Involvement of an Arginine Triplet in M1 Matrix Protein Interaction with Membranes and in M1 Recruitment into Virus-Like Particles of the Influenza A(H1N1)pdm09 Virus.
Identifieur interne : 000490 ( PubMed/Checkpoint ); précédent : 000489; suivant : 000491Involvement of an Arginine Triplet in M1 Matrix Protein Interaction with Membranes and in M1 Recruitment into Virus-Like Particles of the Influenza A(H1N1)pdm09 Virus.
Auteurs : Adeline Kerviel [France] ; Shantoshini Dash [France] ; Olivier Moncorgé [France] ; Baptiste Panthu [France] ; Jan Prchal [France] ; Didier Décimo [France] ; Théophile Ohlmann [France] ; Bruno Lina [France] ; Cyril Favard [France] ; Etienne Decroly [France] ; Michèle Ottmann [France] ; Philippe Roingeard [France] ; Delphine Muriaux [France]Source :
- PloS one [ 1932-6203 ] ; 2016.
Descripteurs français
- KwdFr :
- Acides aminés (métabolisme), Animaux, Arginine (métabolisme), Assemblage viral (physiologie), Cellules HEK293, Cellules rénales canines Madin-Darby, Chiens, Cytoplasme (métabolisme), Grippe humaine (virologie), Humains, Lignée cellulaire, Membrane cellulaire (métabolisme), Mutation (génétique), Noyau de la cellule (métabolisme), Protéines de la matrice virale (génétique), Protéines de la matrice virale (métabolisme), Signaux de localisation nucléaire (métabolisme), Sous-type H1N1 du virus de la grippe A (génétique), Sous-type H1N1 du virus de la grippe A (métabolisme), Virion (métabolisme).
- MESH :
- génétique : Mutation, Protéines de la matrice virale, Sous-type H1N1 du virus de la grippe A.
- métabolisme : Acides aminés, Arginine, Cytoplasme, Membrane cellulaire, Noyau de la cellule, Protéines de la matrice virale, Signaux de localisation nucléaire, Sous-type H1N1 du virus de la grippe A, Virion.
- physiologie : Assemblage viral.
- virologie : Grippe humaine.
- Animaux, Cellules HEK293, Cellules rénales canines Madin-Darby, Chiens, Humains, Lignée cellulaire.
English descriptors
- KwdEn :
- Amino Acids (metabolism), Animals, Arginine (metabolism), Cell Line, Cell Membrane (metabolism), Cell Nucleus (metabolism), Cytoplasm (metabolism), Dogs, HEK293 Cells, Humans, Influenza A Virus, H1N1 Subtype (genetics), Influenza A Virus, H1N1 Subtype (metabolism), Influenza, Human (virology), Madin Darby Canine Kidney Cells, Mutation (genetics), Nuclear Localization Signals (metabolism), Viral Matrix Proteins (genetics), Viral Matrix Proteins (metabolism), Virion (metabolism), Virus Assembly (physiology).
- MESH :
- chemical , genetics : Viral Matrix Proteins.
- chemical , metabolism : Amino Acids, Arginine, Nuclear Localization Signals, Viral Matrix Proteins.
- genetics : Influenza A Virus, H1N1 Subtype, Mutation.
- metabolism : Cell Membrane, Cell Nucleus, Cytoplasm, Influenza A Virus, H1N1 Subtype, Virion.
- physiology : Virus Assembly.
- virology : Influenza, Human.
- Animals, Cell Line, Dogs, HEK293 Cells, Humans, Madin Darby Canine Kidney Cells.
Abstract
The influenza A(H1N1)pdm09 virus caused the first influenza pandemic of the 21st century. In this study, we wanted to decipher the role of conserved basic residues of the viral M1 matrix protein in virus assembly and release. M1 plays many roles in the influenza virus replication cycle. Specifically, it participates in viral particle assembly, can associate with the viral ribonucleoprotein complexes and can bind to the cell plasma membrane and/or the cytoplasmic tail of viral transmembrane proteins. M1 contains an N-terminal domain of 164 amino acids with two basic domains: the nuclear localization signal on helix 6 and an arginine triplet (R76/77/78) on helix 5. To investigate the role of these two M1 basic domains in influenza A(H1N1)pdm09 virus molecular assembly, we analyzed M1 attachment to membranes, virus-like particle (VLP) production and virus infectivity. In vitro, M1 binding to large unilamellar vesicles (LUVs), which contain negatively charged lipids, decreased significantly when the M1 R76/77/78 motif was mutated. In cells, M1 alone was mainly observed in the nucleus (47%) and in the cytosol (42%). Conversely, when co-expressed with the viral proteins NS1/NEP and M2, M1 was relocated to the cell membranes (55%), as shown by subcellular fractionation experiments. This minimal system allowed the production of M1 containing-VLPs. However, M1 with mutations in the arginine triplet accumulated in intracellular clusters and its incorporation in VLPs was strongly diminished. M2 over-expression was essential for M1 membrane localization and VLP production, whereas the viral trans-membrane proteins HA and NA seemed dispensable. These results suggest that the M1 arginine triplet participates in M1 interaction with membranes. This R76/77/78 motif is essential for M1 incorporation in virus particles and the importance of this motif was confirmed by reverse genetic demonstrating that its mutation is lethal for the virus. These results highlight the molecular mechanism of M1-membrane interaction during the formation of influenza A(H1N1)pdm09 virus particles which is essential for infectivity.
