Asthma increases susceptibility to heterologous but not homologous secondary influenza.
Identifieur interne : 000814 ( PubMed/Corpus ); précédent : 000813; suivant : 000815Asthma increases susceptibility to heterologous but not homologous secondary influenza.
Auteurs : Yoichi Furuya ; Sean Roberts ; Gregory J. Hurteau ; Alan M. Sanfilippo ; Rachael Racine ; Dennis W. MetzgerSource :
- Journal of virology [ 1098-5514 ] ; 2014.
English descriptors
- KwdEn :
- Animals, Antibodies, Viral (immunology), Antibody Formation (immunology), Asthma (complications), Asthma (immunology), Asthma (virology), B-Lymphocytes (immunology), B-Lymphocytes (virology), Bronchoalveolar Lavage Fluid (immunology), Bronchoalveolar Lavage Fluid (virology), Disease Susceptibility (etiology), Disease Susceptibility (immunology), Disease Susceptibility (virology), Female, Immunity, Mucosal (immunology), Immunoglobulins (immunology), Inflammation (immunology), Inflammation (virology), Influenza A virus (immunology), Lung (immunology), Lung (virology), Lymphocyte Activation (immunology), Mice, Mice, Inbred BALB C, Orthomyxoviridae Infections (etiology), Orthomyxoviridae Infections (immunology), Orthomyxoviridae Infections (virology).
- MESH :
- chemical , immunology : Antibodies, Viral, Immunoglobulins.
- complications : Asthma.
- etiology : Disease Susceptibility, Orthomyxoviridae Infections.
- immunology : Antibody Formation, Asthma, B-Lymphocytes, Bronchoalveolar Lavage Fluid, Disease Susceptibility, Immunity, Mucosal, Inflammation, Influenza A virus, Lung, Lymphocyte Activation, Orthomyxoviridae Infections.
- virology : Asthma, B-Lymphocytes, Bronchoalveolar Lavage Fluid, Disease Susceptibility, Inflammation, Lung, Orthomyxoviridae Infections.
- Animals, Female, Mice, Mice, Inbred BALB C.
Abstract
Asthma was the most common comorbidity observed among patients hospitalized with influenza A virus during the 2009 pandemic. However, little remains known about how the asthmatic phenotype influences protective immune responses against respiratory viral pathogens. Using the ovalbumin-induced allergic lung inflammation model, we found that asthmatic mice, unlike nonasthmatic mice, were highly susceptible to secondary heterologous virus challenge. While primary virus infection generated protective memory immune responses against homologous secondary virus challenge in both asthmatic and nonasthmatic mice, full protection against heterologous A/California/04/2009 (CA04) viral infection was observed only in nonasthmatic mice. Significant reductions in CA04-specific IgA, IgG, and IgM levels and in CA04-neutralizing activity of bronchoalveolar lavage fluid (BALF) was observed following secondary CA04 challenge of PR8-immunized asthmatic mice. Furthermore, transfer of immune BALF obtained from nonasthmatic, but not asthmatic, donors following secondary viral infection generated protection against CA04 in naive recipients. Nonspecific B-cell activation by CpG inoculation restored protection in PR8-immunized, CA04-challenged asthmatic mice. These results demonstrate a causal link between defective mucosal antibody responses and the heightened susceptibility of asthmatic mice to influenza infection and provide a mechanistic explanation for the observation that asthma was a major risk factor during the 2009 influenza pandemic.
