A Toll-Like Receptor 2 Pathway Regulates the Ppargc1a/b Metabolic Co-Activators in Mice with Staphylococcal aureus Sepsis
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{"title"=>"A toll-like receptor 2 pathway regulates the Ppargc1a/b metabolic co-activators in mice with Staphylococcal aureus sepsis", "type"=>"journal", "authors"=>[{"first_name"=>"Timothy E.", "last_name"=>"Sweeney", "scopus_author_id"=>"35752498100"}, {"first_name"=>"Hagir B.", "last_name"=>"Suliman", "scopus_author_id"=>"35566694800"}, {"first_name"=>"John W.", "last_name"=>"Hollingsworth", "scopus_author_id"=>"8075855000"}, {"first_name"=>"Karen E.", "last_name"=>"Welty-Wolf", "scopus_author_id"=>"6701489967"}, {"first_name"=>"Claude A.", "last_name"=>"Piantadosi", "scopus_author_id"=>"7102792526"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-80053151124", "sgr"=>"80053151124", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0025249", "pmid"=>"21966468", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "pui"=>"362627634"}, "id"=>"0520a157-1695-3350-a15e-3badcb85ecef", "abstract"=>"Activation of the host antibacterial defenses by the toll-like receptors (TLR) also selectively activates energy-sensing and metabolic pathways, but the mechanisms are poorly understood. This includes the metabolic and mitochondrial biogenesis master co-activators, Ppargc1a (PGC-1α) and Ppargc1b (PGC-1β) in Staphylococcus aureus (S. aureus) sepsis. The expression of these genes in the liver is markedly attenuated inTLR2(-/-) mice and markedly accentuated in TLR4(-/-) mice compared with wild type (WT) mice. We sought to explain this difference by using specific TLR-pathway knockout mice to test the hypothesis that these co-activator genes are directly regulated through TLR2 signaling. By comparing their responses to S. aureus with WT mice, we found that MyD88-deficient and MAL-deficient mice expressed hepatic Ppargc1a and Ppargc1b normally, but that neither gene was activated in TRAM-deficient mice. Ppargc1a/b activation did not require NF-kβ, but did require an interferon response factor (IRF), because neither gene was activated in IRF-3/7 double-knockout mice in sepsis, but both were activated normally in Unc93b1-deficient (3d) mice. Nuclear IRF-7 levels in TLR2(-/-) and TLR4(-/-) mice decreased and increased respectively post-inoculation and IRF-7 DNA-binding at the Ppargc1a promoter was demonstrated by chromatin immunoprecipitation. Also, a TLR2-TLR4-TRAM native hepatic protein complex was detected by immunoprecipitation within 6 h of S. aureus inoculation that could support MyD88-independent signaling to Ppargc1a/b. Overall, these findings disclose a novel MyD88-independent pathway in S. aureus sepsis that links TLR2 and TLR4 signaling in innate immunity to Ppargc1a/b gene regulation in a critical metabolic organ, the liver, by means of TRAM, TRIF, and IRF-7.", "link"=>"http://www.mendeley.com/research/tolllike-receptor-2-pathway-regulates-ppargc1ab-metabolic-coactivators-mice-staphylococcal-aureus-se", "reader_count"=>30, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Researcher"=>9, "Student > Ph. D. Student"=>9, "Student > Master"=>4, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Researcher"=>9, "Student > Ph. D. Student"=>9, "Student > Master"=>4, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>11, "Medicine and Dentistry"=>10, "Neuroscience"=>1, "Immunology and Microbiology"=>4}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>10}, "Neuroscience"=>{"Neuroscience"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>11}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>3}}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/369320"], "description"=>"<div><p>Activation of the host antibacterial defenses by the toll-like receptors (TLR) also selectively activates energy-sensing and metabolic pathways, but the mechanisms are poorly understood. This includes the metabolic and mitochondrial biogenesis master co-activators, <em>Ppargc1a</em> (PGC-1α) and <em>Ppargc1b</em> (PGC-1β) in <em>Staphylococcus aureus</em> (<em>S. aureus</em>) sepsis. The expression of these genes in the liver is markedly attenuated inTLR2<sup>−/−</sup> mice and markedly