DOI: 10.1371/journal.pone.0165421
PubMed: 27814373
Affiliations:
- France
- Auvergne-Rhône-Alpes, Centre-Val de Loire, Languedoc-Roussillon, Occitanie (région administrative), Provence-Alpes-Côte d'Azur, Rhône-Alpes, Région Centre
- Lyon, Marseille, Montpellier, Tours
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pubmed:27814373Le document en format XML
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<author><name sortKey="Muriaux, Delphine" sort="Muriaux, Delphine" uniqKey="Muriaux D" first="Delphine" last="Muriaux">Delphine Muriaux</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Involvement of an Arginine Triplet in M1 Matrix Protein Interaction with Membranes and in M1 Recruitment into Virus-Like Particles of the Influenza A(H1N1)pdm09 Virus.</title>
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<author><name sortKey="Dash, Shantoshini" sort="Dash, Shantoshini" uniqKey="Dash S" first="Shantoshini" last="Dash">Shantoshini Dash</name>
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<country xml:lang="fr">France</country>
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<author><name sortKey="Moncorge, Olivier" sort="Moncorge, Olivier" uniqKey="Moncorge O" first="Olivier" last="Moncorgé">Olivier Moncorgé</name>
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<author><name sortKey="Panthu, Baptiste" sort="Panthu, Baptiste" uniqKey="Panthu B" first="Baptiste" last="Panthu">Baptiste Panthu</name>
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<author><name sortKey="Prchal, Jan" sort="Prchal, Jan" uniqKey="Prchal J" first="Jan" last="Prchal">Jan Prchal</name>
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<country xml:lang="fr">France</country>
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<author><name sortKey="Decimo, Didier" sort="Decimo, Didier" uniqKey="Decimo D" first="Didier" last="Décimo">Didier Décimo</name>
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<author><name sortKey="Ohlmann, Theophile" sort="Ohlmann, Theophile" uniqKey="Ohlmann T" first="Théophile" last="Ohlmann">Théophile Ohlmann</name>
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</author>
<author><name sortKey="Lina, Bruno" sort="Lina, Bruno" uniqKey="Lina B" first="Bruno" last="Lina">Bruno Lina</name>
<affiliation wicri:level="3"><nlm:affiliation>Université de Lyon, Université Lyon 1, Faculté de Médecine Lyon Est, Laboratoire de Virologie et Pathologie Humaine, EA 4610, Lyon, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université de Lyon, Université Lyon 1, Faculté de Médecine Lyon Est, Laboratoire de Virologie et Pathologie Humaine, EA 4610, Lyon</wicri:regionArea>
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<author><name sortKey="Favard, Cyril" sort="Favard, Cyril" uniqKey="Favard C" first="Cyril" last="Favard">Cyril Favard</name>
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<country xml:lang="fr">France</country>
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<author><name sortKey="Decroly, Etienne" sort="Decroly, Etienne" uniqKey="Decroly E" first="Etienne" last="Decroly">Etienne Decroly</name>
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<author><name sortKey="Ottmann, Michele" sort="Ottmann, Michele" uniqKey="Ottmann M" first="Michèle" last="Ottmann">Michèle Ottmann</name>
<affiliation wicri:level="3"><nlm:affiliation>Université de Lyon, Université Lyon 1, Faculté de Médecine Lyon Est, Laboratoire de Virologie et Pathologie Humaine, EA 4610, Lyon, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université de Lyon, Université Lyon 1, Faculté de Médecine Lyon Est, Laboratoire de Virologie et Pathologie Humaine, EA 4610, Lyon</wicri:regionArea>
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</author>
<author><name sortKey="Roingeard, Philippe" sort="Roingeard, Philippe" uniqKey="Roingeard P" first="Philippe" last="Roingeard">Philippe Roingeard</name>
<affiliation wicri:level="3"><nlm:affiliation>INSERM U966, Université François Rabelais & CHRU de Tours, Tours, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>INSERM U966, Université François Rabelais & CHRU de Tours, Tours</wicri:regionArea>
<placeName><region type="region">Centre-Val de Loire</region>
<region type="old region">Région Centre</region>
<settlement type="city">Tours</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Muriaux, Delphine" sort="Muriaux, Delphine" uniqKey="Muriaux D" first="Delphine" last="Muriaux">Delphine Muriaux</name>
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<country xml:lang="fr">France</country>
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<region type="old region">Languedoc-Roussillon</region>
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<series><title level="j">PloS one</title>
<idno type="eISSN">1932-6203</idno>
