Single-Dose, Intranasal Immunization with Recombinant Parainfluenza Virus 5 Expressing Middle East Respiratory Syndrome Coronavirus (MERS-CoV) Spike Protein Protects Mice from Fatal MERS-CoV Infection
Identifieur interne : 000066 ( Pmc/Checkpoint ); précédent : 000065; suivant : 000067Single-Dose, Intranasal Immunization with Recombinant Parainfluenza Virus 5 Expressing Middle East Respiratory Syndrome Coronavirus (MERS-CoV) Spike Protein Protects Mice from Fatal MERS-CoV Infection
Auteurs : Kun Li [États-Unis] ; Zhuo Li [États-Unis] ; Christine Wohlford-Lenane [États-Unis] ; David K. Meyerholz [États-Unis] ; Rudragouda Channappanavar [États-Unis] ; Dong An [États-Unis] ; Stanley Perlman [États-Unis] ; Paul B. Mccray [États-Unis] ; Biao He [États-Unis]Source :
- mBio [ 2150-7511 ] ; 2020.
Abstract
MERS-CoV causes lethal infection in humans, and there is no vaccine. Our work demonstrates that PIV5 is a promising vector for developing a MERS vaccine. Furthermore, success of PIV5-based MERS vaccine can be employed to develop a vaccine for emerging CoVs such as SARS-CoV-2, which causes COVID-19.
Url:
DOI: 10.1128/mBio.00554-20
PubMed: 32265331
PubMed Central: 7157776
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Single-Dose, Intranasal Immunization with Recombinant Parainfluenza Virus 5 Expressing Middle East Respiratory Syndrome Coronavirus (MERS-CoV) Spike Protein Protects Mice from Fatal MERS-CoV Infection</title><author><name sortKey="Li, Kun" sort="Li, Kun" uniqKey="Li K" first="Kun" last="Li">Kun Li</name><affiliation wicri:level="4"><nlm:aff id="aff1"><addr-line>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation></author><author><name sortKey="Li, Zhuo" sort="Li, Zhuo" uniqKey="Li Z" first="Zhuo" last="Li">Zhuo Li</name><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></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="4"><nlm:aff id="aff1"><addr-line>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation></author><author><name sortKey="Meyerholz, David K" sort="Meyerholz, David K" uniqKey="Meyerholz D" first="David K." last="Meyerholz">David K. 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Mccray</name><affiliation wicri:level="4"><nlm:aff id="aff1"><addr-line>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff3"><addr-line>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation></author><author><name sortKey="He, Biao" sort="He, Biao" uniqKey="He B" first="Biao" last="He">Biao He</name><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">32265331</idno><idno type="pmc">7157776</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7157776</idno><idno type="RBID">PMC:7157776</idno><idno type="doi">10.1128/mBio.00554-20</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">001637</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001637</idno><idno type="wicri:Area/Pmc/Curation">001637</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">001637</idno><idno type="wicri:Area/Pmc/Checkpoint">000066</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000066</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Single-Dose, Intranasal Immunization with Recombinant Parainfluenza Virus 5 Expressing Middle East Respiratory Syndrome Coronavirus (MERS-CoV) Spike Protein Protects Mice from Fatal MERS-CoV Infection</title><author><name sortKey="Li, Kun" sort="Li, Kun" uniqKey="Li K" first="Kun" last="Li">Kun Li</name><affiliation wicri:level="4"><nlm:aff id="aff1"><addr-line>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation></author><author><name sortKey="Li, Zhuo" sort="Li, Zhuo" uniqKey="Li Z" first="Zhuo" last="Li">Zhuo Li</name><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></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="4"><nlm:aff id="aff1"><addr-line>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></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="4"><nlm:aff id="aff2"><addr-line>Department of Pathology, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathology, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation></author><author><name sortKey="Channappanavar, Rudragouda" sort="Channappanavar, Rudragouda" uniqKey="Channappanavar R" first="Rudragouda" last="Channappanavar">Rudragouda Channappanavar</name><affiliation wicri:level="4"><nlm:aff id="aff3"><addr-line>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation></author><author><name sortKey="An, Dong" sort="An, Dong" uniqKey="An D" first="Dong" last="An">Dong An</name><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name><affiliation wicri:level="4"><nlm:aff id="aff1"><addr-line>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff3"><addr-line>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></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="4"><nlm:aff id="aff1"><addr-line>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff3"><addr-line>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa</wicri:regionArea><placeName><region type="state">Iowa</region><settlement type="city">Iowa City</settlement></placeName><orgName type="university">Université de l'Iowa</orgName></affiliation></author><author><name sortKey="He, Biao" sort="He, Biao" uniqKey="He B" first="Biao" last="He">Biao He</name><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>MERS-CoV causes lethal infection in humans, and there is no vaccine. Our work demonstrates that PIV5 is a promising vector for developing a MERS vaccine. Furthermore, success of PIV5-based MERS vaccine can be employed to develop a vaccine for emerging CoVs such as SARS-CoV-2, which causes COVID-19.