Toxoplasma gondii Triggers Phosphorylation and Nuclear Translocation of Dendritic Cell STAT1 while Simultaneously Blocking IFNγ-Induced STAT1 Transcriptional Activity
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{"title"=>"Toxoplasma gondii Triggers Phosphorylation and Nuclear Translocation of Dendritic Cell STAT1 while Simultaneously Blocking IFNγ-Induced STAT1 Transcriptional Activity", "type"=>"journal", "authors"=>[{"first_name"=>"Anne G.", "last_name"=>"Schneider", "scopus_author_id"=>"55356941600"}, {"first_name"=>"Delbert S.", "last_name"=>"Abi Abdallah", "scopus_author_id"=>"35721489200"}, {"first_name"=>"Barbara A.", "last_name"=>"Butcher", "scopus_author_id"=>"7006188457"}, {"first_name"=>"Eric Y.", "last_name"=>"Denkers", "scopus_author_id"=>"7004256785"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"23527309", "doi"=>"10.1371/journal.pone.0060215", "sgr"=>"84875199094", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "scopus"=>"2-s2.0-84875199094", "issn"=>"19326203", "pui"=>"368562399"}, "id"=>"0105b4af-7a49-33db-a2e1-3e1cc08078a3", "abstract"=>"The protozoan Toxoplasma gondii actively modulates cytokine-induced JAK/STAT signaling pathways to facilitate survival within the host, including blocking IFNγ-mediated STAT1-dependent proinflammatory gene expression. We sought to further characterize inhibition of STAT1 signaling in infected murine dendritic cells (DC) because this cell type has not previously been examined, yet is known to serve as an early target of in vivo infection. Unexpectedly, we discovered that T. gondii infection alone induced sustained STAT1 phosphorylation and nuclear translocation in DC in a parasite strain-independent manner. Maintenance of STAT1 phosphorylation required active invasion but intracellular parasite replication was dispensable. The parasite rhoptry protein ROP16, recently shown to mediate STAT3 and STAT6 phosphorylation, was not required for STAT1 phosphorylation. In combination with IFNγ, T. gondii induced synergistic STAT1 phosphorylation and binding of aberrant STAT1-containing complexes to IFNγ consensus sequence oligonucleotides. Despite these findings, parasite infection blocked STAT1 binding to the native promoters of the IFNγ-inducible genes Irf-1 and Lrg47, along with subsequent gene expression. These results reinforce the importance of parasite-mediated blockade of IFNγ responses in dendritic cells, while simultaneously showing that T. gondii alone induces STAT1 phosphorylation.", "link"=>"http://www.mendeley.com/research/toxoplasma-gondii-triggers-phosphorylation-nuclear-translocation-dendritic-cell-stat1-while-simultan", "reader_count"=>38, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Student > Master"=>4, "Student > Bachelor"=>3, "Lecturer"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Student > Master"=>4, "Student > Bachelor"=>3, "Lecturer"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Agricultural and Biological Sciences"=>25, "Medicine and Dentistry"=>5, "Neuroscience"=>1, "Chemistry"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>2, "Biochemistry, Genetics and Molecular Biology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>25}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"United States"=>3, "Mexico"=>1, "Australia"=>1, "Germany"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/992461"], "description"=>"<p>(A) BMDC were left in medium alone (Med), infected with type I (RH), II (PTG) or III (M774.1) strains of <i>Toxoplasma</i> (3∶1 ratio of parasites to cells), or treated with murine IFNγ (100 ng/ml), prior to fractionation into cytoplasmic (C) and nuclear (N) extracts at the time points indicated. Samples were subjected to immunoblot analysis for phospho-Tyr701-STAT1 (pY-STAT1) and phospho-Ser-STAT1 (pS-STAT1). PARP and Rab5a served as loading controls for nuclear and cytoplasmic fractions, respectively. (B) Cells were infected with live parasites of the three strains as in (A) or exposed to heat-inactivated (HI) tachyzoites for six hours. Cytoplasmic and nuclear fractions were collected and immunoblot analyis was