accentuated in TLR4<sup>−/−</sup> mice compared with wild type (WT) mice. We sought to explain this difference by using specific TLR-pathway knockout mice to test the hypothesis that these co-activator genes are directly regulated through TLR2 signaling. By comparing their responses to <em>S. aureus</em> with WT mice, we found that MyD88-deficient and MAL-deficient mice expressed hepatic <em>Ppargc1a</em> and <em>Ppargc1b</em> normally, but that neither gene was activated in TRAM-deficient mice. <em>Ppargc1a/b</em> activation did not require NF-kβ, but did require an interferon response factor (IRF), because neither gene was activated in IRF-3/7 double-knockout mice in sepsis, but both were activated normally in Unc93b1-deficient (3d) mice. Nuclear IRF-7 levels in TLR2<sup>−/−</sup> and TLR4<sup>−/−</sup> mice decreased and increased respectively post-inoculation and IRF-7 DNA-binding at the <em>Ppargc1a</em> promoter was demonstrated by chromatin immunoprecipitation. Also, a TLR2-TLR4-TRAM native hepatic protein complex was detected by immunoprecipitation within 6 h of <em>S. aureus</em> inoculation that could support MyD88-independent signaling to <em>Ppargc1a/b</em>. Overall, these findings disclose a novel MyD88-independent pathway in <em>S. aureus</em> sepsis that links TLR2 and TLR4 signaling in innate immunity to <em>Ppargc1a/b</em> gene regulation in a critical metabolic organ, the liver, by means of TRAM, TRIF, and IRF-7.</p> </div>", "links"=>[], "tags"=>["toll-like", "receptor", "pathway", "regulates", "metabolic", "co-activators", "mice", "sepsis"], "article_id"=>132973, "categories"=>["Cancer", "Medicine", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Toll_Like_Receptor_2_Pathway_Regulates_the_Ppargc1a_b_Metabolic_Co_Activators_in_Mice_with_Staphylococcal_aureus_Sepsis/132973", "title"=>"A Toll-Like Receptor 2 Pathway Regulates the <em>Ppargc1a/b</em> Metabolic Co-Activators in Mice with <em>Staphylococcal aureus</em> Sepsis", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-26 00:49:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/731673"], "description"=>"<p>Pathway 1 shows the canonical TLR2 MyD88-dependent signaling pathway that activates NF-kB after <i>S. aureus</i>. Pathway 2 shows TLR4 MyD88-dependent signaling to NF-kB and MyD88–independent signaling to TRIF/TRAM. Both MyD88 pathways have been excluded as causes of the <i>Ppargc1a</i> gene expression. Pathway 3 shows a putative TLR2-TLR4 heterodimer interacting with TRIF/TRAM. Pathway 4 indicates TLR2 in the TLR4 null state, as a homodimer or a heterodimer involving a non-TLR4 partner such as TLR1 or 6, interacting with TRIF/TRAM and unmasking the innate immune regulation of <i>Ppargc1a</i> expression. Pathway 5 shows canonical TLR3 endosome signaling also excluded in <i>Ppargc1</i> gene regulation after <i>S. aureus</i>; however, independent TLR3 activation partially rescues the <i>Ppargc1</i> phenotype in mice. TIRAP is Toll/interleukin-1 receptor domain-containing adapter protein (MAL); IRAK4 is Interleukin-1 receptor-associated kinase 4; TRAF3 and TRAF6 are TNF receptor-associated factor 3 and 6; TAK1 is TGF-beta-activated kinase 1 and TBK1 is NF-kappa-B-activating kinase.</p>", "links"=>[], "tags"=>["tlr", "signaling", "pathways", "metabolic", "co-activator", "activation"], "article_id"=>402025, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249.g009", "stats"=>{"downloads"=>6, "page_views"=>312, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Potential_TLR_signaling_pathways_for_Ppargc1_metabolic_co_activator_gene_activation_after_S_aureus_infection_/402025", "title"=>"Potential TLR signaling pathways for <i>Ppargc1</i> metabolic co-activator gene activation after <i>S. aureus</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-26 00:33:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/731467"], "description"=>"<p>Representative paraffin sections were stained for TLR2 in HC (top left) and 6 h PI (bottom left) and for TLR4 in HC (top right) and 6 h PI (bottom right). TLR staining is red; nuclear staining with DAPI is blue. B. Blue native PAGE on whole liver extracts from WT mice at 6 h after inoculation with <i>S. aureus</i>. Each blot shows three lanes: Lane 1, NativeMark molecular weight standard; Lane 2, sample in 0.5% DDM with no DTT or heating; lane 3, sample in 4% SDS with 100 mM DTT, boiled at 95°C for 5 min. At the left, Coomassie staining of entire blot showing molecular markers. Western blots were performed with anti-TLR2, TLR4, or TRAM. A complex near 300 kD was identified by all three primary antibodies (arrows) suggesting a possible interaction among the three proteins.