<imprint><date when="2016" type="published">2016</date>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Amino Acids (metabolism)</term>
<term>Animals</term>
<term>Arginine (metabolism)</term>
<term>Cell Line</term>
<term>Cell Membrane (metabolism)</term>
<term>Cell Nucleus (metabolism)</term>
<term>Cytoplasm (metabolism)</term>
<term>Dogs</term>
<term>HEK293 Cells</term>
<term>Humans</term>
<term>Influenza A Virus, H1N1 Subtype (genetics)</term>
<term>Influenza A Virus, H1N1 Subtype (metabolism)</term>
<term>Influenza, Human (virology)</term>
<term>Madin Darby Canine Kidney Cells</term>
<term>Mutation (genetics)</term>
<term>Nuclear Localization Signals (metabolism)</term>
<term>Viral Matrix Proteins (genetics)</term>
<term>Viral Matrix Proteins (metabolism)</term>
<term>Virion (metabolism)</term>
<term>Virus Assembly (physiology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Acides aminés (métabolisme)</term>
<term>Animaux</term>
<term>Arginine (métabolisme)</term>
<term>Assemblage viral (physiologie)</term>
<term>Cellules HEK293</term>
<term>Cellules rénales canines Madin-Darby</term>
<term>Chiens</term>
<term>Cytoplasme (métabolisme)</term>
<term>Grippe humaine (virologie)</term>
<term>Humains</term>
<term>Lignée cellulaire</term>
<term>Membrane cellulaire (métabolisme)</term>
<term>Mutation (génétique)</term>
<term>Noyau de la cellule (métabolisme)</term>
<term>Protéines de la matrice virale (génétique)</term>
<term>Protéines de la matrice virale (métabolisme)</term>
<term>Signaux de localisation nucléaire (métabolisme)</term>
<term>Sous-type H1N1 du virus de la grippe A (génétique)</term>
<term>Sous-type H1N1 du virus de la grippe A (métabolisme)</term>
<term>Virion (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Viral Matrix Proteins</term>
</keywords>
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<term>Arginine</term>
<term>Nuclear Localization Signals</term>
<term>Viral Matrix Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Influenza A Virus, H1N1 Subtype</term>
<term>Mutation</term>
</keywords>
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<term>Protéines de la matrice virale</term>
<term>Sous-type H1N1 du virus de la grippe A</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Cell Membrane</term>
<term>Cell Nucleus</term>
<term>Cytoplasm</term>
<term>Influenza A Virus, H1N1 Subtype</term>
<term>Virion</term>
</keywords>
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<term>Arginine</term>
<term>Cytoplasme</term>
<term>Membrane cellulaire</term>
<term>Noyau de la cellule</term>
<term>Protéines de la matrice virale</term>
<term>Signaux de localisation nucléaire</term>
<term>Sous-type H1N1 du virus de la grippe A</term>
<term>Virion</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Assemblage viral</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Virus Assembly</term>
</keywords>
<keywords scheme="MESH" qualifier="virologie" xml:lang="fr"><term>Grippe humaine</term>
</keywords>
<keywords scheme="MESH" qualifier="virology" xml:lang="en"><term>Influenza, Human</term>
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<term>Cell Line</term>
<term>Dogs</term>
<term>HEK293 Cells</term>
<term>Humans</term>
<term>Madin Darby Canine Kidney Cells</term>
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<keywords scheme="MESH" xml:lang="fr"><term>Animaux</term>
<term>Cellules HEK293</term>
<term>Cellules rénales canines Madin-Darby</term>
<term>Chiens</term>
<term>Humains</term>
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<front><div type="abstract" xml:lang="en">The influenza A(H1N1)pdm09 virus caused the first influenza pandemic of the 21st century. In this study, we wanted to decipher the role of conserved basic residues of the viral M1 matrix protein in virus assembly and release. M1 plays many roles in the influenza virus replication cycle. Specifically, it participates in viral particle assembly, can associate with the viral ribonucleoprotein complexes and can bind to the cell plasma membrane and/or the cytoplasmic tail of viral transmembrane proteins. M1 contains an N-terminal domain of 164 amino acids with two basic domains: the nuclear localization signal on helix 6 and an arginine triplet (R76/77/78) on helix 5. To investigate the role of these two M1 basic domains in influenza A(H1N1)pdm09 virus molecular assembly, we analyzed M1 attachment to membranes, virus-like particle (VLP) production and virus infectivity. In vitro, M1 binding to large unilamellar vesicles (LUVs), which contain negatively charged lipids, decreased significantly when the M1 R76/77/78 motif was mutated. In cells, M1 alone was mainly observed in the nucleus (47%) and in the cytosol (42%). Conversely, when co-expressed with the viral proteins NS1/NEP and M2, M1 was relocated to the cell membranes (55%), as shown by subcellular fractionation experiments. This minimal system allowed the production of M1 containing-VLPs. However, M1 