IFN-I response timing relative to virus replication determines MERS coronavirus infection outcomes.
Identifieur interne : 000468 ( PubMed/Curation ); précédent : 000467; suivant : 000469IFN-I response timing relative to virus replication determines MERS coronavirus infection outcomes.
Auteurs : Rudragouda Channappanavar [États-Unis] ; Anthony R. Fehr [États-Unis] ; Jian Zheng [États-Unis] ; Christine Wohlford-Lenane [États-Unis] ; Juan E. Abrahante [États-Unis] ; Matthias Mack [Allemagne] ; Ramakrishna Sompallae [États-Unis] ; Paul B. Mccray [États-Unis] ; David K. Meyerholz [États-Unis] ; Stanley Perlman [États-Unis]Source :
- The Journal of clinical investigation [ 1558-8238 ] ; 2019.
Abstract
Type 1 IFNs (IFN-I) generally protect mammalian hosts from virus infections, but in some cases, IFN-I is pathogenic. Because IFN-I is protective, it is commonly used to treat virus infections for which no specific approved drug or vaccine is available. The Middle East respiratory syndrome-coronavirus (MERS-CoV) is such an infection, yet little is known about the role of IFN-I in this setting. Here, we show that IFN-I signaling is protective during MERS-CoV infection. Blocking IFN-I signaling resulted in delayed virus clearance, enhanced neutrophil infiltration, and impaired MERS-CoV-specific T cell responses. Notably, IFN-I administration within 1 day after infection (before virus titers peak) protected mice from lethal infection, despite a decrease in IFN-stimulated gene (ISG) and inflammatory cytokine gene expression. In contrast, delayed IFN-β treatment failed to effectively inhibit virus replication, increased infiltration and activation of monocytes, macrophages, and neutrophils in the lungs, and enhanced proinflammatory cytokine expression, resulting in fatal pneumonia in an otherwise sublethal infection. Together, these results suggest that the relative timing of the IFN-I response and maximal virus replication is key in determining outcomes, at least in infected mice. By extension, IFN-αβ or combination therapy may need to be used cautiously to treat viral infections in clinical settings.
DOI: 10.1172/JCI126363
PubMed: 31355779
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Fehr</name><affiliation wicri:level="1"><nlm:affiliation>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa</wicri:regionArea></affiliation></author><author><name sortKey="Zheng, Jian" sort="Zheng, Jian" uniqKey="Zheng J" first="Jian" last="Zheng">Jian Zheng</name><affiliation wicri:level="1"><nlm:affiliation>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa</wicri:regionArea></affiliation></author><author><name sortKey="Wohlford Lenane, Christine" sort="Wohlford Lenane, Christine" uniqKey="Wohlford Lenane C" first="Christine" last="Wohlford-Lenane">Christine Wohlford-Lenane</name><affiliation wicri:level="1"><nlm:affiliation>Department of Pediatrics, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, University of Iowa, Iowa City, Iowa</wicri:regionArea></affiliation></author><author><name sortKey="Abrahante, Juan E" sort="Abrahante, Juan E" uniqKey="Abrahante J" first="Juan E" last="Abrahante">Juan E. Abrahante</name><affiliation wicri:level="1"><nlm:affiliation>University of Minnesota Informatics Institute, University of Minnesota, Minneapolis, Minnesota, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>University of Minnesota Informatics Institute, University of Minnesota, Minneapolis, Minnesota</wicri:regionArea></affiliation></author><author><name sortKey="Mack, Matthias" sort="Mack, Matthias" uniqKey="Mack M" first="Matthias" last="Mack">Matthias Mack</name><affiliation wicri:level="1"><nlm:affiliation>Department of Internal Medicine, University Hospital Regensburg, Regensburg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Internal Medicine, University Hospital Regensburg, Regensburg</wicri:regionArea></affiliation></author><author><name sortKey="Sompallae, Ramakrishna" sort="Sompallae, Ramakrishna" uniqKey="Sompallae R" first="Ramakrishna" last="Sompallae">Ramakrishna Sompallae</name><affiliation wicri:level="1"><nlm:affiliation>Department of Pathology, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathology, University of Iowa, Iowa City, Iowa</wicri:regionArea></affiliation></author><author><name sortKey="Mccray, Paul B" sort="Mccray, Paul B" uniqKey="Mccray P" first="Paul B" last="Mccray">Paul B. Mccray</name><affiliation wicri:level="1"><nlm:affiliation>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa</wicri:regionArea></affiliation></author><author><name sortKey="Meyerholz, David K" sort="Meyerholz, David K" uniqKey="Meyerholz D" first="David K" last="Meyerholz">David K. Meyerholz</name><affiliation wicri:level="1"><nlm:affiliation>Department of Pathology, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathology, University of Iowa, Iowa City, Iowa</wicri:regionArea></affiliation></author><author><name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name><affiliation wicri:level="1"><nlm:affiliation>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa</wicri:regionArea></affiliation></author></analytic><series><title level="j">The Journal of clinical investigation</title><idno type="eISSN">1558-8238</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Type 1 IFNs (IFN-I) generally protect mammalian hosts from virus infections, but in some cases, IFN-I is pathogenic. Because IFN-I is protective, it is commonly used to treat virus infections for which no specific approved drug or vaccine is available. The Middle East respiratory syndrome-coronavirus (MERS-CoV) is such an infection, yet little is known about the role of IFN-I in this setting. Here, we show that IFN-I signaling is protective during MERS-CoV infection. Blocking IFN-I signaling resulted in delayed virus clearance, enhanced neutrophil infiltration, and impaired MERS-CoV-specific T cell responses. Notably, IFN-I administration within 1 day after infection (before virus titers peak) protected mice from lethal infection, despite a decrease in IFN-stimulated gene (ISG) and inflammatory cytokine gene expression. In contrast, delayed IFN-β treatment failed to effectively inhibit virus replication, increased infiltration and activation of monocytes, macrophages, and neutrophils in the lungs, and enhanced proinflammatory cytokine expression, resulting in fatal pneumonia in an otherwise sublethal infection. Together, these results suggest that the relative timing of the IFN-I response and maximal virus replication is key in determining outcomes, at least in infected mice. By extension, IFN-αβ or combination therapy may need to be used cautiously to treat viral infections in clinical settings.