TMPRSS11A activates the influenza A virus hemagglutinin and the MERS coronavirus spike protein and is insensitive against blockade by HAI-1.
Identifieur interne : 001E91 ( Ncbi/Merge ); précédent : 001E90; suivant : 001E92TMPRSS11A activates the influenza A virus hemagglutinin and the MERS coronavirus spike protein and is insensitive against blockade by HAI-1.
Auteurs : Pawel Zmora [Allemagne] ; Markus Hoffmann [Allemagne] ; Heike Kollmus [Allemagne] ; Anna-Sophie Moldenhauer [Allemagne] ; Olga Danov ; Armin Braun ; Michael Winkler [Allemagne] ; Klaus Schughart [Allemagne] ; Stefan PöhlmannSource :
- The Journal of biological chemistry [ 1083-351X ] ; 2018.
Descripteurs français
- KwdFr :
- Animaux, Glycoprotéine de spicule des coronavirus (métabolisme), Glycoprotéine hémagglutinine du virus influenza (métabolisme), Glycoprotéines membranaires, Humains, Hémagglutinines (métabolisme), Protéases à sérine (métabolisme), Protéines membranaires (métabolisme), Protéines sécrétoires inhibitrices de protéinases (pharmacologie), Pénétration virale, Serine endopeptidases (métabolisme), Souris, Virus de la grippe A (croissance et développement).
- MESH :
- croissance et développement : Virus de la grippe A.
- métabolisme : Glycoprotéine de spicule des coronavirus, Glycoprotéine hémagglutinine du virus influenza, Hémagglutinines, Protéases à sérine, Protéines membranaires, Serine endopeptidases.
- pharmacologie : Protéines sécrétoires inhibitrices de protéinases.
- Animaux, Glycoprotéines membranaires, Humains, Pénétration virale, Souris.
English descriptors
- KwdEn :
- Animals, Hemagglutinin Glycoproteins, Influenza Virus (metabolism), Hemagglutinins (metabolism), Humans, Influenza A virus (growth & development), Membrane Glycoproteins, Membrane Proteins (metabolism), Mice, Proteinase Inhibitory Proteins, Secretory (pharmacology), Serine Endopeptidases (metabolism), Serine Proteases (metabolism), Spike Glycoprotein, Coronavirus (metabolism), Virus Internalization.
- MESH :
- chemical , metabolism : Hemagglutinin Glycoproteins, Influenza Virus, Hemagglutinins, Membrane Proteins, Serine Endopeptidases, Serine Proteases, Spike Glycoprotein, Coronavirus.
- growth & development : Influenza A virus.
- chemical , pharmacology : Proteinase Inhibitory Proteins, Secretory.
- Animals, Humans, Membrane Glycoproteins, Mice, Virus Internalization.
Abstract
The influenza virus hemagglutinin (HA) facilitates viral entry into target cells. Cleavage of HA by host cell proteases is essential for viral infectivity, and the responsible enzymes are potential targets for antiviral intervention. The type II transmembrane serine protease (TTSP) TMPRSS2 has been identified as an HA activator in cell culture and in the infected host. However, it is less clear whether TMPRSS2-related enzymes can also activate HA for spread in target cells. Moreover, the activity of cellular serine protease inhibitors against HA-activating TTSPs is poorly understood. Here, we show that TMPRSS11A, another member of the TTSP family, cleaves and activates the influenza A virus (FLUAV) HA and the Middle East respiratory syndrome coronavirus spike protein (MERS-S). Moreover, we demonstrate that TMPRSS11A is expressed in murine tracheal epithelium, which is a target of FLUAV infection, and in human trachea, suggesting that the protease could support FLUAV spread in patients. Finally, we show that HA activation by the TMPRSS11A-related enzymes human airway tryptase and DESC1, but not TMPRSS11A itself, is blocked by the cellular serine protease inhibitor hepatocyte growth factor activator inhibitor type-1 (HAI-1). Our results suggest that TMPRSS11A could promote FLUAV spread in target cells and that HA-activating TTSPs exhibit differential sensitivity to blockade by cellular serine protease inhibitors.