with mutations in the arginine triplet accumulated in intracellular clusters and its incorporation in VLPs was strongly diminished. M2 over-expression was essential for M1 membrane localization and VLP production, whereas the viral trans-membrane proteins HA and NA seemed dispensable. These results suggest that the M1 arginine triplet participates in M1 interaction with membranes. This R76/77/78 motif is essential for M1 incorporation in virus particles and the importance of this motif was confirmed by reverse genetic demonstrating that its mutation is lethal for the virus. These results highlight the molecular mechanism of M1-membrane interaction during the formation of influenza A(H1N1)pdm09 virus particles which is essential for infectivity.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">27814373</PMID>
<DateCompleted><Year>2017</Year>
<Month>06</Month>
<Day>26</Day>
</DateCompleted>
<DateRevised><Year>2018</Year>
<Month>11</Month>
<Day>13</Day>
</DateRevised>
<Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1932-6203</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>11</Volume>
<Issue>11</Issue>
<PubDate><Year>2016</Year>
</PubDate>
</JournalIssue>
<Title>PloS one</Title>
<ISOAbbreviation>PLoS ONE</ISOAbbreviation>
</Journal>
<ArticleTitle>Involvement of an Arginine Triplet in M1 Matrix Protein Interaction with Membranes and in M1 Recruitment into Virus-Like Particles of the Influenza A(H1N1)pdm09 Virus.</ArticleTitle>
<Pagination><MedlinePgn>e0165421</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pone.0165421</ELocationID>
<Abstract><AbstractText>The influenza A(H1N1)pdm09 virus caused the first influenza pandemic of the 21st century. In this study, we wanted to decipher the role of conserved basic residues of the viral M1 matrix protein in virus assembly and release. M1 plays many roles in the influenza virus replication cycle. Specifically, it participates in viral particle assembly, can associate with the viral ribonucleoprotein complexes and can bind to the cell plasma membrane and/or the cytoplasmic tail of viral transmembrane proteins. M1 contains an N-terminal domain of 164 amino acids with two basic domains: the nuclear localization signal on helix 6 and an arginine triplet (R76/77/78) on helix 5. To investigate the role of these two M1 basic domains in influenza A(H1N1)pdm09 virus molecular assembly, we analyzed M1 attachment to membranes, virus-like particle (VLP) production and virus infectivity. In vitro, M1 binding to large unilamellar vesicles (LUVs), which contain negatively charged lipids, decreased significantly when the M1 R76/77/78 motif was mutated. In cells, M1 alone was mainly observed in the nucleus (47%) and in the cytosol (42%). Conversely, when co-expressed with the viral proteins NS1/NEP and M2, M1 was relocated to the cell membranes (55%), as shown by subcellular fractionation experiments. This minimal system allowed the production of M1 containing-VLPs. However, M1 with mutations in the arginine triplet accumulated in intracellular clusters and its incorporation in VLPs was strongly diminished. M2 over-expression was essential for M1 membrane localization and VLP production, whereas the viral trans-membrane proteins HA and NA seemed dispensable. These results suggest that the M1 arginine triplet participates in M1 interaction with membranes. This R76/77/78 motif is essential for M1 incorporation in virus particles and the importance of this motif was confirmed by reverse genetic demonstrating that its mutation is lethal for the virus. These results highlight the molecular mechanism of M1-membrane interaction during the formation of influenza A(H1N1)pdm09 virus particles which is essential for infectivity.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Kerviel</LastName>
<ForeName>Adeline</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>Centre d'études d'agents Pathogènes et Biotechnologies pour la Santé (CPBS), CNRS & Université of Montpellier, Montpellier, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Dash</LastName>
<ForeName>Shantoshini</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Centre d'études d'agents Pathogènes et Biotechnologies pour la Santé (CPBS), CNRS & Université of Montpellier, Montpellier, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Moncorgé</LastName>
<ForeName>Olivier</ForeName>
<Initials>O</Initials>
<AffiliationInfo><Affiliation>Centre d'études d'agents Pathogènes et Biotechnologies pour la Santé (CPBS), CNRS & Université of Montpellier, Montpellier, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Panthu</LastName>
<ForeName>Baptiste</ForeName>
<Initials>B</Initials>
<AffiliationInfo><Affiliation>CIRI, INSERM U 1111, France & ENS de Lyon, Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Prchal</LastName>
<ForeName>Jan</ForeName>
<Initials>J</Initials>
