DHR at 60 min). (<b>F</b>) <i>Fas</i> and <i>Bcl2</i> expressions were assessed by real–time RT–PCR after 6 h–exposure. Representative of 3 experiments. *<i>P</i><0.05, treated <i>vs</i> untreated (–) cells.</p>", "links"=>[], "tags"=>["s100b", "neutralization"], "article_id"=>462591, "categories"=>["Immunology", "Microbiology", "Medicine"], "users"=>["Guglielmo Sorci", "Gloria Giovannini", "Francesca Riuzzi", "Pierluigi Bonifazi", "Teresa Zelante", "Silvia Zagarella", "Francesco Bistoni", "Rosario Donato", "Luigina Romani"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1001315.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_S100B_administration_or_neutralization_on_aspergillosis_/462591", "title"=>"Effects of S100B administration or neutralization on aspergillosis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-10 00:43:11"}

PMC Usage Stats | Further Information

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Relative Metric

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