DOI: 10.1128/JVI.00265-14
PubMed: 24899197
Links to Exploration step
pubmed:24899197Le document en format XML
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Hurteau</name><affiliation><nlm:affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Sanfilippo, Alan M" sort="Sanfilippo, Alan M" uniqKey="Sanfilippo A" first="Alan M" last="Sanfilippo">Alan M. Sanfilippo</name><affiliation><nlm:affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Racine, Rachael" sort="Racine, Rachael" uniqKey="Racine R" first="Rachael" last="Racine">Rachael Racine</name><affiliation><nlm:affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Metzger, Dennis W" sort="Metzger, Dennis W" uniqKey="Metzger D" first="Dennis W" last="Metzger">Dennis W. Metzger</name><affiliation><nlm:affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA metzged@mail.amc.edu.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2014">2014</date><idno type="RBID">pubmed:24899197</idno><idno type="pmid">24899197</idno><idno type="doi">10.1128/JVI.00265-14</idno><idno type="wicri:Area/PubMed/Corpus">000814</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">000814</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Asthma increases susceptibility to heterologous but not homologous secondary influenza.</title><author><name sortKey="Furuya, Yoichi" sort="Furuya, Yoichi" uniqKey="Furuya Y" first="Yoichi" last="Furuya">Yoichi Furuya</name><affiliation><nlm:affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Roberts, Sean" sort="Roberts, Sean" uniqKey="Roberts S" first="Sean" last="Roberts">Sean Roberts</name><affiliation><nlm:affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Hurteau, Gregory J" sort="Hurteau, Gregory J" uniqKey="Hurteau G" first="Gregory J" last="Hurteau">Gregory J. Hurteau</name><affiliation><nlm:affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Sanfilippo, Alan M" sort="Sanfilippo, Alan M" uniqKey="Sanfilippo A" first="Alan M" last="Sanfilippo">Alan M. Sanfilippo</name><affiliation><nlm:affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Racine, Rachael" sort="Racine, Rachael" uniqKey="Racine R" first="Rachael" last="Racine">Rachael Racine</name><affiliation><nlm:affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Metzger, Dennis W" sort="Metzger, Dennis W" uniqKey="Metzger D" first="Dennis W" last="Metzger">Dennis W. Metzger</name><affiliation><nlm:affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA metzged@mail.amc.edu.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Journal of virology</title><idno type="eISSN">1098-5514</idno><imprint><date when="2014" type="published">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Antibodies, Viral (immunology)</term><term>Antibody Formation (immunology)</term><term>Asthma (complications)</term><term>Asthma (immunology)</term><term>Asthma (virology)</term><term>B-Lymphocytes (immunology)</term><term>B-Lymphocytes (virology)</term><term>Bronchoalveolar Lavage Fluid (immunology)</term><term>Bronchoalveolar Lavage Fluid (virology)</term><term>Disease Susceptibility (etiology)</term><term>Disease Susceptibility (immunology)</term><term>Disease Susceptibility (virology)</term><term>Female</term><term>Immunity, Mucosal (immunology)</term><term>Immunoglobulins (immunology)</term><term>Inflammation (immunology)</term><term>Inflammation (virology)</term><term>Influenza A virus (immunology)</term><term>Lung (immunology)</term><term>Lung (virology)</term><term>Lymphocyte Activation (immunology)</term><term>Mice</term><term>Mice, Inbred BALB C</term><term>Orthomyxoviridae Infections (etiology)</term><term>Orthomyxoviridae Infections (immunology)</term><term>Orthomyxoviridae Infections (virology)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="immunology" xml:lang="en"><term>Antibodies, Viral</term><term>Immunoglobulins</term></keywords><keywords scheme="MESH" qualifier="complications" xml:lang="en"><term>Asthma</term></keywords><keywords scheme="MESH" qualifier="etiology" xml:lang="en"><term>Disease Susceptibility</term><term>Orthomyxoviridae Infections</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Antibody Formation</term><term>Asthma</term><term>B-Lymphocytes</term><term>Bronchoalveolar Lavage Fluid</term><term>Disease Susceptibility</term><term>Immunity, Mucosal</term><term>Inflammation</term><term>Influenza A virus</term><term>Lung</term><term>Lymphocyte Activation</term><term>Orthomyxoviridae Infections</term></keywords><keywords scheme="MESH" qualifier="virology" xml:lang="en"><term>Asthma</term><term>B-Lymphocytes</term><term>Bronchoalveolar Lavage Fluid</term><term>Disease Susceptibility</term><term>Inflammation</term><term>Lung</term><term>Orthomyxoviridae Infections</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Female</term><term>Mice</term><term>Mice, Inbred BALB C</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Asthma was the most common comorbidity observed among patients hospitalized with influenza A virus during the 2009 pandemic. However, little remains known about how the asthmatic phenotype influences protective immune responses against respiratory viral pathogens. Using the ovalbumin-induced allergic lung inflammation model, we found that asthmatic mice, unlike nonasthmatic mice, were highly susceptible to secondary heterologous virus challenge. While primary virus infection generated protective memory immune responses against homologous secondary virus challenge in both asthmatic and nonasthmatic mice, full protection against heterologous A/California/04/2009 (CA04) viral infection was observed only in nonasthmatic mice. Significant reductions in CA04-specific IgA, IgG, and IgM levels and in CA04-neutralizing activity of bronchoalveolar lavage fluid (BALF) was observed following secondary CA04 challenge of PR8-immunized asthmatic mice. Furthermore, transfer of immune BALF obtained from nonasthmatic, but not asthmatic, donors following secondary viral infection generated protection against CA04 in naive recipients. Nonspecific B-cell activation by CpG inoculation restored protection in PR8-immunized, CA04-challenged asthmatic mice. These results demonstrate a causal link between defective mucosal antibody responses and the heightened susceptibility of asthmatic mice to influenza infection and provide a mechanistic explanation for the observation that asthma was a major risk factor during the 2009 influenza pandemic.