Structural basis for influenza virus NS1 protein block of mRNA nuclear export.
Identifieur interne : 000851 ( Main/Exploration ); précédent : 000850; suivant : 000852Structural basis for influenza virus NS1 protein block of mRNA nuclear export.
Auteurs : Ke Zhang [États-Unis] ; Yihu Xie [États-Unis] ; Raquel Mu Oz-Moreno [États-Unis] ; Juan Wang [États-Unis] ; Liang Zhang [République populaire de Chine] ; Matthew Esparza [États-Unis] ; Adolfo García-Sastre [États-Unis] ; Beatriz M A. Fontoura [États-Unis] ; Yi Ren [États-Unis]Source :
- Nature microbiology [ 2058-5276 ] ; 2019.
Descripteurs français
- KwdFr :
- ARN messager (métabolisme), Cellules A549, Cellules cultivées, Complexe protéique du pore nucléaire (), Complexe protéique du pore nucléaire (métabolisme), Complexes multiprotéiques (), Complexes multiprotéiques (métabolisme), Cristallographie aux rayons X, Grippe humaine (métabolisme), Humains, Liaison aux protéines, Modèles moléculaires, Noyau de la cellule (métabolisme), Protéines de liaison à l'ARN (), Protéines de liaison à l'ARN (génétique), Protéines de liaison à l'ARN (métabolisme), Protéines virales non structurales (génétique), Protéines virales non structurales (métabolisme), Sites de fixation, Transport nucléaire actif, Transporteurs nucléocytoplasmiques (), Transporteurs nucléocytoplasmiques (génétique), Transporteurs nucléocytoplasmiques (métabolisme), Virus de la grippe A (génétique), Virus de la grippe A (métabolisme), Virus de la grippe A (physiologie).
- MESH :
- génétique : Protéines de liaison à l'ARN, Protéines virales non structurales, Transporteurs nucléocytoplasmiques, Virus de la grippe A.
- métabolisme : ARN messager, Complexe protéique du pore nucléaire, Complexes multiprotéiques, Grippe humaine, Noyau de la cellule, Protéines de liaison à l'ARN, Protéines virales non structurales, Transporteurs nucléocytoplasmiques, Virus de la grippe A.
- physiologie : Virus de la grippe A.
- Cellules A549, Cellules cultivées, Complexe protéique du pore nucléaire, Complexes multiprotéiques, Cristallographie aux rayons X, Humains, Liaison aux protéines, Modèles moléculaires, Protéines de liaison à l'ARN, Sites de fixation, Transport nucléaire actif, Transporteurs nucléocytoplasmiques.
English descriptors
- KwdEn :
- A549 Cells, Active Transport, Cell Nucleus, Binding Sites, Cell Nucleus (metabolism), Cells, Cultured, Crystallography, X-Ray, Humans, Influenza A virus (genetics), Influenza A virus (metabolism), Influenza A virus (physiology), Influenza, Human (metabolism), Models, Molecular, Multiprotein Complexes (chemistry), Multiprotein Complexes (metabolism), Nuclear Pore Complex Proteins (chemistry), Nuclear Pore Complex Proteins (metabolism), Nucleocytoplasmic Transport Proteins (chemistry), Nucleocytoplasmic Transport Proteins (genetics), Nucleocytoplasmic Transport Proteins (metabolism), Protein Binding, RNA, Messenger (metabolism), RNA-Binding Proteins (chemistry), RNA-Binding Proteins (genetics), RNA-Binding Proteins (metabolism), Viral Nonstructural Proteins (genetics), Viral Nonstructural Proteins (metabolism).
- MESH :
- chemical , chemistry : Multiprotein Complexes, Nuclear Pore Complex Proteins, Nucleocytoplasmic Transport Proteins, RNA-Binding Proteins.
- genetics : Influenza A virus, Nucleocytoplasmic Transport Proteins, RNA-Binding Proteins, Viral Nonstructural Proteins.
- metabolism : Cell Nucleus, Influenza A virus, Influenza, Human, Multiprotein Complexes, Nuclear Pore Complex Proteins, Nucleocytoplasmic Transport Proteins, RNA, Messenger, RNA-Binding Proteins, Viral Nonstructural Proteins.
