Vehicular exhaust particles promote allergic airway inflammation through an aryl hydrocarbon receptor–notch signaling cascade
Traffic-related particulate matter (PM) has been linked to a heightened incidence of asthma and allergic diseases. However, the molecular mechanisms by which PM exposure promotes allergic diseases remain elusive. We sought to determine the expression, function, and regulation of pathways involved in...
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| Published in | Journal of allergy and clinical immunology Vol. 136; no. 2; pp. 441 - 453 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.08.2015
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0091-6749 1097-6825 |
| DOI | 10.1016/j.jaci.2015.02.014 |
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| Abstract | Traffic-related particulate matter (PM) has been linked to a heightened incidence of asthma and allergic diseases. However, the molecular mechanisms by which PM exposure promotes allergic diseases remain elusive.
We sought to determine the expression, function, and regulation of pathways involved in promotion of allergic airway inflammation by PM.
We used gene expression transcriptional profiling, in vitro culture assays, and in vivo murine models of allergic airway inflammation.
We identified components of the Notch pathway, most notably Jagged 1 (Jag1), as targets of PM induction in human monocytes and murine dendritic cells. PM, especially ultrafine particles, upregulated TH cytokine levels, IgE production, and allergic airway inflammation in mice in a Jag1- and Notch-dependent manner, especially in the context of the proasthmatic IL-4 receptor allele Il4raR576. PM-induced Jag1 expression was mediated by the aryl hydrocarbon receptor (AhR), which bound to and activated AhR response elements in the Jag1 promoter. Pharmacologic antagonism of AhR or its lineage-specific deletion in CD11c+ cells abrogated the augmentation of airway inflammation by PM.
PM activates an AhR-Jag1-Notch cascade to promote allergic airway inflammation in concert with proasthmatic alleles. |
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| AbstractList | Traffic-related particulate matter (PM) has been linked to a heightened incidence of asthma and allergic diseases. However, the molecular mechanisms by which PM exposure promotes allergic diseases remain elusive.
We sought to determine the expression, function, and regulation of pathways involved in promotion of allergic airway inflammation by PM.
We used gene expression transcriptional profiling, in vitro culture assays, and in vivo murine models of allergic airway inflammation.
We identified components of the Notch pathway, most notably Jagged 1 (Jag1), as targets of PM induction in human monocytes and murine dendritic cells. PM, especially ultrafine particles, upregulated TH cytokine levels, IgE production, and allergic airway inflammation in mice in a Jag1- and Notch-dependent manner, especially in the context of the proasthmatic IL-4 receptor allele Il4raR576. PM-induced Jag1 expression was mediated by the aryl hydrocarbon receptor (AhR), which bound to and activated AhR response elements in the Jag1 promoter. Pharmacologic antagonism of AhR or its lineage-specific deletion in CD11c+ cells abrogated the augmentation of airway inflammation by PM.
PM activates an AhR-Jag1-Notch cascade to promote allergic airway inflammation in concert with proasthmatic alleles. Traffic-related particulate matter (PM) has been linked to a heightened incidence of asthma and allergic diseases. However, the molecular mechanisms by which PM exposure promotes allergic diseases remain elusive. We sought to determine the expression, function, and regulation of pathways involved in promotion of allergic airway inflammation by PM. We used gene expression transcriptional profiling, in vitro culture assays, and in vivo murine models of allergic airway inflammation. We identified components of the Notch pathway, most notably Jagged 1 (Jag1), as targets of PM induction in human monocytes and murine dendritic cells. PM, especially ultrafine particles, upregulated TH cytokine levels, IgE production, and allergic airway inflammation in mice in a Jag1- and Notch-dependent manner, especially in the context of the proasthmatic IL-4 receptor allele Il4raR576. PM-induced Jag1 expression was mediated by the aryl hydrocarbon receptor (AhR), which bound to and activated AhR response elements in the Jag1 promoter. Pharmacologic antagonism of AhR or its lineage-specific deletion in CD11c(+) cells abrogated the augmentation of airway inflammation by PM. PM activates an AhR-Jag1-Notch cascade to promote allergic airway inflammation in concert with proasthmatic alleles. Background