performed as in (A). (C) RH parasites were pre-treated for 10 min on ice with 1 μM cytochalasin D (CytD) prior to infection in the continued presence of the drug. Cells treated with the solvent DMSO alone served as controls. Cells were fractionated after six hours and subjected to immunoblot analysis for pY-STAT1. (D and E) BMDC were treated with IFNγ or infected with RH in comparison with either the <i>cps1-1</i> replication-deficient strain (D) or the ΔROP16 strain (E). Samples were fractionated after 6 and 20 hours and subjected to immunoblot analysis for pY-STAT1. All experiments were repeated at least three times with similar results.</p>", "links"=>[], "tags"=>["stat1", "phosphorylation", "translocation"], "article_id"=>656144, "categories"=>["Microbiology", "Immunology"], "users"=>["Anne G. Schneider", "Delbert S. Abi Abdallah", "Barbara A. Butcher", "Eric Y. Denkers"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060215.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Toxoplasma_induces_STAT1_phosphorylation_and_nuclear_translocation_in_BMDC_/656144", "title"=>"<i>Toxoplasma</i> induces STAT1 phosphorylation and nuclear translocation in BMDC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-21 01:35:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/992462"], "description"=>"<p>(A) BMDC were left in medium alone (Med), infected with type I (RH), type II (PTG) or type III (M774.1) strains of <i>Toxoplasma</i> (3∶1 ratio of parasites to cells) or treated with murine IFNγ (100 ng/ml). After 22 hours supernatants were collected (22 hr sup), centrifuged and filtered to remove debris and parasites, and subsequently transferred to additional untreated/uninfected BMDC for an additional 20 hours (B). For all samples (A and B), cytoplasmic (C) and nuclear (N) fractions were prepared and subjected to immunoblot analysis with phospho-Tyr701-STAT1 (pY-STAT1). PARP and Rab5a served as cytoplasmic and nuclear loading controls, respectively. (C – E) Cells were infected with the RH strain at a ratio of 0.5 parasites/cell for 20 hours, then subjected to intracellular staining for <i>Toxoplasma</i> (anti-p30/SAG-1) and pY-STAT1 prior to flow cytometric analysis. BMDC were gated on uninfected (D) and infected (E) populations to assess pY-STAT1 expression (blue lines) relative to staining with an isotype control antibody (red lines). All experiments were repeated at least twice with similar results.</p>", "links"=>[], "tags"=>["phosphorylation", "confined", "infected"], "article_id"=>656145, "categories"=>["Microbiology", "Immunology"], "users"=>["Anne G. Schneider", "Delbert S. Abi Abdallah", "Barbara A. Butcher", "Eric Y. Denkers"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060215.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_STAT1_phosphorylation_is_confined_to_infected_cells_/656145", "title"=>"STAT1 phosphorylation is confined to infected cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-21 01:35:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/992463"], "description"=>"<p>Nuclear extracts were prepared from cells infected with the RH parasite strain (Tg, <i>Toxoplasma gondii</i>; 3∶1 parasites to cells) or treated with IFNγ (100 ng/ml) for 6 hours. The <i>in vitro</i> binding activity of nuclear STAT1 to solid phase IFNγ-activated sequence (GAS) oligonucleotides was assessed using an ELISA-based method. Binding activity is expressed as fold increase over cells cultured in medium alone (Med, value of 1). +cOligo, addition of soluble competitive oligonucleotides; +mOligo, addition of mutated non-competitive oligonucleotides. The experiment was repeated three times with similar results. *, p<0.05 comparing nuclear extracts alone with nuclear extracts plus cOligo.</p>", "links"=>[], "tags"=>["stat1", "binding"], "article_id"=>656146, "categories"=>["Microbiology", "Immunology"], "users"=>["Anne G. Schneider", "Delbert S. Abi Abdallah", "Barbara A. Butcher", "Eric Y. Denkers"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060215.