Predictive Computational Modeling of the Mucosal Immune Responses during Helicobacter pylori Infection
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{"title"=>"Predictive Computational Modeling of the Mucosal Immune Responses during Helicobacter pylori Infection", "type"=>"journal", "authors"=>[{"first_name"=>"Adria", "last_name"=>"Carbo", "scopus_author_id"=>"36637003700"}, {"first_name"=>"Josep", "last_name"=>"Bassaganya-Riera", "scopus_author_id"=>"6603033549"}, {"first_name"=>"Mireia", "last_name"=>"Pedragosa", "scopus_author_id"=>"55017879700"}, {"first_name"=>"Monica", "last_name"=>"Viladomiu", "scopus_author_id"=>"42962600000"}, {"first_name"=>"Madhav", "last_name"=>"Marathe", "scopus_author_id"=>"7005103606"}, {"first_name"=>"Stephen", "last_name"=>"Eubank", "scopus_author_id"=>"6602912192"}, {"first_name"=>"Katherine", "last_name"=>"Wendelsdorf", "scopus_author_id"=>"26025382700"}, {"first_name"=>"Keith", "last_name"=>"Bisset", "scopus_author_id"=>"6701651050"}, {"first_name"=>"Stefan", "last_name"=>"Hoops", "scopus_author_id"=>"15128967000"}, {"first_name"=>"Xinwei", "last_name"=>"Deng", "scopus_author_id"=>"55548133200"}, {"first_name"=>"Maksudul", "last_name"=>"Alam", "scopus_author_id"=>"57199298020"}, {"first_name"=>"Barbara", "last_name"=>"Kronsteiner", "scopus_author_id"=>"17135052500"}, {"first_name"=>"Yongguo", "last_name"=>"Mei", "scopus_author_id"=>"55369974500"}, {"first_name"=>"Raquel", "last_name"=>"Hontecillas", "scopus_author_id"=>"6602639316"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"24039925", "doi"=>"10.1371/journal.pone.0073365", "sgr"=>"84883495378", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "scopus"=>"2-s2.0-84883495378", "issn"=>"19326203", "pui"=>"369755200"}, "id"=>"2c89b6f7-3d11-32ef-9f05-44a9c4f3e417", "abstract"=>"T helper (Th) cells play a major role in the immune response and pathology at the gastric mucosa during Helicobacter pylori infection. There is a limited mechanistic understanding regarding the contributions of CD4+ T cell subsets to gastritis development during H. pylori colonization. We used two computational approaches: ordinary differential equation (ODE)-based and agent-based modeling (ABM) to study the mechanisms underlying cellular immune responses to H. pylori and how CD4+ T cell subsets influenced initiation, progression and outcome of disease. To calibrate the model, in vivo experimentation was performed by infecting C57BL/6 mice intragastrically with H. pylori and assaying immune cell subsets in the stomach and gastric lymph nodes (GLN) on days 0, 7, 14, 30 and 60 post-infection. Our computational model reproduced the dynamics of effector and regulatory pathways in the gastric lamina propria (LP) in silico. Simulation results show the induction of a Th17 response and a dominant Th1 response, together with a regulatory response characterized by high levels of mucosal Treg) cells. We also investigated the potential role of peroxisome proliferator-activated receptor γ (PPARγ) activation on the modulation of host responses to H. pylori by using loss-of-function approaches. Specifically, in silico results showed a predominance of Th1 and Th17 cells in the stomach of the cell-specific PPARγ knockout system when compared to the wild-type simulation. Spatio-temporal, object-oriented ABM approaches suggested similar dynamics in induction of host responses showing analogous T cell distributions to ODE modeling and facilitated tracking lesion formation. In addition, sensitivity analysis predicted a crucial contribution of Th1 and Th17 effector responses as mediators of histopathological changes in the gastric mucosa during chronic stages of infection, which were experimentally validated in mice. These integrated immunoinformatics approaches characterized the induction of mucosal effector and regulatory pathways controlled by PPARγ during H. pylori infection affecting disease outcomes.", "link"=>"http://www.mendeley.com/research/predictive-computational-modeling-mucosal-immune-responses-during-helicobacter-pylori-infection-2", "reader_count"=>31, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Student > Master"=>1, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Student > Master"=>1, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>20, "Medicine and Dentistry"=>2, "Arts and Humanities"=>1, "Neuroscience"=>1, "Computer Science"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>1}, "Arts and Humanities"=>{"Arts and Humanities"=>1}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1193284"], "description"=>"<p>Systems Biology Markup Language (SBML)-compliant network of the interactions between <i>H. pylori</i> and cells participating in the innate and adaptive immune response such as macrophages (M1 and M2), dendritic cells (tDC and eDC), epithelial cells (E) and CD4+ T cell subsets (Th1, Th17, iTreg) in the gastric lumen, the epithelium, lamina propria (LP) and the gastric lymph nodes (GLN).