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Zaki, Am" uniqKey="Zaki A">AM Zaki</name></author><author><name sortKey="Van Boheemen, S" uniqKey="Van Boheemen S">S van Boheemen</name></author><author><name sortKey="Bestebroer, Tm" uniqKey="Bestebroer T">TM Bestebroer</name></author><author><name sortKey="Osterhaus, Ad" uniqKey="Osterhaus A">AD Osterhaus</name></author><author><name sortKey="Fouchier, Ra" uniqKey="Fouchier R">RA Fouchier</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yusof, Mf" uniqKey="Yusof M">MF Yusof</name></author><author><name sortKey="Eltahir, Ym" uniqKey="Eltahir Y">YM Eltahir</name></author><author><name sortKey="Serhan, Ws" uniqKey="Serhan W">WS Serhan</name></author><author><name sortKey="Hashem, Fm" uniqKey="Hashem F">FM 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<front><journal-meta><journal-id journal-id-type="nlm-ta">mBio</journal-id><journal-id journal-id-type="iso-abbrev">mBio</journal-id><journal-id journal-id-type="hwp">mbio</journal-id><journal-id journal-id-type="pmc">mbio</journal-id><journal-id journal-id-type="publisher-id">mBio</journal-id><journal-title-group><journal-title>mBio</journal-title></journal-title-group><issn pub-type="epub">2150-7511</issn><publisher><publisher-name>American Society for Microbiology</publisher-name><publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">32265331</article-id><article-id pub-id-type="pmc">7157776</article-id><article-id pub-id-type="publisher-id">mBio00554-20</article-id><article-id pub-id-type="doi">10.1128/mBio.00554-20</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="overline"><subject>Therapeutics and Prevention</subject></subj-group></article-categories><title-group><article-title>Single-Dose, Intranasal Immunization with Recombinant Parainfluenza Virus 5 Expressing Middle East Respiratory Syndrome Coronavirus (MERS-CoV) Spike Protein Protects Mice from Fatal MERS-CoV Infection</article-title><alt-title alt-title-type="running-head">Immunization with PIV5 Expressing MERS-CoV Spike</alt-title><alt-title alt-title-type="short-authors">Li et al.</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Li</surname><given-names>Kun</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Zhuo</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref><xref ref-type="author-notes" rid="fn1">*</xref></contrib><contrib contrib-type="author"><name><surname>Wohlford-Lenane</surname><given-names>Christine</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Meyerholz</surname><given-names>David K.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Channappanavar</surname><given-names>Rudragouda</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref><xref ref-type="author-notes" rid="fn1">*</xref></contrib><contrib contrib-type="author"><name><surname>An</surname><given-names>Dong</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-4213-2354</contrib-id><name><surname>Perlman</surname><given-names>Stanley</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>McCray</surname><given-names>Paul B.</given-names><suffix>Jr.</suffix></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>He</surname><given-names>Biao</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref></contrib><aff id="aff1"><label>a</label><addr-line>Department of Pediatrics, Pappajohn Biomedical Institute, University of Iowa, Iowa City, Iowa, USA</addr-line></aff><aff id="aff2"><label>b</label><addr-line>Department of Pathology, University of Iowa, Iowa City, Iowa, USA</addr-line></aff><aff id="aff3"><label>c</label><addr-line>Department of Microbiology and Immunology, University of Iowa, Iowa City, Iowa, USA</addr-line></aff><aff id="aff4"><label>d</label><addr-line>Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA</addr-line></aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Subbarao</surname><given-names>Kanta</given-names></name><role>Editor</role><aff>The Peter Doherty Institute for Infection and Immunity</aff></contrib></contrib-group><author-notes><corresp id="cor1">Address correspondence to Paul B. McCray, Jr., <email>paul-mccray@uiowa.edu</email>, or Biao He, <email>bhe@uga.edu</email>.</corresp><fn id="fn1" fn-type="present-address"><label>*</label><p>Present address: Zhuo Li, Center for Inflammation, Immunity & Infection, Institute for Biomedical Sciences, Georgia State University, Atlanta, Georgia, USA; Rudragouda Channappanavar, Departments of Acute and Tertiary Care and of Microbiology and Immunology, University of Tennessee Health Sciences Center, Memphis, Tennessee, USA.