</p>", "links"=>[], "tags"=>["tlr2", "tlr4", "localization", "wt", "immunofluorescence"], "article_id"=>401818, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249.g007", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_TLR2_and_TLR4_localization_in_WT_mouse_liver_by_immunofluorescence_microscopy_/401818", "title"=>"A. TLR2 and TLR4 localization in WT mouse liver by immunofluorescence microscopy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-26 00:30:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/731229"], "description"=>"<p>Hepatic mRNA levels of (A) <i>Ppargc1a</i> and (B) <i>Ppargc1b</i> were measured in WT, TRAM<sup>−/−</sup>, and TRIF<sup>−/−</sup> mice in healthy controls (HC) and at 6 h and 24 h PI by Q-PCR, compared with mRNA levels of (C) <i>Tnf</i> at 6 h PI (fold-induction compared to HC; n≥3 mice at each point for each strain); * <i>P</i><0.05 compared to HC of the same strain; #, <i>P</i><0.05, ##, <i>P</i><0.01 compared to WT data at 6 h. Bars are SD.</p>", "links"=>[], "tags"=>["mrna", "levels"], "article_id"=>401588, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ppargc1a_Ppargc1b_and_Tnf_mRNA_levels_in_S_aureus_sepsis_/401588", "title"=>"<i>Ppargc1a</i>, <i>Ppargc1b</i>, and <i>Tnf</i> mRNA levels in <i>S. aureus</i> sepsis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-26 00:26:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/731740"], "description"=>"<p>Antibodies and Primers.</p>", "links"=>[], "tags"=>["immunology", "Infectious diseases", "Critical care and emergency medicine"], "article_id"=>402095, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249.t001", "stats"=>{"downloads"=>2, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Antibodies_and_Primers_/402095", "title"=>"Antibodies and Primers.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-26 00:34:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/731097"], "description"=>"<p>Immunoblots are shown for NF-κB family members in nuclear extracts and in whole-liver extracts from WT, TLR2<sup>−/−</sup>, and TLR4<sup>−/−</sup> mice in HC and at 6 h PI (A). <i>Ppargc1a</i> and <i>Tnf</i> mRNA levels in <i>S. aureus</i> sepsis (B). <i>Ppargc1a</i> and <i>Tnf</i> mRNA levels at 6 h PI (compared to HC) were measured in WT, p50<sup>−/−</sup>, and BAY-11-7082-treated mice (n = 3 mice of each strain); * <i>P</i><0.01 compared with WT <i>Tnf</i> levels at 6 h PI. Vertical bars are SD.</p>", "links"=>[], "tags"=>["whole-cell"], "article_id"=>401455, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nuclear_p65_p50_and_c_rel_and_whole_cell_phospho_p65_/401455", "title"=>"Nuclear p65, p50, and c-rel, and whole-cell phospho-p65.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-26 00:24:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/731609"], "description"=>"<p>Hepatic mRNA levels of <i>Ppargc1a</i>, <i>Ppargc1b</i>, <i>Il10</i>, and <i>Tnf</i> were measured in healthy controls (HC) and in <i>S. aureus</i> sepsis at 6 h PI in WT and Unc93b1<sup>−/−</sup> mice. There was no significant difference between induction levels in WT and Unc93b1<sup>−/−</sup> mice for the four genes (n≥3 mice at each point for each strain). Vertical bars are SD.</p>", "links"=>[], "tags"=>["mrna", "levels"], "article_id"=>401962, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249.g008", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ppargc1a_Ppargc1b_Il10_and_Tnf_mRNA_levels_in_Unc93b1_8722_8722_mice_/401962", "title"=>"<i>Ppargc1a</i>, <i>Ppargc1b</i>, <i>Il10</i>, and <i>Tnf</i> mRNA levels in Unc93b1<sup>−/−</sup> mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-26 00:32:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/731032"], "description"=>"<p>Hepatic mRNA levels of <i>Tnf</i> (A), <i>Il6</i> (B), and <i>Il10</i> (C) were measured in WT, TLR2<sup>−/−</sup>, and TLR4<sup>−/−</sup> mice at 0 h (healthy control; HC), 6 h and 24 h PI in <i>S. aureus</i> sepsis. For each strain, n≥3 mice at each time point were compared with HC of the same strain. * <i>P</i><0.05, ** <i>P</i><0.01; # indicates higher and ## lower values than WT. Vertical bars are SD.