</p>", "links"=>[], "tags"=>["mucosal", "responses"], "article_id"=>790413, "categories"=>["Biological Sciences"], "users"=>["Adria Carbo", "Josep Bassaganya-Riera", "Mireia Pedragosa", "Monica Viladomiu", "Madhav Marathe", "Stephen Eubank", "Katherine Wendelsdorf", "Keith Bisset", "Stefan Hoops", "Xinwei Deng", "Maksudul Alam", "Barbara Kronsteiner", "Yongguo Mei", "Raquel Hontecillas"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0073365.g001", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Network_model_of_the_mucosal_immune_responses_during_Helicobacter_pylori_infection_/790413", "title"=>"Network model of the mucosal immune responses during <i>Helicobacter pylori</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:36:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193292"], "description"=>"<p>Healthy epithelial cells changing state into pro-inflammatory epithelial cells, thereby contributing to the formation of gastric lesions. (A) Differential time-dependent patterns of lesion formation in the early, meridian and chronic-late stage of infection. (B) ODE-based deterministic sensitivity analysis on pro-inflammatory epithelial cells, as variables, and its formation at day 60 post-infection using a delta factor of 0.001 with a delta minimum of 1×10<sup>−12</sup>. (C) Flow cytometric analysis showing differences in the expression of CD4+ IL-17A+ cells in the gastric lamina propria after <i>H. pylori</i> infection. (D) Flow cytometric analysis showing differences in the expression of CD4+ IFNγ+ cells in the gastric lamina propria after <i>H. pylori</i> infection. (E) Cartoon model representation of the effect of DC activation, T cell expansion and macrophage differentiation on the formation of histopathological lesions in the gastric lamina propria (LP) during <i>H. pylori</i> infection.</p>", "links"=>[], "tags"=>["gastric", "inflammatory", "lesion"], "article_id"=>790421, "categories"=>["Biological Sciences"], "users"=>["Adria Carbo", "Josep Bassaganya-Riera", "Mireia Pedragosa", "Monica Viladomiu", "Madhav Marathe", "Stephen Eubank", "Katherine Wendelsdorf", "Keith Bisset", "Stefan Hoops", "Xinwei Deng", "Maksudul Alam", "Barbara Kronsteiner", "Yongguo Mei", "Raquel Hontecillas"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0073365.g005", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sensitivity_analysis_of_factors_involved_in_gastric_inflammatory_lesion_formation_following_Helicobacter_pylori_infection_/790421", "title"=>"Sensitivity analysis of factors involved in gastric inflammatory lesion formation following <i>Helicobacter pylori</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:36:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193286"], "description"=>"<p>(A) <i>In silico</i> time-course experiment performed with a challenge of 5×10<sup>7</sup> colony forming units of initial <i>H. pylori</i> injected in the mathematical model, showing differences in numbers of gastric lamina propria (LP) CD4+ T cell subsets over time. (B) Equilibrium constant regulating CD4+ T cell gastric lymph nodes (GLN) differentiation in our computational model. (C, D) Flow cytometry analysis results showing differences in the percentages of regulatory T (Treg) cells in spleen and GLN. (E) Flow cytometric analysis showing differences in the expression of IFNγ+ Tbet+ CD4+ T (Th1) cells in the spleen at day 30 post-infection. (F, G) Histopathological analysis on the gastric mucosa showed lesions consistent with <i>H. pylori</i> infection. Mouse stomachs had increased leukocyte infiltration in the LP and gastric mucosal thickening due to epithelial cell proliferation.</p>", "links"=>[], "tags"=>["subsets", "modulate", "responses"], "article_id"=>790415, "categories"=>["Biological Sciences"], "users"=>["Adria Carbo", "Josep Bassaganya-Riera", "Mireia Pedragosa", "Monica Viladomiu", "Madhav Marathe", "Stephen Eubank", "Katherine Wendelsdorf", "Keith Bisset", "Stefan Hoops", "Xinwei Deng", "Maksudul Alam", "Barbara Kronsteiner", "Yongguo Mei", "Raquel Hontecillas"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0073365.g002", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effector_and_regulatory_CD4_T_cell_subsets_modulate_the_immune_responses_during_Helicobacter_pylori_infection_/790415", "title"=>"Effector and regulatory CD4+ T cell subsets modulate the immune responses during <i>Helicobacter pylori</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:36:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193287"], "description"=>"<p>Time-course experiments following infection with 5×10<sup>7</sup> colony-forming units (CFU) of <i>H. pylori</i> to determine dynamics on CD4+ T cell phenotypes. Blue lines represent wild type mice and violet lines represent T cell-specific PPARγ knockout mice. T helper (Th) 1 (A), Th17 (B), induced regulatory T cell (iTreg) (C), effector dendritic cells (D), tolerogenic dendritic cells (E), M1 macrophages (F) and M2 macrophages (G) are illustrated.