Traffic-related particulate matter (PM) has been linked to a heightened incidence of asthma and allergic diseases. However, the molecular mechanisms by which PM exposure promotes allergic diseases remain elusive. Objective We sought to determine the expression, function, and regulation of pathways involved in promotion of allergic airway inflammation by PM. Methods We used gene expression transcriptional profiling, in vitro culture assays, and in vivo murine models of allergic airway inflammation. Results We identified components of the Notch pathway, most notably Jagged 1 (Jag1), as targets of PM induction in human monocytes and murine dendritic cells. PM, especially ultrafine particles, upregulated TH cytokine levels, IgE production, and allergic airway inflammation in mice in a Jag1- and Notch-dependent manner, especially in the context of the proasthmatic IL-4 receptor allele Il4raR576 . PM-induced Jag1 expression was mediated by the aryl hydrocarbon receptor (AhR), which bound to and activated AhR response elements in the Jag1 promoter. Pharmacologic antagonism of AhR or its lineage-specific deletion in CD11c+ cells abrogated the augmentation of airway inflammation by PM. Conclusion PM activates an AhR-Jag1-Notch cascade to promote allergic airway inflammation in concert with proasthmatic alleles. Background Traffic-related particulate matter (PM) has been linked to a heightened incidence of asthma and allergic diseases. However, the molecular mechanisms by which PM exposure promotes allergic diseases remain elusive. Objective We sought to determine the expression, function, and regulation of pathways involved in promotion of allergic airway inflammation by PM. Methods We used gene expression transcriptional profiling, in vitro culture assays, and in vivo murine models of allergic airway inflammation. Results We identified components of the Notch pathway, most notably Jagged 1 (Jag1), as targets of PM induction in human monocytes and murine dendritic cells. PM, especially ultrafine particles, upregulated TH cytokine levels, IgE production, and allergic airway inflammation in mice in a Jag1- and Notch-dependent manner, especially in the context of the proasthmatic IL-4 receptor allele Il4raR576. PM-induced Jag1 expression was mediated by the aryl hydrocarbon receptor (AhR), which bound to and activated AhR response elements in the Jag1 promoter. Pharmacologic antagonism of AhR or its lineage-specific deletion in CD11c+ cells abrogated the augmentation of airway inflammation by PM. Conclusion PM activates an AhR-Jag1-Notch cascade to promote allergic airway inflammation in concert with proasthmatic alleles. Background Traffic-related particulate matter (PM) has been linked to a heightened incidence of asthma and allergic diseases. However, the molecular mechanisms by which PM exposure promotes allergic diseases remain elusive. Objective We sought to determine the expression, function, and regulation of pathways involved in promotion of allergic airway inflammation by PM. Methods We used gene expression transcriptional profiling,in vitroculture assays, andin vivomurine models of allergic airway inflammation. Results We identified components of the Notch pathway, most notably Jagged 1 (Jag1), as targets of PM induction in human monocytes and murine dendritic cells. PM, especially ultrafine particles, upregulated THcytokine levels, IgE production, and allergic airway inflammation in mice in a Jag1- and Notch-dependent manner, especially in the context of the proasthmatic IL-4 receptor alleleIl4raR576. PM-induced Jag1 expression was mediated by the aryl hydrocarbon receptor (AhR), which bound to and activated AhR response elements in theJag1promoter. Pharmacologic antagonism of AhR or its lineage-specific deletion in CD11c+cells abrogated the augmentation of airway inflammation by PM. Conclusion PM activates an AhR-Jag1-Notch cascade to promote allergic airway inflammation in concert with proasthmatic alleles. |
| Author | Xia, Mingcan Garcia-Lloret, Maria Wise, Petra McGhee, Sean A. Chatila, Zena K. Daher, Nancy Chatila, Talal A. Viera-Hutchins, Loida Noval Rivas, Magali Sioutas, Constantinos |