<AffiliationInfo><Affiliation>Centre d'études d'agents Pathogènes et Biotechnologies pour la Santé (CPBS), CNRS & Université of Montpellier, Montpellier, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Décimo</LastName>
<ForeName>Didier</ForeName>
<Initials>D</Initials>
<AffiliationInfo><Affiliation>CIRI, INSERM U 1111, France & ENS de Lyon, Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Ohlmann</LastName>
<ForeName>Théophile</ForeName>
<Initials>T</Initials>
<AffiliationInfo><Affiliation>CIRI, INSERM U 1111, France & ENS de Lyon, Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Lina</LastName>
<ForeName>Bruno</ForeName>
<Initials>B</Initials>
<AffiliationInfo><Affiliation>Université de Lyon, Université Lyon 1, Faculté de Médecine Lyon Est, Laboratoire de Virologie et Pathologie Humaine, EA 4610, Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Favard</LastName>
<ForeName>Cyril</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>Centre d'études d'agents Pathogènes et Biotechnologies pour la Santé (CPBS), CNRS & Université of Montpellier, Montpellier, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Decroly</LastName>
<ForeName>Etienne</ForeName>
<Initials>E</Initials>
<AffiliationInfo><Affiliation>Aix-Marseille Université & CNRS, AFMB UMR 7257, 163 Avenue de Luminy, 13288 Marseille cedex 09, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Ottmann</LastName>
<ForeName>Michèle</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>Université de Lyon, Université Lyon 1, Faculté de Médecine Lyon Est, Laboratoire de Virologie et Pathologie Humaine, EA 4610, Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Roingeard</LastName>
<ForeName>Philippe</ForeName>
<Initials>P</Initials>
<AffiliationInfo><Affiliation>INSERM U966, Université François Rabelais & CHRU de Tours, Tours, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Muriaux</LastName>
<ForeName>Delphine</ForeName>
<Initials>D</Initials>
<AffiliationInfo><Affiliation>Centre d'études d'agents Pathogènes et Biotechnologies pour la Santé (CPBS), CNRS & Université of Montpellier, Montpellier, France.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2016</Year>
<Month>11</Month>
<Day>04</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>United States</Country>
<MedlineTA>PLoS One</MedlineTA>
<NlmUniqueID>101285081</NlmUniqueID>
<ISSNLinking>1932-6203</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D000596">Amino Acids</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C488936">M1 protein, Influenza A virus</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D019913">Nuclear Localization Signals</NameOfSubstance>
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<CitationSubset>IM</CitationSubset>
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<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D001120" MajorTopicYN="N">Arginine</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002460" MajorTopicYN="N">Cell Line</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002462" MajorTopicYN="N">Cell Membrane</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002467" MajorTopicYN="N">Cell Nucleus</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
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<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D004285" MajorTopicYN="N">Dogs</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D057809" MajorTopicYN="N">HEK293 Cells</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D053118" MajorTopicYN="N">Influenza A Virus, H1N1 Subtype</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D007251" MajorTopicYN="N">Influenza, Human</DescriptorName>
<QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D061985" MajorTopicYN="N">Madin Darby Canine Kidney Cells</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D009154" MajorTopicYN="N">Mutation</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D019913" MajorTopicYN="N">Nuclear Localization Signals</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D014763" MajorTopicYN="N">Viral Matrix Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D014771" MajorTopicYN="N">Virion</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D019065" MajorTopicYN="N">Virus Assembly</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
</MeshHeadingList>
<CoiStatement>The authors have declared that no competing interests exist.</CoiStatement>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2016</Year>
<Month>07</Month>
<Day>07</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted"><Year>2016</Year>
<Month>10</Month>
<Day>11</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez"><Year>2016</Year>
<Month>11</Month>
<Day>5</Day>
<Hour>6</Hour>
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<PubMedPubDate PubStatus="pubmed"><Year>2016</Year>
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