</p></fn></author-notes><pub-date pub-type="epub"><day>7</day><month>4</month><year>2020</year></pub-date><pub-date pub-type="collection"><season>Mar-Apr</season><year>2020</year></pub-date><volume>11</volume><issue>2</issue><elocation-id>e00554-20</elocation-id><history><date date-type="received"><day>6</day><month>3</month><year>2020</year></date><date date-type="accepted"><day>24</day><month>3</month><year>2020</year></date></history><permissions><copyright-statement>Copyright © 2020 Li et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Li et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="mBio.00554-20.pdf"></self-uri><abstract abstract-type="precis"><p>MERS-CoV causes lethal infection in humans, and there is no vaccine. Our work demonstrates that PIV5 is a promising vector for developing a MERS vaccine. Furthermore, success of PIV5-based MERS vaccine can be employed to develop a vaccine for emerging CoVs such as SARS-CoV-2, which causes COVID-19.</p></abstract><abstract><title>ABSTRACT</title><p>Middle East respiratory syndrome coronavirus (MERS-CoV) can cause severe and fatal acute respiratory disease in humans and remains endemic in the Middle East since first being identified in 2012. There are currently no approved vaccines or therapies available for MERS-CoV. In this study, we evaluated parainfluenza virus 5 (PIV5)-based vaccine expressing the MERS-CoV envelope spike protein (PIV5/MERS-S) in a human DPP4 knockin C57BL/6 congenic mouse model (hDPP4 KI). Following a single-dose intranasal immunization, PIV5-MERS-S induced neutralizing antibody and robust T cell responses in hDPP4 KI mice. A single intranasal administration of 10<sup>4</sup> PFU PIV5-MERS-S provided complete protection against a lethal challenge with mouse-adapted MERS-CoV (MERS<sub>MA</sub>6.1.2) and improved virus clearance in the lung. In comparison, single-dose intramuscular immunization with 10<sup>6</sup> PFU UV-inactivated MERS<sub>MA</sub>6.1.2 mixed with Imject alum provided protection to only 25% of immunized mice. Intriguingly, an influx of eosinophils was observed only in the lungs of mice immunized with inactivated MERS-CoV, suggestive of a hypersensitivity-type response. Overall, our study indicated that PIV5-MERS-S is a promising effective vaccine candidate against MERS-CoV infection.</p></abstract><kwd-group><title>KEYWORDS</title><kwd>COVID-19</kwd><kwd>MERS</kwd><kwd>coronavirus</kwd><kwd>vaccine</kwd></kwd-group><funding-group><award-group id="award1"><funding-source><institution-wrap><institution>HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID)</institution><institution-id>https://doi.org/10.13039/100000060</institution-id></institution-wrap></funding-source><award-id>P01 AI060699</award-id><principal-award-recipient><name><surname>McCray</surname><given-names>Paul B.</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Perlman</surname><given-names>Stanley</given-names></name></principal-award-recipient></award-group><award-group id="award2"><funding-source><institution-wrap><institution>HHS | NIH | National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK)</institution><institution-id>https://doi.org/10.13039/100000062</institution-id></institution-wrap></funding-source><award-id>P30 DK54759</award-id><principal-award-recipient><name><surname>McCray</surname><given-names>Paul B.</given-names></name></principal-award-recipient></award-group><award-group id="award3"><funding-source><institution-wrap><institution>Cystic Fibrosis Foundation (CF Foundation)</institution><institution-id>https://doi.org/10.13039/100000897</institution-id></institution-wrap></funding-source><principal-award-recipient><name><surname>McCray</surname><given-names>Paul B.</given-names></name></principal-award-recipient></award-group></funding-group><counts><fig-count count="7"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="53"></ref-count><page-count count="12"></page-count><word-count count="7726"></word-count></counts><custom-meta-group><custom-meta><meta-name>cover-date</meta-name><meta-value>March/April 2020</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list><country><li>États-Unis</li></country><region><li>Géorgie (États-Unis)</li><li>Iowa</li></region><settlement><li>Iowa City</li></settlement><orgName><li>Université de l'Iowa</li></orgName></list><tree><country name="États-Unis"><region name="Iowa"><name sortKey="Li, Kun" sort="Li, Kun" uniqKey="Li K" first="Kun" last="Li">Kun Li</name></region><name sortKey="An, Dong" sort="An, Dong" uniqKey="An D" first="Dong" last="An">Dong An</name><name sortKey="Channappanavar, Rudragouda" sort="Channappanavar, Rudragouda" uniqKey="Channappanavar R" first="Rudragouda" last="Channappanavar">Rudragouda Channappanavar</name><name sortKey="He, Biao" sort="He, Biao" uniqKey="He B" first="Biao" last="He">Biao He</name><name sortKey="Li, Zhuo" sort="Li, Zhuo" uniqKey="Li Z" first="Zhuo" last="Li">Zhuo Li</name><name sortKey="Mccray, Paul B" sort="Mccray, Paul B" uniqKey="Mccray P" first="Paul B." last="Mccray">Paul B. Mccray</name><name sortKey="Mccray, Paul B" sort="Mccray, Paul B" uniqKey="Mccray P" first="Paul B." last="Mccray">Paul B. Mccray</name><name sortKey="Meyerholz, David K" sort="Meyerholz, David K" uniqKey="Meyerholz D" first="David K." last="Meyerholz">David K. Meyerholz</name><name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name><name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name><name sortKey="Wohlford Lenane, Christine" sort="Wohlford Lenane, Christine" uniqKey="Wohlford Lenane C" first="Christine" last="Wohlford-Lenane">Christine Wohlford-Lenane</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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