DOI: 10.1074/jbc.RA118.001273
PubMed: 29976755
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Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen, Germany</wicri:regionArea><wicri:noRegion>Germany</wicri:noRegion><wicri:noRegion>Germany</wicri:noRegion><wicri:noRegion>Germany</wicri:noRegion></affiliation></author><author><name sortKey="Hoffmann, Markus" sort="Hoffmann, Markus" uniqKey="Hoffmann M" first="Markus" last="Hoffmann">Markus Hoffmann</name><affiliation wicri:level="3"><nlm:affiliation>From the Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>From the Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Kollmus, Heike" sort="Kollmus, Heike" uniqKey="Kollmus H" 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Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Danov, Olga" sort="Danov, Olga" uniqKey="Danov O" first="Olga" last="Danov">Olga Danov</name><affiliation><nlm:affiliation>the Fraunhofer Institute for Toxicology and Experimental Medicine (ITEM), German Center for Lung Research (DZL), Biomedical Research in Endstage and Obstructive Lung Disease Hannover (BREATH), Member of REBIRTH Cluster of Excellence, 30625 Hannover, Germany, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation></author><author><name sortKey="Braun, Armin" sort="Braun, Armin" uniqKey="Braun A" first="Armin" last="Braun">Armin Braun</name><affiliation><nlm:affiliation>the Fraunhofer Institute for Toxicology and Experimental Medicine (ITEM), German Center for Lung Research (DZL), Biomedical Research in Endstage and Obstructive Lung Disease Hannover (BREATH), Member of REBIRTH Cluster of Excellence, 30625 Hannover, Germany, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation></author><author><name sortKey="Winkler, Michael" sort="Winkler, Michael" uniqKey="Winkler M" first="Michael" last="Winkler">Michael Winkler</name><affiliation wicri:level="3"><nlm:affiliation>From the Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>From the Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen</wicri:regionArea><placeName><region type="land" nuts="2">Basse-Saxe</region><settlement type="city">Göttingen</settlement></placeName></affiliation></author><author><name sortKey="Schughart, Klaus" sort="Schughart, Klaus" uniqKey="Schughart K" first="Klaus" last="Schughart">Klaus Schughart</name><affiliation wicri:level="1"><nlm:affiliation>the Department of Infection Genetics, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>the Department of Infection Genetics, Helmholtz Centre for Infection Research, 38124 Braunschweig</wicri:regionArea><wicri:noRegion>38124 Braunschweig</wicri:noRegion><wicri:noRegion>38124 Braunschweig</wicri:noRegion><wicri:noRegion>38124 Braunschweig</wicri:noRegion></affiliation></author><author><name sortKey="Pohlmann, Stefan" sort="Pohlmann, Stefan" uniqKey="Pohlmann S" first="Stefan" last="Pöhlmann">Stefan Pöhlmann</name><affiliation><nlm:affiliation>From the Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen, Germany, spoehlmann@dpz.eu.</nlm:affiliation><wicri:noCountry code="subField">spoehlmann@dpz.eu.</wicri:noCountry></affiliation></author></analytic><series><title level="j">The Journal of biological chemistry</title><idno type="eISSN">1083-351X</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Hemagglutinin Glycoproteins, Influenza Virus (metabolism)</term><term>Hemagglutinins (metabolism)</term><term>Humans</term><term>Influenza A virus (growth & development)</term><term>Membrane Glycoproteins</term><term>Membrane Proteins (metabolism)</term><term>Mice</term><term>Proteinase Inhibitory Proteins, Secretory (pharmacology)</term><term>Serine Endopeptidases (metabolism)</term><term>Serine Proteases (metabolism)</term><term>Spike Glycoprotein, Coronavirus (metabolism)</term><term>Virus Internalization</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux</term><term>Glycoprotéine de spicule des coronavirus (métabolisme)</term><term>Glycoprotéine hémagglutinine du virus influenza (métabolisme)</term><term>Glycoprotéines membranaires</term><term>Humains</term><term>Hémagglutinines (métabolisme)</term><term>Protéases à sérine (métabolisme)</term><term>Protéines membranaires (métabolisme)</term><term>Protéines sécrétoires inhibitrices de protéinases (pharmacologie)</term><term>Pénétration virale</term><term>Serine endopeptidases (métabolisme)</term><term>Souris</term><term>Virus de la grippe A (croissance et développement)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Hemagglutinin Glycoproteins, Influenza Virus</term><term>Hemagglutinins</term><term>Membrane Proteins</term><term>Serine Endopeptidases</term><term>Serine Proteases</term><term>Spike Glycoprotein, Coronavirus</term></keywords><keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr"><term>Virus de la grippe A</term></keywords><keywords scheme="MESH" qualifier="growth & development" xml:lang="en"><term>Influenza A virus</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Glycoprotéine de spicule des coronavirus</term><term>Glycoprotéine hémagglutinine du virus influenza</term><term>Hémagglutinines</term><term>Protéases à sérine</term><term>Protéines