- physiology : Influenza A virus.
- A549 Cells, Active Transport, Cell Nucleus, Binding Sites, Cells, Cultured, Crystallography, X-Ray, Humans, Models, Molecular, Protein Binding.
Abstract
Influenza viruses antagonize key immune defence mechanisms via the virulence factor non-structural protein 1 (NS1). A key mechanism of virulence by NS1 is blocking nuclear export of host messenger RNAs, including those encoding immune factors1-3; however, the direct cellular target of NS1 and the mechanism of host mRNA export inhibition are not known. Here, we identify the target of NS1 as the mRNA export receptor complex, nuclear RNA export factor 1-nuclear transport factor 2-related export protein 1 (NXF1-NXT1), which is the principal receptor mediating docking and translocation of mRNAs through the nuclear pore complex via interactions with nucleoporins4,5. We determined the crystal structure of NS1 in complex with NXF1-NXT1 at 3.8 Å resolution. The structure reveals that NS1 prevents binding of NXF1-NXT1 to nucleoporins, thereby inhibiting mRNA export through the nuclear pore complex into the cytoplasm for translation. We demonstrate that a mutant influenza virus deficient in binding NXF1-NXT1 does not block host mRNA export and is attenuated. This attenuation is marked by the release of mRNAs encoding immune factors from the nucleus. In sum, our study uncovers the molecular basis of a major nuclear function of influenza NS1 protein that causes potent blockage of host gene expression and contributes to inhibition of host immunity.
DOI: 10.1038/s41564-019-0482-x
PubMed: 31263181
Affiliations:
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Fontoura</name><affiliation wicri:level="2"><nlm:affiliation>Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX, USA. beatriz.fontoura@utsouthwestern.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Ren, Yi" sort="Ren, Yi" uniqKey="Ren Y" first="Yi" last="Ren">Yi Ren</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry, Vanderbilt University School of Medicine, Nashville, TN, USA. yi.ren@vanderbilt.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry, Vanderbilt University School of Medicine, Nashville, TN</wicri:regionArea><placeName><region 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type="wicri:Area/Main/Exploration">000851</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Structural basis for influenza virus NS1 protein block of mRNA nuclear export.</title><author><name sortKey="Zhang, Ke" sort="Zhang, Ke" uniqKey="Zhang K" first="Ke" last="Zhang">Ke Zhang</name><affiliation wicri:level="2"><nlm:affiliation>Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Xie, Yihu" sort="Xie, Yihu" uniqKey="Xie Y" first="Yihu" last="Xie">Yihu Xie</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry, Vanderbilt University School of Medicine, Nashville, TN, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry, Vanderbilt University School of Medicine, Nashville, TN</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Mu Oz Moreno, Raquel" sort="Mu Oz Moreno, Raquel" uniqKey="Mu Oz Moreno R" first="Raquel" last="Mu Oz-Moreno">Raquel Mu Oz-Moreno</name><affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Wang, Juan" sort="Wang, Juan" uniqKey="Wang J" first="Juan" last="Wang">Juan Wang</name><affiliation wicri:level="2"><nlm:affiliation>Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Zhang, Liang" sort="Zhang, Liang" uniqKey="Zhang L" first="Liang" last="Zhang">Liang Zhang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Cellular Stress Biology, Innovation Center for Cell Signaling Network, School of Life Sciences, Xiamen University, Xiamen, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Cellular Stress Biology, Innovation Center for Cell Signaling Network, School of Life Sciences, Xiamen University, Xiamen</wicri:regionArea><wicri:noRegion>Xiamen</wicri:noRegion></affiliation></author><author><name sortKey="Esparza, Matthew" sort="Esparza, Matthew" uniqKey="Esparza M" first="Matthew" last="Esparza">Matthew Esparza</name><affiliation wicri:level="2"><nlm:affiliation>Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="García-Sastre">Adolfo García-Sastre</name><affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Fontoura, Beatriz M A" sort="Fontoura, Beatriz M A" uniqKey="Fontoura B" first="Beatriz M A" last="Fontoura">Beatriz M A. Fontoura</name><affiliation wicri:level="2"><nlm:affiliation>Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX, USA. beatriz.fontoura@utsouthwestern.