Downregulation of Key Early Events in the Mobilization of Antigen-bearing Dendritic Cells by Leukocyte Immunoglobulin-like Receptor B4 in a Mouse Model of Allergic Pulmonary Inflammation
Identifieur interne : 004467 ( Pmc/Curation ); précédent : 004466; suivant : 004468Downregulation of Key Early Events in the Mobilization of Antigen-bearing Dendritic Cells by Leukocyte Immunoglobulin-like Receptor B4 in a Mouse Model of Allergic Pulmonary Inflammation
Auteurs : Laura B. Fanning ; Carolyn C. Buckley ; Wei Xing ; Rebecca G. Breslow ; Howard R. KatzSource :
- PLoS ONE [ 1932-6203 ] ; 2013.
Abstract
Leukocyte Immunoglobulin-like Receptor B4 (LILRB4) null mice have an exacerbated T helper cell type 2 (Th2) immune response and pulmonary inflammation compared with
Url:
DOI: 10.1371/journal.pone.0057007
PubMed: 23431396
PubMed Central: 3576413
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Downregulation of Key Early Events in the Mobilization of Antigen-bearing Dendritic Cells by Leukocyte Immunoglobulin-like Receptor B4 in a Mouse Model of Allergic Pulmonary Inflammation</title>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Downregulation of Key Early Events in the Mobilization of Antigen-bearing Dendritic Cells by Leukocyte Immunoglobulin-like Receptor B4 in a Mouse Model of Allergic Pulmonary Inflammation</title>
<author><name sortKey="Fanning, Laura B" sort="Fanning, Laura B" uniqKey="Fanning L" first="Laura B." last="Fanning">Laura B. Fanning</name>
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<author><name sortKey="Buckley, Carolyn C" sort="Buckley, Carolyn C" uniqKey="Buckley C" first="Carolyn C." last="Buckley">Carolyn C. Buckley</name>
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<author><name sortKey="Xing, Wei" sort="Xing, Wei" uniqKey="Xing W" first="Wei" last="Xing">Wei Xing</name>
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<author><name sortKey="Breslow, Rebecca G" sort="Breslow, Rebecca G" uniqKey="Breslow R" first="Rebecca G." last="Breslow">Rebecca G. Breslow</name>
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<author><name sortKey="Katz, Howard R" sort="Katz, Howard R" uniqKey="Katz H" first="Howard R." last="Katz">Howard R. Katz</name>
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<series><title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
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<front><div type="abstract" xml:lang="en"><p>Leukocyte Immunoglobulin-like Receptor B4 (LILRB4) null mice have an exacerbated T helper cell type 2 (Th2) immune response and pulmonary inflammation compared with <italic>Lilrb4<sup>+/+</sup>
</italic>
animals when sensitized intranasally with ovalbumin (OVA) and low-dose lipopolysaccharide (LPS) followed by challenge with OVA. Moreover, OVA-challenged <italic>Lilrb4</italic>
<sup>−/−</sup>
mice exhibit greater migration of antigen (Ag)-bearing dendritic cells (DCs) to lymph nodes and accumulation of interleukin 4- and interleukin 5-producing lymph node lymphocytes. The main objective of this study was to determine how the absence of LILRB4 leads to a greater number of DCs in the lymph nodes of Ag-challenged mice and increased lung Th2 inflammation. Mice were sensitized intranasally with PBS alone or containing OVA and LPS; additional cohorts were subsequently challenged with OVA. Expression of chemokine (C-C motif) ligand 21 (CCL21) in the lung was assessed immunohistologically. OVA ingestion and expression of LILRB4 and chemokine (C-C motif) receptor 7 (CCR7) were quantified by flow cytometry. Inhalation of OVA and LPS induced upregulation of LILRB4 selectively on lung Ag-bearing DCs. After sensitization and challenge, the lung lymphatic vessels of <italic>Lilrb4</italic>
<sup>−/−</sup>
mice expressed more CCL21, a chemokine that directs the migration of DCs from peripheral tissue to draining lymph nodes, compared with <italic>Lilrb4<sup>+/+</sup>
</italic>
mice. In addition, lung DCs of challenged <italic>Lilrb4</italic>
<sup>−/−</sup>
mice expressed more CCR7, the CCL21 receptor. The lungs of challenged <italic>Lilrb4</italic>
<sup>−/−</sup>
mice also contained significantly greater numbers of CD4+ cells expressing interleukin-4 or interleukin-5, consistent with the greater number of Ag-bearing DCs and Th2 cells in lymph nodes and the attendant exacerbated Th2 lung pathology. Our data establish a new mechanism by which LILRB4 can downregulate the development of pathologic allergic inflammation: reduced upregulation of key molecules needed for DC migration leading to decreases in Th2 cells in lymph nodes and their target tissue.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">23431396</article-id>
<article-id pub-id-type="pmc">3576413</article-id>
<article-id pub-id-type="publisher-id">PONE-D-12-38138</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0057007</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology</subject>
<subj-group><subject>Developmental Biology</subject>
<subj-group><subject>Morphogenesis</subject>
<subj-group><subject>Cell Migration</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Immunology</subject>
<subj-group><subject>Immunity</subject>
<subj-group><subject>Immunoregulation</subject>
<subject>Inflammation</subject>
