Modeling the Regulatory Mechanisms by Which NLRX1 Modulates Innate Immune Responses to Helicobacter pylori Infection
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{"title"=>"Modeling the regulatory mechanisms by which NLRX1 modulates innate immune responses to Helicobacter pylori infection", "type"=>"journal", "authors"=>[{"first_name"=>"Casandra W.", "last_name"=>"Philipson", "scopus_author_id"=>"55613529300"}, {"first_name"=>"Josep", "last_name"=>"Bassaganya-Riera", "scopus_author_id"=>"6603033549"}, {"first_name"=>"Monica", "last_name"=>"Viladomiu", "scopus_author_id"=>"42962600000"}, {"first_name"=>"Barbara", "last_name"=>"Kronsteiner", "scopus_author_id"=>"17135052500"}, {"first_name"=>"Vida", "last_name"=>"Abedi", "scopus_author_id"=>"36116538600"}, {"first_name"=>"Stefan", "last_name"=>"Hoops", "scopus_author_id"=>"15128967000"}, {"first_name"=>"Pawel", "last_name"=>"Michalak", "scopus_author_id"=>"6603442556"}, {"first_name"=>"Lin", "last_name"=>"Kang", "scopus_author_id"=>"55277177700"}, {"first_name"=>"Stephen E.", "last_name"=>"Girardin", "scopus_author_id"=>"6602157821"}, {"first_name"=>"Raquel", "last_name"=>"Hontecillas", "scopus_author_id"=>"6602639316"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "doi"=>"10.1371/journal.pone.0137839", "sgr"=>"84947416904", "scopus"=>"2-s2.0-84947416904", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"26367386", "pui"=>"606945787"}, "id"=>"28662e0e-f9ab-37b7-b98d-7f536f9812dc", "abstract"=>"Helicobacter pylori colonizes half of the world's population as the dominant member of the gastric microbiota resulting in a lifelong chronic infection. Host responses toward the bacterium can result in asymptomatic, pathogenic or even favorable health outcomes; however, mechanisms underlying the dual role of H. pylori as a commensal versus pathogenic organism are not well characterized. Recent evidence suggests mononuclear phagocytes are largely involved in shaping dominant immunity during infection mediating the balance between host tolerance and succumbing to overt disease. We combined computational modeling, bioinformatics and experimental validation in order to investigate interactions between macrophages and intracellular H. pylori. Global transcriptomic analysis on bone marrow-derived macrophages (BMDM) in a gentamycin protection assay at six time points unveiled the presence of three sequential host response waves: an early transient regulatory gene module followed by sustained and late effector responses. Kinetic behaviors of pattern recognition receptors (PRRs) are linked to differential expression of spatiotemporal response waves and function to induce effector immunity through extracellular and intracellular detection of H. pylori. We report that bacterial interaction with the host intracellular environment caused significant suppression of regulatory NLRC3 and NLRX1 in a pattern inverse to early regulatory responses. To further delineate complex immune responses and pathway crosstalk between effector and regulatory PRRs, we built a computational model calibrated using time-series RNAseq data. Our validated computational hypotheses are that: 1) NLRX1 expression regulates bacterial burden in macrophages; and 2) early host response cytokines down-regulate NLRX1 expression through a negative feedback circuit. This paper applies modeling approaches to characterize the regulatory role of NLRX1 in mechanisms of host tolerance employed by macrophages to respond to and/or to co-exist with intracellular H. pylori.", "link"=>"http://www.mendeley.com/research/modeling-regulatory-mechanisms-nlrx1-modulates-innate-immune-responses-helicobacter-pylori-infection", "reader_count"=>24, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>4, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>1, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>4}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>4, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>1, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>4}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>3, "Mathematics"=>1, "Medicine and Dentistry"=>6, "Agricultural and Biological Sciences"=>9, "Neuroscience"=>1, "Physics and Astronomy"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Neuroscience"=>{"Neuroscience"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>9}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Mathematics"=>{"Mathematics"=>1}}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2263777"], "description"=>"<p>Clustering analysis was performed on differentially expressed genes (FDR p-value <0.05) obtained from RNAseq performed on macrophages co-cultured with <i>H</i>. <i>pylori</i>. Values are presented as the log2 (ratio) of average infected (n = 3) to average non-infected (n = 3) for each time point (0, 60, 120, 240, 360 and 720 min post-co-culture). Transcripts were grouped into 12 gene-modules based on expression levels and temporal behavior. Gene expression profiles for each cluster are plotted with representative members (M) and similarities in function identified by Gene Ontology (GO).