membranaires</term><term>Serine endopeptidases</term></keywords><keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr"><term>Protéines sécrétoires inhibitrices de protéinases</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Proteinase Inhibitory Proteins, Secretory</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Humans</term><term>Membrane Glycoproteins</term><term>Mice</term><term>Virus Internalization</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Glycoprotéines membranaires</term><term>Humains</term><term>Pénétration virale</term><term>Souris</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The influenza virus hemagglutinin (HA) facilitates viral entry into target cells. Cleavage of HA by host cell proteases is essential for viral infectivity, and the responsible enzymes are potential targets for antiviral intervention. The type II transmembrane serine protease (TTSP) TMPRSS2 has been identified as an HA activator in cell culture and in the infected host. However, it is less clear whether TMPRSS2-related enzymes can also activate HA for spread in target cells. Moreover, the activity of cellular serine protease inhibitors against HA-activating TTSPs is poorly understood. Here, we show that TMPRSS11A, another member of the TTSP family, cleaves and activates the influenza A virus (FLUAV) HA and the Middle East respiratory syndrome coronavirus spike protein (MERS-S). Moreover, we demonstrate that TMPRSS11A is expressed in murine tracheal epithelium, which is a target of FLUAV infection, and in human trachea, suggesting that the protease could support FLUAV spread in patients. Finally, we show that HA activation by the TMPRSS11A-related enzymes human airway tryptase and DESC1, but not TMPRSS11A itself, is blocked by the cellular serine protease inhibitor hepatocyte growth factor activator inhibitor type-1 (HAI-1). Our results suggest that TMPRSS11A could promote FLUAV spread in target cells and that HA-activating TTSPs exhibit differential sensitivity to blockade by cellular serine protease inhibitors.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">29976755</PMID><DateCompleted><Year>2019</Year><Month>02</Month><Day>25</Day></DateCompleted><DateRevised><Year>2019</Year><Month>09</Month><Day>07</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1083-351X</ISSN><JournalIssue CitedMedium="Internet"><Volume>293</Volume><Issue>36</Issue><PubDate><Year>2018</Year><Month>09</Month><Day>07</Day></PubDate></JournalIssue><Title>The Journal of biological chemistry</Title><ISOAbbreviation>J. Biol. Chem.</ISOAbbreviation></Journal><ArticleTitle>TMPRSS11A activates the influenza A virus hemagglutinin and the MERS coronavirus spike protein and is insensitive against blockade by HAI-1.</ArticleTitle><Pagination><MedlinePgn>13863-13873</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1074/jbc.RA118.001273</ELocationID><Abstract><AbstractText>The influenza virus hemagglutinin (HA) facilitates viral entry into target cells. Cleavage of HA by host cell proteases is essential for viral infectivity, and the responsible enzymes are potential targets for antiviral intervention. The type II transmembrane serine protease (TTSP) TMPRSS2 has been identified as an HA activator in cell culture and in the infected host. However, it is less clear whether TMPRSS2-related enzymes can also activate HA for spread in target cells. Moreover, the activity of cellular serine protease inhibitors against HA-activating TTSPs is poorly understood. Here, we show that TMPRSS11A, another member of the TTSP family, cleaves and activates the influenza A virus (FLUAV) HA and the Middle East respiratory syndrome coronavirus spike protein (MERS-S). Moreover, we demonstrate that TMPRSS11A is expressed in murine tracheal epithelium, which is a target of FLUAV infection, and in human trachea, suggesting that the protease could support FLUAV spread in patients. Finally, we show that HA activation by the TMPRSS11A-related enzymes human airway tryptase and DESC1, but not TMPRSS11A itself, is blocked by the cellular serine protease inhibitor hepatocyte growth factor activator inhibitor type-1 (HAI-1). Our results suggest that TMPRSS11A could promote FLUAV spread in target cells and that HA-activating TTSPs exhibit differential sensitivity to blockade by cellular serine protease inhibitors.</AbstractText><CopyrightInformation>© 2018 Zmora et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zmora</LastName><ForeName>Pawel</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>From the Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen, Germany, zmora@mpi-magdeburg.mpg.de.