</p>", "links"=>[], "tags"=>["gastric", "mucosal", "subset", "wild-type", "cell-specific", "peroxisome", "proliferator-activated", "receptor", "knockout", "mice"], "article_id"=>790416, "categories"=>["Biological Sciences"], "users"=>["Adria Carbo", "Josep Bassaganya-Riera", "Mireia Pedragosa", "Monica Viladomiu", "Madhav Marathe", "Stephen Eubank", "Katherine Wendelsdorf", "Keith Bisset", "Stefan Hoops", "Xinwei Deng", "Maksudul Alam", "Barbara Kronsteiner", "Yongguo Mei", "Raquel Hontecillas"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0073365.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_silico_dynamics_of_gastric_mucosal_T_cell_subset_in_wild_type_and_T_cell_specific_peroxisome_proliferator_activated_receptor_PPAR_knockout_mice_following_infection_with_Helicobacter_pylori_/790416", "title"=>"<i>In silico</i> dynamics of gastric mucosal T cell subset in wild-type and T cell-specific peroxisome proliferator-activated receptor γ (PPARγ) knockout mice following infection with <i>Helicobacter pylori</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:36:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193296", "https://ndownloader.figshare.com/files/1193297", "https://ndownloader.figshare.com/files/1193298", "https://ndownloader.figshare.com/files/1193299", "https://ndownloader.figshare.com/files/1193300", "https://ndownloader.figshare.com/files/1193301", "https://ndownloader.figshare.com/files/1193302", "https://ndownloader.figshare.com/files/1193303", "https://ndownloader.figshare.com/files/1193305", "https://ndownloader.figshare.com/files/1193306", "https://ndownloader.figshare.com/files/1193307"], "description"=>"<div><p>T helper (Th) cells play a major role in the immune response and pathology at the gastric mucosa during <i>Helicobacter pylori</i> infection. There is a limited mechanistic understanding regarding the contributions of CD4+ T cell subsets to gastritis development during <i>H. pylori</i> colonization. We used two computational approaches: ordinary differential equation (ODE)-based and agent-based modeling (ABM) to study the mechanisms underlying cellular immune responses to <i>H. pylori</i> and how CD4+ T cell subsets influenced initiation, progression and outcome of disease. To calibrate the model, <i>in vivo</i> experimentation was performed by infecting C57BL/6 mice intragastrically with <i>H. pylori</i> and assaying immune cell subsets in the stomach and gastric lymph nodes (GLN) on days 0, 7, 14, 30 and 60 post-infection. Our computational model reproduced the dynamics of effector and regulatory pathways in the gastric lamina propria (LP) <i>in silico</i>. Simulation results show the induction of a Th17 response and a dominant Th1 response, together with a regulatory response characterized by high levels of mucosal Treg) cells. We also investigated the potential role of peroxisome proliferator-activated receptor γ (PPARγ) activation on the modulation of host responses to <i>H. pylori</i> by using loss-of-function approaches. Specifically, <i>in silico</i> results showed a predominance of Th1 and Th17 cells in the stomach of the cell-specific PPARγ knockout system when compared to the wild-type simulation. Spatio-temporal, object-oriented ABM approaches suggested similar dynamics in induction of host responses showing analogous T cell distributions to ODE modeling and facilitated tracking lesion formation. In addition, sensitivity analysis predicted a crucial contribution of Th1 and Th17 effector responses as mediators of histopathological changes in the gastric mucosa during chronic stages of infection, which were experimentally validated in mice. These integrated immunoinformatics approaches characterized the induction of mucosal effector and regulatory pathways controlled by PPARγ during <i>H. pylori</i> infection affecting disease outcomes.