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Ren, Yi" sort="Ren, Yi" uniqKey="Ren Y" first="Yi" last="Ren">Yi Ren</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry, Vanderbilt University School of Medicine, Nashville, TN, USA. yi.ren@vanderbilt.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry, Vanderbilt University School of Medicine, Nashville, TN</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author></analytic><series><title level="j">Nature microbiology</title><idno type="eISSN">2058-5276</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>A549 Cells</term><term>Active Transport, Cell Nucleus</term><term>Binding Sites</term><term>Cell Nucleus (metabolism)</term><term>Cells, Cultured</term><term>Crystallography, X-Ray</term><term>Humans</term><term>Influenza A virus (genetics)</term><term>Influenza A virus (metabolism)</term><term>Influenza A virus (physiology)</term><term>Influenza, Human (metabolism)</term><term>Models, Molecular</term><term>Multiprotein Complexes (chemistry)</term><term>Multiprotein Complexes (metabolism)</term><term>Nuclear Pore Complex Proteins (chemistry)</term><term>Nuclear Pore Complex Proteins (metabolism)</term><term>Nucleocytoplasmic Transport Proteins (chemistry)</term><term>Nucleocytoplasmic Transport Proteins (genetics)</term><term>Nucleocytoplasmic Transport Proteins (metabolism)</term><term>Protein Binding</term><term>RNA, Messenger (metabolism)</term><term>RNA-Binding Proteins (chemistry)</term><term>RNA-Binding Proteins (genetics)</term><term>RNA-Binding Proteins (metabolism)</term><term>Viral Nonstructural Proteins (genetics)</term><term>Viral Nonstructural Proteins (metabolism)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>ARN messager (métabolisme)</term><term>Cellules A549</term><term>Cellules cultivées</term><term>Complexe protéique du pore nucléaire ()</term><term>Complexe protéique du pore nucléaire (métabolisme)</term><term>Complexes multiprotéiques ()</term><term>Complexes multiprotéiques (métabolisme)</term><term>Cristallographie aux rayons X</term><term>Grippe humaine (métabolisme)</term><term>Humains</term><term>Liaison aux protéines</term><term>Modèles moléculaires</term><term>Noyau de la cellule (métabolisme)</term><term>Protéines de liaison à l'ARN ()</term><term>Protéines de liaison à l'ARN (génétique)</term><term>Protéines de liaison à l'ARN (métabolisme)</term><term>Protéines virales non structurales (génétique)</term><term>Protéines virales non structurales (métabolisme)</term><term>Sites de fixation</term><term>Transport nucléaire actif</term><term>Transporteurs nucléocytoplasmiques ()</term><term>Transporteurs nucléocytoplasmiques (génétique)</term><term>Transporteurs nucléocytoplasmiques (métabolisme)</term><term>Virus de la grippe A (génétique)</term><term>Virus de la grippe A (métabolisme)</term><term>Virus de la grippe A (physiologie)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Multiprotein Complexes</term><term>Nuclear Pore Complex Proteins</term><term>Nucleocytoplasmic Transport Proteins</term><term>RNA-Binding Proteins</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Influenza A virus</term><term>Nucleocytoplasmic Transport Proteins</term><term>RNA-Binding Proteins</term><term>Viral Nonstructural Proteins</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Protéines de liaison à l'ARN</term><term>Protéines virales non structurales</term><term>Transporteurs nucléocytoplasmiques</term><term>Virus de la grippe A</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Cell Nucleus</term><term>Influenza A virus</term><term>Influenza, Human</term><term>Multiprotein Complexes</term><term>Nuclear Pore Complex Proteins</term><term>Nucleocytoplasmic Transport Proteins</term><term>RNA, Messenger</term><term>RNA-Binding Proteins</term><term>Viral Nonstructural