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hoffmann</LastName><ForeName>Markus</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>From the Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kollmus</LastName><ForeName>Heike</ForeName><Initials>H</Initials><Identifier Source="ORCID">0000-0002-9473-8676</Identifier><AffiliationInfo><Affiliation>the Department of Infection Genetics, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Moldenhauer</LastName><ForeName>Anna-Sophie</ForeName><Initials>AS</Initials><AffiliationInfo><Affiliation>From the Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Danov</LastName><ForeName>Olga</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>the Fraunhofer Institute for Toxicology and Experimental Medicine (ITEM), German Center for Lung Research (DZL), Biomedical Research in Endstage and Obstructive Lung Disease Hannover (BREATH), Member of REBIRTH Cluster of Excellence, 30625 Hannover, Germany, and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Braun</LastName><ForeName>Armin</ForeName><Initials>A</Initials><Identifier Source="ORCID">0000-0002-1142-1463</Identifier><AffiliationInfo><Affiliation>the Fraunhofer Institute for Toxicology and Experimental Medicine (ITEM), German Center for Lung Research (DZL), Biomedical Research in Endstage and Obstructive Lung Disease Hannover (BREATH), Member of REBIRTH Cluster of Excellence, 30625 Hannover, Germany, and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Winkler</LastName><ForeName>Michael</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>From the Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schughart</LastName><ForeName>Klaus</ForeName><Initials>K</Initials><Identifier Source="ORCID">0000-0002-6824-7523</Identifier><AffiliationInfo><Affiliation>the Department of Infection Genetics, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>the University of Veterinary Medicine Hannover, 30599 Hannover, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>the Department of Microbiology, Immunology and Biochemistry, University of Tennessee Health Science Center, Memphis, Tennessee 38163.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pöhlmann</LastName><ForeName>Stefan</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0001-6086-9136</Identifier><AffiliationInfo><Affiliation>From the Infection Biology Unit, German Primate Center-Leibniz Institute for Primate Research, 37077 Göttingen, Germany, spoehlmann@dpz.eu.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>the Faculty of Biology and Psychology, University of Göttingen, 37073 Göttingen, Germany.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>07</Month><Day>05</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Biol Chem</MedlineTA><NlmUniqueID>2985121R</NlmUniqueID><ISSNLinking>0021-9258</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D019267">Hemagglutinin Glycoproteins, Influenza Virus</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D006388">Hemagglutinins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D008562">Membrane Glycoproteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D008565">Membrane Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D053491">Proteinase Inhibitory Proteins, Secretory</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C109149">SPINT1 protein, human</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D064370">Spike Glycoprotein, Coronavirus</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C504591">Spint1 protein, mouse</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.4.-</RegistryNumber><NameOfSubstance UI="D057057">Serine Proteases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.4.-</RegistryNumber><NameOfSubstance UI="C568601">TMPRSS11A protein, mouse</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.4.21.-</RegistryNumber><NameOfSubstance UI="D012697">Serine Endopeptidases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.4.21.-</RegistryNumber><NameOfSubstance UI="C421305">TMPRSS2 protein, human</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D019267" MajorTopicYN="N">Hemagglutinin Glycoproteins, Influenza Virus</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006388" MajorTopicYN="N">Hemagglutinins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009980" MajorTopicYN="N">Influenza A virus</DescriptorName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008562" MajorTopicYN="N">Membrane Glycoproteins</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008565" MajorTopicYN="N">Membrane Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D053491" MajorTopicYN="N">Proteinase Inhibitory Proteins, Secretory</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D012697" MajorTopicYN="N">Serine Endopeptidases</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D057057" MajorTopicYN="N">Serine Proteases</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D064370" MajorTopicYN="N">Spike Glycoprotein, Coronavirus</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D053586" MajorTopicYN="N">Virus Internalization</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">TMPRSS11A</Keyword><Keyword MajorTopicYN="Y">influenza virus</Keyword><Keyword MajorTopicYN="Y">protease</Keyword><Keyword MajorTopicYN="Y">protease inhibitor</Keyword><Keyword MajorTopicYN="Y">virology</Keyword><Keyword MajorTopicYN="Y">virus entry</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>01</Month><Day>17</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2018</Year><Month>06</Month><Day>15</Day></PubMedPubDate><PubMedPubDate 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