| Author_xml | – sequence: 1 givenname: Mingcan surname: Xia fullname: Xia, Mingcan organization: Division of Immunology, Department of Pediatrics, Boston Children's Hospital, Harvard Medical School, Boston, Mass – sequence: 2 givenname: Loida surname: Viera-Hutchins fullname: Viera-Hutchins, Loida organization: Division of Immunology, Allergy and Rheumatology, Department of Pediatrics, David Geffen School of Medicine at the University of California at Los Angeles, Los Angeles, Calif – sequence: 3 givenname: Maria surname: Garcia-Lloret fullname: Garcia-Lloret, Maria organization: Division of Immunology, Allergy and Rheumatology, Department of Pediatrics, David Geffen School of Medicine at the University of California at Los Angeles, Los Angeles, Calif – sequence: 4 givenname: Magali surname: Noval Rivas fullname: Noval Rivas, Magali organization: Division of Immunology, Department of Pediatrics, Boston Children's Hospital, Harvard Medical School, Boston, Mass – sequence: 5 givenname: Petra surname: Wise fullname: Wise, Petra organization: Department of Hematology/Oncology and Bone Marrow Transplant, Children's Hospital Los Angeles, Los Angeles, Calif – sequence: 6 givenname: Sean A. surname: McGhee fullname: McGhee, Sean A. organization: Division of Immunology & Allergy, Department of Pediatrics, Stanford University School of Medicine, Stanford, Calif – sequence: 7 givenname: Zena K. surname: Chatila fullname: Chatila, Zena K. organization: Division of Immunology, Department of Pediatrics, Boston Children's Hospital, Harvard Medical School, Boston, Mass – sequence: 8 givenname: Nancy surname: Daher fullname: Daher, Nancy organization: Department of Civil and Environmental Engineering, University of Southern California, Los Angeles, Calif – sequence: 9 givenname: Constantinos surname: Sioutas fullname: Sioutas, Constantinos organization: Department of Civil and Environmental Engineering, University of Southern California, Los Angeles, Calif – sequence: 10 givenname: Talal A. surname: Chatila fullname: Chatila, Talal A. email: talal.chatila@childrens.harvard.edu organization: Division of Immunology, Department of Pediatrics, Boston Children's Hospital, Harvard Medical School, Boston, Mass |
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| Keywords | PAS DLL DMSO FP Notch1c allergic airway inflammation aryl hydrocarbon receptor diesel exhaust particles BMDC Jagged 1 FICZ GSI WT UFP CB airway hyperresponsiveness Jag1 Notch asthma AhR DEP Traffic-related particulate matter ultrafine particles PAH OVA PM TLR4 DC Periodic acid–Schiff Polycyclic aryl hydrocarbon Gamma-secretase inhibitor Toll-like receptor Carbon black particles Dendritic cell Ovalbumin Notch1 intracellular domain Bone marrow–derived dendritic cell Wild-type Delta-like ligand Fine particles Particulate matter Dimethyl sulfoxide 6-Formylindolo (3,2-b) carbazole |
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Part Fibre Toxicol. 2009 Jul 24;6:19 |
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| Snippet | Traffic-related particulate matter (PM) has been linked to a heightened incidence of asthma and allergic diseases. However, the molecular mechanisms by which... Background Traffic-related particulate matter (PM) has been linked to a heightened incidence of asthma and allergic diseases. However, the molecular mechanisms... |
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| SubjectTerms | airway hyperresponsiveness Alleles Allergens - adverse effects allergic airway inflammation Allergy and Immunology Animals Antigens Aqueous solutions aryl hydrocarbon receptor Asthma Atherosclerosis Atoms & subatomic particles Bronchial Hyperreactivity - chemically induced Bronchial Hyperreactivity - genetics Bronchial Hyperreactivity - immunology Bronchial Hyperreactivity - pathology Calcium-Binding Proteins - genetics Calcium-Binding Proteins - immunology CD11c Antigen - genetics CD11c Antigen - immunology Cytokines Dendritic cells Dendritic Cells - immunology Dendritic Cells - pathology diesel exhaust particles Disease Models, Animal Gene Expression Profiling Gene Expression Regulation Humans Hydrocarbons Immunoglobulin E - genetics Inflammation Intercellular Signaling Peptides and Proteins - genetics Intercellular Signaling Peptides and Proteins - immunology Jagged 1 Jagged-1 Protein Lymphocytes Membrane Proteins - genetics Membrane Proteins - immunology Mice Mice, Transgenic Monocytes - immunology Monocytes - pathology Notch Particulate Matter - adverse effects Pollutants Primary Cell Culture Receptor, Notch1 - genetics Receptor, Notch1 - immunology Receptors, Aryl Hydrocarbon - genetics Receptors, Aryl Hydrocarbon - immunology Receptors, Cell Surface - genetics Receptors, Cell Surface - immunology Respiratory Hypersensitivity - chemically induced Respiratory Hypersensitivity - genetics Respiratory Hypersensitivity - immunology Respiratory Hypersensitivity - pathology Serrate-Jagged Proteins Signal Transduction T-Lymphocytes, Helper-Inducer - immunology T-Lymphocytes, Helper-Inducer - pathology Traffic Traffic-related particulate matter ultrafine particles Vehicle Emissions |
| Title | Vehicular exhaust particles promote allergic airway inflammation through an aryl hydrocarbon receptor–notch signaling cascade |
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