</p>", "links"=>[], "tags"=>["gentamycin protection assay", "effector", "prr", "host tolerance", "Helicobacter pylori Infection Helicobacter pylori colonizes half", "host intracellular environment", "intracellular H", "modeling", "expression", "NLRX 1 Modulates Innate Immune Responses", "NLRX 1", "bmdm", "sequential host response waves", "spatiotemporal response waves", "Global Transcriptomic Analysis", "Pattern recognition receptors", "macrophage", "NLRC"], "article_id"=>1543368, "categories"=>["Uncategorised"], "users"=>["Casandra W. Philipson", "Josep Bassaganya-Riera", "Monica Viladomiu", "Barbara Kronsteiner", "Vida Abedi", "Stefan Hoops", "Pawel Michalak", "Lin Kang", "Stephen E. Girardin", "Raquel Hontecillas"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137839.g001", "stats"=>{"downloads"=>2, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Intracellular_Helicobacter_pylori_induces_temporal_waves_in_macrophage_immunity_/1543368", "title"=>"Intracellular <i>Helicobacter pylori</i> induces temporal waves in macrophage immunity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-14 05:26:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/2263785", "https://ndownloader.figshare.com/files/2263786", "https://ndownloader.figshare.com/files/2263787"], "description"=>"<div><p><i>Helicobacter pylori</i> colonizes half of the world’s population as the dominant member of the gastric microbiota resulting in a lifelong chronic infection. Host responses toward the bacterium can result in asymptomatic, pathogenic or even favorable health outcomes; however, mechanisms underlying the dual role of <i>H</i>. <i>pylori</i> as a commensal versus pathogenic organism are not well characterized. Recent evidence suggests mononuclear phagocytes are largely involved in shaping dominant immunity during infection mediating the balance between host tolerance and succumbing to overt disease. We combined computational modeling, bioinformatics and experimental validation in order to investigate interactions between macrophages and intracellular <i>H</i>. <i>pylori</i>. Global transcriptomic analysis on bone marrow-derived macrophages (BMDM) in a gentamycin protection assay at six time points unveiled the presence of three sequential host response waves: an early transient regulatory gene module followed by sustained and late effector responses. Kinetic behaviors of pattern recognition receptors (PRRs) are linked to differential expression of spatiotemporal response waves and function to induce effector immunity through extracellular and intracellular detection of <i>H</i>. <i>pylori</i>. We report that bacterial interaction with the host intracellular environment caused significant suppression of regulatory NLRC3 and NLRX1 in a pattern inverse to early regulatory responses. To further delineate complex immune responses and pathway crosstalk between effector and regulatory PRRs, we built a computational model calibrated using time-series RNAseq data. Our validated computational hypotheses are that: 1) NLRX1 expression regulates bacterial burden in macrophages; and 2) early host response cytokines down-regulate NLRX1 expression through a negative feedback circuit. This paper applies modeling approaches to characterize the regulatory role of NLRX1 in mechanisms of host tolerance employed by macrophages to respond to and/or to co-exist with intracellular <i>H</i>. <i>pylori</i>.</p></div>", "links"=>[], "tags"=>["gentamycin protection assay", "effector", "prr", "host tolerance", "Helicobacter pylori Infection Helicobacter pylori colonizes half", "host intracellular environment", "intracellular H", "modeling", "expression", "NLRX 1 Modulates Innate Immune Responses", "NLRX 1", "bmdm", "sequential host response waves", "spatiotemporal response waves", "Global Transcriptomic Analysis", "Pattern recognition receptors", "macrophage", "NLRC"], "article_id"=>1543376, "categories"=>["Uncategorised"], "users"=>["Casandra W. Philipson", "Josep Bassaganya-Riera", "Monica Viladomiu", "Barbara Kronsteiner", "Vida Abedi", "Stefan Hoops", "Pawel Michalak", "Lin Kang", "Stephen E. Girardin", "Raquel