</p>", "links"=>[], "tags"=>["mrna"], "article_id"=>401391, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tnf_Il6_and_Il10_mRNA_expression_/401391", "title"=>"<i>Tnf</i>, <i>Il6</i>, and <i>Il10</i> mRNA expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-26 00:23:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/731298"], "description"=>"<p>Immunoblots are shown for IRF-3 and IRF-7 in nuclear extracts from WT, TLR2<sup>−/−</sup>, and TLR4<sup>−/−</sup> mice in HC and at 6 h PI (One of duplicate experiments with two mice per strain). (C) Immunoblots for PGC-1α protein in WT, TLR2<sup>−/−</sup> and TLR4<sup>−/−</sup> mice at 0, 6, and 24 h after <i>S aureus</i> inoculation. Equal protein loading was confirmed by Coomassie blue staining. (D) Immunoblots for the mitochondrial VLCAD fatty acid oxidation enzyme in HC and at 6 h PI in WT, TLR2<sup>−/−</sup>, and TLR4<sup>−/−</sup> mice. Porin is a mitochondrial reference protein. (E) Chromatin Immunoprecipitation. ChIP for IRF7 binding on the <i>Ppargc1a</i> promoter at −289 bp from TSS. WT and TLR2<sup>−/−</sup> mice (HC, 6 h PI, and 24 h PI) were tested. Arrow shows the position of the binding. Pol II pull-downs on EF1a are shown as loading controls.</p>", "links"=>[], "tags"=>["immunoblots", "irf-3", "irf-7"], "article_id"=>401651, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nuclear_immunoblots_for_IRF_3_A_and_IRF_7_B_/401651", "title"=>"Nuclear immunoblots for IRF-3 (A) and IRF-7 (B).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-26 00:27:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/731367"], "description"=>"<p>Hepatic levels of (A) <i>Ppargc1a</i> and (B) <i>Ppargc1b</i> mRNA were measured in WT and IRF3/7<sup>−/−</sup> mice in healthy controls (HC) and at 6 h and 24 h PI (n≥3 at each point for each strain). (C) <i>Ppargc1a</i> mRNA levels after PolyI:C treatment with or without <i>S. aureus</i> sepsis. <i>Ppargc1a</i> mRNA levels were measured in WT and TLR2<sup>−/−</sup> mice in healthy controls (HC), in mice dosed with 400 ug PolyI:C, and in mice given PolyI:C plus <i>S. aureus</i> sepsis at 6 h and 24 h PI (n = 3 mice at each point for each strain *, <i>P</i><0.05 compared to HC of the same strain; ##, <i>P</i><0.05, #, <i>P</i> = 0.08 compared to WT at 6 h). Vertical bars are SD.</p>", "links"=>[], "tags"=>["mrna", "levels"], "article_id"=>401729, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ppargc1a_and_Ppargc1b_mRNA_levels_in_S_aureus_sepsis_/401729", "title"=>"<i>Ppargc1a</i> and <i>Ppargc1b</i> mRNA levels in <i>S. aureus</i> sepsis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-26 00:28:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/731161"], "description"=>"<p><i>Ppargc1a</i> (A) and <i>Ppargc1b</i> (B) mRNA levels were measured in WT, MyD88<sup>−/−</sup>, and MAL<sup>−/−</sup> mice in healthy controls (HC) and at 6 h and 24 h PI by Q-PCR, together with <i>Tnf</i> mRNA levels (C) at 6 h PI (fold-induction compared to HCs; n≥3 mice at each point for each strain); * <i>P</i><0.05, ** <i>P</i><0.01 compared to HC of the same strain. Vertical bars are SD.</p>", "links"=>[], "tags"=>["mrna", "levels"], "article_id"=>401522, "categories"=>["Medicine", "Infectious Diseases", "Immunology"], "users"=>["Timothy E. Sweeney", "Hagir B. Suliman", "John W. Hollingsworth", "Karen E. Welty-Wolf", "Claude A. Piantadosi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025249.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ppargc1a_Ppargc1b_and_Tnf_mRNA_levels_in_S_aureus_sepsis_/401522", "title"=>"<i>Ppargc1a</i>, <i>Ppargc1b</i>, and <i>Tnf</i> mRNA levels in <i>S. aureus</i> sepsis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-26 00:25:22"}

PMC Usage Stats | Further Information

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