</subj-group>
</subj-group>
<subj-group><subject>Immunologic Subspecialties</subject>
<subj-group><subject>Pulmonary Immunology</subject>
</subj-group>
</subj-group>
<subj-group><subject>Allergy and Hypersensitivity</subject>
<subject>Immunomodulation</subject>
<subject>Immunopathology</subject>
</subj-group>
</subj-group>
<subj-group><subject>Model Organisms</subject>
<subj-group><subject>Animal Models</subject>
<subj-group><subject>Mouse</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Downregulation of Key Early Events in the Mobilization of Antigen-bearing Dendritic Cells by Leukocyte Immunoglobulin-like Receptor B4 in a Mouse Model of Allergic Pulmonary Inflammation</article-title>
<alt-title alt-title-type="running-head">Downregulation of DC Migration by LILRB4</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Fanning</surname>
<given-names>Laura B.</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Buckley</surname>
<given-names>Carolyn C.</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Xing</surname>
<given-names>Wei</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Breslow</surname>
<given-names>Rebecca G.</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Katz</surname>
<given-names>Howard R.</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><addr-line>From the Department of Medicine, Harvard Medical School, Boston, Massachusetts, United States of America, and the Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital, Boston, Massachusetts, United States of America</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Gao</surname>
<given-names>Hongwei</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>Harvard Medical School, United States of America</addr-line>
</aff>
<author-notes><corresp id="cor1">* E-mail: <email>hkatz@rics.bwh.harvard.edu</email>
</corresp>
<fn fn-type="conflict"><p><bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con"><p>Conceived and designed the experiments: LF CB WX RB HK. Performed the experiments: LF CB WX RB. Analyzed the data: LF CB WX RB HK. Wrote the paper: LF WX RB HK.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2013</year>
</pub-date>
<pub-date pub-type="epub"><day>19</day>
<month>2</month>
<year>2013</year>
</pub-date>
<volume>8</volume>
<issue>2</issue>
<elocation-id>e57007</elocation-id>
<history><date date-type="received"><day>4</day>
<month>12</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>17</day>
<month>1</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-year>2013</copyright-year>
<copyright-holder>Fanning et al</copyright-holder>
<license><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<abstract><p>Leukocyte Immunoglobulin-like Receptor B4 (LILRB4) null mice have an exacerbated T helper cell type 2 (Th2) immune response and pulmonary inflammation compared with <italic>Lilrb4<sup>+/+</sup>
</italic>
animals when sensitized intranasally with ovalbumin (OVA) and low-dose lipopolysaccharide (LPS) followed by challenge with OVA. Moreover, OVA-challenged <italic>Lilrb4</italic>
<sup>−/−</sup>
mice exhibit greater migration of antigen (Ag)-bearing dendritic cells (DCs) to lymph nodes and accumulation of interleukin 4- and interleukin 5-producing lymph node lymphocytes. The main objective of this study was to determine how the absence of LILRB4 leads to a greater number of DCs in the lymph nodes of Ag-challenged mice and increased lung Th2 inflammation. Mice were sensitized intranasally with PBS alone or containing OVA and LPS; additional cohorts were subsequently challenged with OVA. Expression of chemokine (C-C motif) ligand 21 (CCL21) in the lung was assessed immunohistologically. OVA ingestion and expression of LILRB4 and chemokine (C-C motif) receptor 7 (CCR7) were quantified by flow cytometry. Inhalation of OVA and LPS induced upregulation of LILRB4 selectively on lung Ag-bearing DCs. After sensitization and challenge, the lung lymphatic vessels of <italic>Lilrb4</italic>
<sup>−/−</sup>
mice expressed more CCL21, a chemokine that directs the migration of DCs from peripheral tissue to draining lymph nodes, compared with <italic>Lilrb4<sup>+/+</sup>
</italic>
mice. In addition, lung DCs of challenged <italic>Lilrb4</italic>
<sup>−/−</sup>
mice expressed more CCR7, the CCL21 receptor. The lungs of challenged <italic>Lilrb4</italic>
<sup>−/−</sup>
mice also contained significantly greater numbers of CD4+ cells expressing interleukin-4 or interleukin-5, consistent with the greater number of Ag-bearing DCs and Th2 cells in lymph nodes and the attendant exacerbated Th2 lung pathology. Our data establish a new mechanism by which LILRB4 can downregulate the development of pathologic allergic inflammation: reduced upregulation of key molecules needed for DC migration leading to decreases in Th2 cells in lymph nodes and their target tissue.</p>
</abstract>
<funding-group><funding-statement>This work was supported by AI07306, AI41144, and HL36110 from the National Institutes of Health; and a Senior Research Training Fellowship from the American Lung Association. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><page-count count="10"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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