Hontecillas"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0137839.s001", "https://dx.doi.org/10.1371/journal.pone.0137839.s002", "https://dx.doi.org/10.1371/journal.pone.0137839.s003"], "stats"=>{"downloads"=>7, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Modeling_the_Regulatory_Mechanisms_by_Which_NLRX1_Modulates_Innate_Immune_Responses_to_Helicobacter_pylori_Infection/1543376", "title"=>"Modeling the Regulatory Mechanisms by Which NLRX1 Modulates Innate Immune Responses to <i>Helicobacter pylori</i> Infection", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-09-14 05:26:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/2263779"], "description"=>"<p>Genes involved in pathogen detection were extracted from the RNAseq dataset and analyzed at each time point for significance (A; left–expression, right–significance). Expression of effector PRRs conformed to sustained or late waves whereas regulatory molecules were suppressed (B). Dynamic expression of transcripts observed by RNAseq was validated by quantitative real time RT-PCR (C). Transcriptomic data (A,B) are presented as average log2(ratio) whereas validation gene expression is presented as pg cDNA/500ug RNA. Asterisk indicates <i>P</i>-value < 0.05 based on ANOVA.</p>", "links"=>[], "tags"=>["gentamycin protection assay", "effector", "prr", "host tolerance", "Helicobacter pylori Infection Helicobacter pylori colonizes half", "host intracellular environment", "intracellular H", "modeling", "expression", "NLRX 1 Modulates Innate Immune Responses", "NLRX 1", "bmdm", "sequential host response waves", "spatiotemporal response waves", "Global Transcriptomic Analysis", "Pattern recognition receptors", "macrophage", "NLRC"], "article_id"=>1543370, "categories"=>["Uncategorised"], "users"=>["Casandra W. Philipson", "Josep Bassaganya-Riera", "Monica Viladomiu", "Barbara Kronsteiner", "Vida Abedi", "Stefan Hoops", "Pawel Michalak", "Lin Kang", "Stephen E. Girardin", "Raquel Hontecillas"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137839.g002", "stats"=>{"downloads"=>2, "page_views"=>41, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pattern_recognition_receptors_are_differentially_regulated_by_Helicobacter_pylori_/1543370", "title"=>"Pattern recognition receptors are differentially regulated by <i>Helicobacter pylori</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-14 05:26:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/2263784"], "description"=>"<p>Differentially regulated genes from the RNAseq dataset were analyzed for molecular crosstalk using Ingenuity Pathway Analyzer and a preliminary interaction network was created. Red indicates increased expression whereas green indicates reduced expression at time 360 min. Molecules in white are not detected (A). Early, sustained and late wave responses were included. Feedback circuits were added to canonical pathways and a biological system was engineered in Systems Biology Mark-up Language (B). In B: red lines represent negative regulation, positive reactions are black, solid lines are experimentally validated and dashed lines are hypothetical feedback loops. Two sensitivity analyses were performed on the calibrated mathematical model: effects of model species on NLRX1 (C); and effect of NLRX1 on local parameters (D). Time course model simulations for a wild type compared to Nlrx1-deficient system demonstrate differences in NF-kB signaling (E) and <i>H</i>. <i>pyori</i> burden <i>in silico</i> (F).</p>", "links"=>[], "tags"=>["gentamycin protection assay", "effector", "prr", "host tolerance", "Helicobacter pylori Infection Helicobacter pylori colonizes half", "host intracellular environment", "intracellular H", "modeling", "expression", "NLRX 1 Modulates Innate Immune Responses", "NLRX 1", "bmdm", "sequential host response waves", "spatiotemporal response waves", "Global Transcriptomic Analysis", "Pattern recognition receptors", "macrophage", "NLRC"], "article_id"=>1543375, "categories"=>["Uncategorised"], "users"=>["Casandra W. Philipson", "Josep Bassaganya-Riera", "Monica Viladomiu", "Barbara Kronsteiner", "Vida Abedi", "Stefan Hoops", "Pawel Michalak", "Lin Kang", "Stephen E. Girardin", "Raquel Hontecillas"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137839.g003", "stats"=>{"downloads"=>0, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Modeling_macrophage_immunity_to_Helicobacter_pylori_infection_reveals_an_essential_role_for_NLRX1_in_favoring_bacterial_burden_/1543375", "title"=>"Modeling macrophage immunity to <i>Helicobacter pylori</i> infection reveals an essential role for NLRX1 in favoring bacterial burden.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-14 05:26:05"}

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{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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