Proteins</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>ARN messager</term><term>Complexe protéique du pore nucléaire</term><term>Complexes multiprotéiques</term><term>Grippe humaine</term><term>Noyau de la cellule</term><term>Protéines de liaison à l'ARN</term><term>Protéines virales non structurales</term><term>Transporteurs nucléocytoplasmiques</term><term>Virus de la grippe A</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Virus de la grippe A</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Influenza A virus</term></keywords><keywords scheme="MESH" xml:lang="en"><term>A549 Cells</term><term>Active Transport, Cell Nucleus</term><term>Binding Sites</term><term>Cells, Cultured</term><term>Crystallography, X-Ray</term><term>Humans</term><term>Models, Molecular</term><term>Protein Binding</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Cellules A549</term><term>Cellules cultivées</term><term>Complexe protéique du pore nucléaire</term><term>Complexes multiprotéiques</term><term>Cristallographie aux rayons X</term><term>Humains</term><term>Liaison aux protéines</term><term>Modèles moléculaires</term><term>Protéines de liaison à l'ARN</term><term>Sites de fixation</term><term>Transport nucléaire actif</term><term>Transporteurs nucléocytoplasmiques</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Influenza viruses antagonize key immune defence mechanisms via the virulence factor non-structural protein 1 (NS1). A key mechanism of virulence by NS1 is blocking nuclear export of host messenger RNAs, including those encoding immune factors<sup>1-3</sup>; however, the direct cellular target of NS1 and the mechanism of host mRNA export inhibition are not known. Here, we identify the target of NS1 as the mRNA export receptor complex, nuclear RNA export factor 1-nuclear transport factor 2-related export protein 1 (NXF1-NXT1), which is the principal receptor mediating docking and translocation of mRNAs through the nuclear pore complex via interactions with nucleoporins<sup>4,5</sup>. We determined the crystal structure of NS1 in complex with NXF1-NXT1 at 3.8 Å resolution. The structure reveals that NS1 prevents binding of NXF1-NXT1 to nucleoporins, thereby inhibiting mRNA export through the nuclear pore complex into the cytoplasm for translation. We demonstrate that a mutant influenza virus deficient in binding NXF1-NXT1 does not block host mRNA export and is attenuated. This attenuation is marked by the release of mRNAs encoding immune factors from the nucleus. In sum, our study uncovers the molecular basis of a major nuclear function of influenza NS1 protein that causes potent blockage of host gene expression and contributes to inhibition of host immunity.</div></front></TEI><affiliations><list><country><li>République populaire de Chine</li><li>États-Unis</li></country><region><li>Tennessee</li><li>Texas</li><li>État de New York</li></region></list><tree><country name="États-Unis"><region name="Texas"><name sortKey="Zhang, Ke" sort="Zhang, Ke" uniqKey="Zhang K" first="Ke" last="Zhang">Ke Zhang</name></region><name sortKey="Esparza, Matthew" sort="Esparza, Matthew" uniqKey="Esparza M" first="Matthew" last="Esparza">Matthew Esparza</name><name sortKey="Fontoura, Beatriz M A" sort="Fontoura, Beatriz M A" uniqKey="Fontoura B" first="Beatriz M A" last="Fontoura">Beatriz M A. Fontoura</name><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="García-Sastre">Adolfo García-Sastre</name><name sortKey="Mu Oz Moreno, Raquel" sort="Mu Oz Moreno, Raquel" uniqKey="Mu Oz Moreno R" first="Raquel" last="Mu Oz-Moreno">Raquel Mu Oz-Moreno</name><name sortKey="Ren, Yi" sort="Ren, Yi" uniqKey="Ren Y" first="Yi" last="Ren">Yi Ren</name><name sortKey="Wang, Juan" sort="Wang, Juan" uniqKey="Wang J" first="Juan" last="Wang">Juan Wang</name><name sortKey="Xie, Yihu" sort="Xie, Yihu" uniqKey="Xie Y" first="Yihu" last="Xie">Yihu Xie</name></country><country name="République populaire de Chine"><noRegion><name sortKey="Zhang, Liang" sort="Zhang, Liang" uniqKey="Zhang L" first="Liang" last="Zhang">Liang Zhang</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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