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">24899197</PMID><DateCompleted><Year>2014</Year><Month>09</Month><Day>25</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1098-5514</ISSN><JournalIssue CitedMedium="Internet"><Volume>88</Volume><Issue>16</Issue><PubDate><Year>2014</Year><Month>Aug</Month></PubDate></JournalIssue><Title>Journal of virology</Title><ISOAbbreviation>J. Virol.</ISOAbbreviation></Journal><ArticleTitle>Asthma increases susceptibility to heterologous but not homologous secondary influenza.</ArticleTitle><Pagination><MedlinePgn>9166-81</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1128/JVI.00265-14</ELocationID><Abstract><AbstractText Label="UNLABELLED">Asthma was the most common comorbidity observed among patients hospitalized with influenza A virus during the 2009 pandemic. However, little remains known about how the asthmatic phenotype influences protective immune responses against respiratory viral pathogens. Using the ovalbumin-induced allergic lung inflammation model, we found that asthmatic mice, unlike nonasthmatic mice, were highly susceptible to secondary heterologous virus challenge. While primary virus infection generated protective memory immune responses against homologous secondary virus challenge in both asthmatic and nonasthmatic mice, full protection against heterologous A/California/04/2009 (CA04) viral infection was observed only in nonasthmatic mice. Significant reductions in CA04-specific IgA, IgG, and IgM levels and in CA04-neutralizing activity of bronchoalveolar lavage fluid (BALF) was observed following secondary CA04 challenge of PR8-immunized asthmatic mice. Furthermore, transfer of immune BALF obtained from nonasthmatic, but not asthmatic, donors following secondary viral infection generated protection against CA04 in naive recipients. Nonspecific B-cell activation by CpG inoculation restored protection in PR8-immunized, CA04-challenged asthmatic mice. These results demonstrate a causal link between defective mucosal antibody responses and the heightened susceptibility of asthmatic mice to influenza infection and provide a mechanistic explanation for the observation that asthma was a major risk factor during the 2009 influenza pandemic.</AbstractText><AbstractText Label="IMPORTANCE" NlmCategory="OBJECTIVE">The prevalence of asthma worldwide is increasing each year. Unfortunately, there is no cure for asthma. Asthmatic individuals not only suffer from consistent wheezing and coughing but are also believed to be more prone to serious lung infections that result in bronchitis and pneumonia. However, little is known about the influence of asthma on host mucosal immunity. Here we show that antibody responses during secondary heterologous influenza infections are suboptimal and that this is responsible for the increased mortality in asthmatic mice from viral infections. Understanding the mechanism of increased susceptibility will aid in developing new antiviral therapies for asthmatic patients.</AbstractText><CopyrightInformation>Copyright © 2014, American Society for Microbiology. All Rights Reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Furuya</LastName><ForeName>Yoichi</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Roberts</LastName><ForeName>Sean</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hurteau</LastName><ForeName>Gregory J</ForeName><Initials>GJ</Initials><AffiliationInfo><Affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sanfilippo</LastName><ForeName>Alan M</ForeName><Initials>AM</Initials><AffiliationInfo><Affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Racine</LastName><ForeName>Rachael</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Metzger</LastName><ForeName>Dennis W</ForeName><Initials>DW</Initials><AffiliationInfo><Affiliation>Center for Immunology and Microbial Disease, Albany Medical College, Albany, New York, USA metzged@mail.amc.edu.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>R01 AI075312</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 AI75312</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2014</Year><Month>06</Month><Day>04</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Virol</MedlineTA><NlmUniqueID>0113724</NlmUniqueID><ISSNLinking>0022-538X</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000914">Antibodies, Viral</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D007136">Immunoglobulins</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000914" MajorTopicYN="N">Antibodies, Viral</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000917" MajorTopicYN="N">Antibody Formation</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D001249" MajorTopicYN="N">Asthma</DescriptorName><QualifierName UI="Q000150" MajorTopicYN="N">complications</QualifierName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName><QualifierName UI="Q000821" MajorTopicYN="Y">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D001402" MajorTopicYN="N">B-Lymphocytes</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D001992" MajorTopicYN="N">Bronchoalveolar Lavage Fluid</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D004198" MajorTopicYN="N">Disease Susceptibility</DescriptorName><QualifierName UI="Q000209" MajorTopicYN="N">etiology</QualifierName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName><QualifierName UI="Q000821" MajorTopicYN="Y">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005260" MajorTopicYN="N">Female</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018928" MajorTopicYN="N">Immunity, Mucosal</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D007136" MajorTopicYN="N">Immunoglobulins</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D007249" MajorTopicYN="N">Inflammation</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D009980" MajorTopicYN="N">Influenza A virus</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008168" MajorTopicYN="N">Lung</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008213" MajorTopicYN="N">Lymphocyte Activation</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008807" MajorTopicYN="N">Mice, Inbred BALB C</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009976" MajorTopicYN="N">Orthomyxoviridae Infections</DescriptorName><QualifierName UI="Q000209" MajorTopicYN="N">etiology</QualifierName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2014</Year><Month>6</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2014</Year><Month>6</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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