</p></div>", "links"=>[], "tags"=>["predictive", "computational", "modeling", "mucosal", "responses"], "article_id"=>790425, "categories"=>["Biological Sciences"], "users"=>["Adria Carbo", "Josep Bassaganya-Riera", "Mireia Pedragosa", "Monica Viladomiu", "Madhav Marathe", "Stephen Eubank", "Katherine Wendelsdorf", "Keith Bisset", "Stefan Hoops", "Xinwei Deng", "Maksudul Alam", "Barbara Kronsteiner", "Yongguo Mei", "Raquel Hontecillas"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0073365.s001", "https://dx.doi.org/10.1371/journal.pone.0073365.s002", "https://dx.doi.org/10.1371/journal.pone.0073365.s003", "https://dx.doi.org/10.1371/journal.pone.0073365.s004", "https://dx.doi.org/10.1371/journal.pone.0073365.s005", "https://dx.doi.org/10.1371/journal.pone.0073365.s006", "https://dx.doi.org/10.1371/journal.pone.0073365.s007", "https://dx.doi.org/10.1371/journal.pone.0073365.s008", "https://dx.doi.org/10.1371/journal.pone.0073365.s009", "https://dx.doi.org/10.1371/journal.pone.0073365.s010", "https://dx.doi.org/10.1371/journal.pone.0073365.s011"], "stats"=>{"downloads"=>7, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Predictive_Computational_Modeling_of_the_Mucosal_Immune_Responses_during_Helicobacter_pylori_Infection/790425", "title"=>"Predictive Computational Modeling of the Mucosal Immune Responses during <i>Helicobacter pylori</i> Infection", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-09-05 03:36:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193294"], "description"=>"<p>Representative photomicrographs of stomachs from either non infected or <i>H. pylori</i>-infected mice following administration of PBS or metronidazole treatment. Original magnification 40×.</p>", "links"=>[], "tags"=>["gastric", "mucosa", "mice"], "article_id"=>790423, "categories"=>["Biological Sciences"], "users"=>["Adria Carbo", "Josep Bassaganya-Riera", "Mireia Pedragosa", "Monica Viladomiu", "Madhav Marathe", "Stephen Eubank", "Katherine Wendelsdorf", "Keith Bisset", "Stefan Hoops", "Xinwei Deng", "Maksudul Alam", "Barbara Kronsteiner", "Yongguo Mei", "Raquel Hontecillas"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0073365.g006", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Histopathological_assessment_of_the_gastric_mucosa_of_mice_after_Helicobacter_pylori_infection_/790423", "title"=>"Histopathological assessment of the gastric mucosa of mice after <i>Helicobacter pylori</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:36:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/1193289"], "description"=>"<p>The <i>H. pylori</i> ABM was run as a time-course for 60 days. Model parameters were changed to simulate myeloid or T cell-specific PPARγ knockout systems as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073365#pone.0073365.s007\" target=\"_blank\">Table S2</a>. Dynamical variation of Th1 (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073365#pone-0073365-g006\" target=\"_blank\">Figure 6A, 6G</a>) as well as Th17 (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073365#pone-0073365-g006\" target=\"_blank\">Figure 6B, 6H</a>) and regulatory T cells (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073365#pone-0073365-g006\" target=\"_blank\">Figure 6C, 6I</a>) changing over time were plotted. A functional T-test was used with 95% confidence interval to create statistics assessing differences in the myeloid and T cell specific PPARγ knock-out for Th1 (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073365#pone-0073365-g006\" target=\"_blank\">Figure 6D, 6J</a>), Th17 (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073365#pone-0073365-g006\" target=\"_blank\">Figure 6E, 6K</a>) and Treg (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073365#pone-0073365-g006\" target=\"_blank\">Figure 6F, 6L</a>). A threshold value representing the critical value of significance vertically divides the plot into two parts, showing significant differences above the threshold. Data were obtained in 15 runs of the simulation for each different genotype.</p>", "links"=>[], "tags"=>["immunity", "simulator", "peroxisome", "proliferator", "activated", "receptor", "myeloid", "subset", "modulated", "responses", "gastric", "lamina", "propria", "lymph", "nodes"], "article_id"=>790418, "categories"=>["Biological Sciences"], "users"=>["Adria Carbo", "Josep Bassaganya-Riera", "Mireia Pedragosa", "Monica Viladomiu", "Madhav Marathe", "Stephen Eubank", "Katherine Wendelsdorf", "Keith Bisset", "Stefan Hoops", "Xinwei Deng", "Maksudul Alam", "Barbara Kronsteiner", "Yongguo Mei", "Raquel Hontecillas"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0073365.g004", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Enteric_Immunity_Simulator_ENISI_output_results_and_assessment_of_the_role_of_the_Peroxisome_Proliferator_Activated_Receptor_PPAR_in_both_the_myeloid_and_T_cell_subset_modulated_T_cell_responses_after_Helicobacter_pylori_infection_in_silico_in_the_gastri/790418", "title"=>"Enteric Immunity Simulator (ENISI) output results and assessment of the role of the Peroxisome Proliferator Activated Receptor γ (PPARγ) in both the myeloid and T cell subset modulated T cell responses after <i>Helicobacter pylori</i> infection <i>in silico</i> in the gastric lamina propria (LP) and gastric lymph nodes (GLN).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-05 03:36:23"}

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Relative Metric

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