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Toxoplasma_induces_in_vitro_STAT1_binding_activity_in_BMDC_/656146", "title"=>"<i>Toxoplasma</i> induces <i>in vitro</i> STAT1 binding activity in BMDC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-21 01:36:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/992464"], "description"=>"<p>BMDC were left in medium alone (Med), infected with <i>Toxoplasma</i> (Tg, RH strain) at a ratio of 3 parasites per cell, treated with IFNγ (100 ng/ml), or infected with <i>Toxoplasma</i> followed 2 hours later by IFNγ treatment for the indicated times. In (A), cells were fractionated into cytosolic (C) and nuclear (N) extracts prior to immunoblot analysis for phospho-Tyr701-STAT1 (pY-STAT1). PARP and Rab5a served as loading controls for nuclear and cytoplasmic fractions, respectively. In (B) and (C), nuclear extracts were tested for binding to biotinylated probes containing the gamma-activated sequence (GAS) from the <i>Irf-1</i> promoter by EMSA. Supershift assays were also performed with samples in (C) using an antibody against STAT1α or normal rabbit IgG as a negative control. Experiments were repeated at least three times with similar results. GAF, gamma-activated factor (STAT1 homodimer).</p>", "links"=>[], "tags"=>["synergizes", "phosphorylation", "vitro", "binding"], "article_id"=>656147, "categories"=>["Microbiology", "Immunology"], "users"=>["Anne G. Schneider", "Delbert S. Abi Abdallah", "Barbara A. Butcher", "Eric Y. Denkers"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060215.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Toxoplasma_synergizes_with_IFN_in_terms_of_phosphorylation_and_in_vitro_binding_activity_of_STAT1_/656147", "title"=>"<i>Toxoplasma</i> synergizes with IFNγ in terms of phosphorylation and in vitro binding activity of STAT1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-21 01:36:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/992465"], "description"=>"<p>BMDC were infected with the RH strain of <i>T. gondii</i> (Tg, ratio of 3 parasites/cell), treated with treated IFNγ (100 ng/ml), or pre-infected for 2 hours with RH prior to addition of IFNγ (Tg+IFNγ). At the indicated time points post cytokine treatment, total RNA was harvested and reverse-transcribed to cDNA prior to qPCR amplification of the IFNγ-responsive, STAT1-dependent genes <i>Irf-1</i> (A) and <i>Lrg-47</i> (B). Fold change in gene expression is expressed relative to BMDC in medium alone. Samples were normalized to the house-keeping gene GAPDH. To assess native chromatin binding, ChIP was performed using an anti-STAT1α antibody followed by qPCR amplification with primers specific for the <i>Irf-1</i> promoter (C). Experimental conditions are replicated as in (A and B), with a time point of 2 hours shown. In (C), fold change in promoter binding is expressed relative to untreated cells (Med). Samples were normalized to input chromatin. Experiments were repeated at least three times with similar results.</p>", "links"=>[], "tags"=>["blocks", "stat1-dependent"], "article_id"=>656148, "categories"=>["Microbiology", "Immunology"], "users"=>["Anne G. Schneider", "Delbert S. Abi Abdallah", "Barbara A. Butcher", "Eric Y. Denkers"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060215.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Toxoplasma_blocks_IFN_driven_STAT1_dependent_gene_induction_/656148", "title"=>"<i>Toxoplasma</i> blocks IFNγ-driven STAT1-dependent gene induction.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-21 01:36:35"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[281, 484, 611, 728, 835, 934, 1030, 1123, 1214, 1299, 1383, 1464]}, {"subject_area"=>"/Medicine and health sciences", "average_usage"=>[264, 460, 584, 692, 794, 887, 978, 1067, 1154, 1241, 1328, 1408, 1474]}, {"subject_area"=>"/Medicine and health sciences/Parasitic diseases", "average_usage"=>[320, 619, 774, 903, 1012, 1118, 1224, 1333, 1442, 1518, 1600, 1702, 1779]}, {"subject_area"=>"/Physical sciences/Materials science", "average_usage"=>[250, 417, 535, 649, 758, 857, 952, 1036, 1113, 1206, 1287, 1353, 1429]}]}
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