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">31355779</PMID><DateRevised><Year>2020</Year><Month>02</Month><Day>27</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1558-8238</ISSN><JournalIssue CitedMedium="Internet"><Volume>130</Volume><PubDate><Year>2019</Year><Month>Jul</Month><Day>29</Day></PubDate></JournalIssue><Title>The Journal of clinical investigation</Title><ISOAbbreviation>J. Clin. Invest.</ISOAbbreviation></Journal><ArticleTitle>IFN-I response timing relative to virus replication determines MERS coronavirus infection outcomes.</ArticleTitle><Pagination><MedlinePgn>3625-3639</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1172/JCI126363</ELocationID><ELocationID EIdType="pii" ValidYN="Y">126363</ELocationID><Abstract><AbstractText>Type 1 IFNs (IFN-I) generally protect mammalian hosts from virus infections, but in some cases, IFN-I is pathogenic. Because IFN-I is protective, it is commonly used to treat virus infections for which no specific approved drug or vaccine is available. The Middle East respiratory syndrome-coronavirus (MERS-CoV) is such an infection, yet little is known about the role of IFN-I in this setting. Here, we show that IFN-I signaling is protective during MERS-CoV infection. Blocking IFN-I signaling resulted in delayed virus clearance, enhanced neutrophil infiltration, and impaired MERS-CoV-specific T cell responses. Notably, IFN-I administration within 1 day after infection (before virus titers peak) protected mice from lethal infection, despite a decrease in IFN-stimulated gene (ISG) and inflammatory cytokine gene expression. In contrast, delayed IFN-β treatment failed to effectively inhibit virus replication, increased infiltration and activation of monocytes, macrophages, and neutrophils in the lungs, and enhanced proinflammatory cytokine expression, resulting in fatal pneumonia in an otherwise sublethal infection. Together, these results suggest that the relative timing of the IFN-I response and maximal virus replication is key in determining outcomes, at least in infected mice. By extension, IFN-αβ or combination therapy may need to be used cautiously to treat viral infections in clinical settings.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Channappanavar</LastName><ForeName>Rudragouda</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Acute and Tertiary Care, and.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, University of Tennessee Health Sciences Center, Memphis, Tennessee, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fehr</LastName><ForeName>Anthony R</ForeName><Initials>AR</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zheng</LastName><ForeName>Jian</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wohlford-Lenane</LastName><ForeName>Christine</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Pediatrics, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Abrahante</LastName><ForeName>Juan E</ForeName><Initials>JE</Initials><AffiliationInfo><Affiliation>University of Minnesota Informatics Institute, University of Minnesota, Minneapolis, Minnesota, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mack</LastName><ForeName>Matthias</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Internal Medicine, University Hospital Regensburg, Regensburg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sompallae</LastName><ForeName>Ramakrishna</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Department of Pathology, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>McCray</LastName><ForeName>Paul B</ForeName><Initials>PB</Initials><Suffix>Jr</Suffix><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Pediatrics, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Meyerholz</LastName><ForeName>David K</ForeName><Initials>DK</Initials><AffiliationInfo><Affiliation>Department of Pathology, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Perlman</LastName><ForeName>Stanley</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Pediatrics, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>State Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>P20 GM113117</GrantID><Acronym>GM</Acronym><Agency>NIGMS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>P30 ES005605</GrantID><Acronym>ES</Acronym><Agency>NIEHS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 AI129269</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>P01 AI060699</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R21 AG060222</GrantID><Acronym>AG</Acronym><Agency>NIA NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>07</Month><Day>29</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Clin Invest</MedlineTA><NlmUniqueID>7802877</NlmUniqueID><ISSNLinking>0021-9738</ISSNLinking></MedlineJournalInfo><CitationSubset>AIM</CitationSubset><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Infectious disease</Keyword><Keyword MajorTopicYN="N">Innate 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