Serveur d'exploration MERS

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Host species restriction of Middle East respiratory syndrome coronavirus through its receptor, dipeptidyl peptidase 4.

Identifieur interne : 001890 ( PubMed/Checkpoint ); précédent : 001889; suivant : 001891

Host species restriction of Middle East respiratory syndrome coronavirus through its receptor, dipeptidyl peptidase 4.

Auteurs : Neeltje Van Doremalen [États-Unis] ; Kerri L. Miazgowicz [États-Unis] ; Shauna Milne-Price [États-Unis] ; Trenton Bushmaker [États-Unis] ; Shelly Robertson [États-Unis] ; Dana Scott [États-Unis] ; Joerg Kinne [Émirats arabes unis] ; Jason S. Mclellan [États-Unis] ; Jiang Zhu [États-Unis] ; Vincent J. Munster

Source :

RBID : pubmed:24899185

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English descriptors

Abstract

Middle East respiratory syndrome coronavirus (MERS-CoV) emerged in 2012. Recently, the MERS-CoV receptor dipeptidyl peptidase 4 (DPP4) was identified and the specific interaction of the receptor-binding domain (RBD) of MERS-CoV spike protein and DPP4 was determined by crystallography. Animal studies identified rhesus macaques but not hamsters, ferrets, or mice to be susceptible for MERS-CoV. Here, we investigated the role of DPP4 in this observed species tropism. Cell lines of human and nonhuman primate origin were permissive of MERS-CoV, whereas hamster, ferret, or mouse cell lines were not, despite the presence of DPP4. Expression of human DPP4 in nonsusceptible BHK and ferret cells enabled MERS-CoV replication, whereas expression of hamster or ferret DPP4 did not. Modeling the binding energies of MERS-CoV spike protein RBD to DPP4 of human (susceptible) or hamster (nonsusceptible) identified five amino acid residues involved in the DPP4-RBD interaction. Expression of hamster DPP4 containing the five human DPP4 amino acids rendered BHK cells susceptible to MERS-CoV, whereas expression of human DPP4 containing the five hamster DPP4 amino acids did not. Using the same approach, the potential of MERS-CoV to utilize the DPP4s of common Middle Eastern livestock was investigated. Modeling of the DPP4 and MERS-CoV RBD interaction predicted the ability of MERS-CoV to bind the DPP4s of camel, goat, cow, and sheep. Expression of the DPP4s of these species on BHK cells supported MERS-CoV replication. This suggests, together with the abundant DPP4 presence in the respiratory tract, that these species might be able to function as a MERS-CoV intermediate reservoir.

DOI: 10.1128/JVI.00676-14
PubMed: 24899185


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Le document en format XML

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<nlm:affiliation>Central Veterinary Research Laboratories, Dubai, Dubai, United Arab Emirates.</nlm:affiliation>
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<name sortKey="Zhu, Jiang" sort="Zhu, Jiang" uniqKey="Zhu J" first="Jiang" last="Zhu">Jiang Zhu</name>
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<nlm:affiliation>Department of Immunology and Microbial Science and Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, California, USA.</nlm:affiliation>
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<term>Animals</term>
<term>Camelus (metabolism)</term>
<term>Camelus (virology)</term>
<term>Cattle</term>
<term>Cell Line</term>
<term>Cell Line, Tumor</term>
<term>Coronavirus (metabolism)</term>
<term>Coronavirus (pathogenicity)</term>
<term>Cricetinae</term>
<term>Dipeptidyl Peptidase 4 (metabolism)</term>
<term>Ferrets (metabolism)</term>
<term>Ferrets (virology)</term>
<term>Goats (metabolism)</term>
<term>Goats (virology)</term>
<term>Host Specificity</term>
<term>Humans</term>
<term>Livestock (metabolism)</term>
<term>Livestock (virology)</term>
<term>Macaca mulatta (metabolism)</term>
<term>Macaca mulatta (virology)</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Middle East</term>
<term>Primates (metabolism)</term>
<term>Primates (virology)</term>
<term>Protein Binding</term>
<term>Receptors, Virus (metabolism)</term>
<term>Respiratory Syncytial Viruses (metabolism)</term>
<term>Respiratory Syncytial Viruses (pathogenicity)</term>
<term>Sheep (metabolism)</term>
<term>Sheep (virology)</term>
<term>Vero Cells</term>
<term>Viral Tropism</term>
<term>Virus Replication (genetics)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Animaux</term>
<term>Bovins</term>
<term>Bétail (métabolisme)</term>
<term>Bétail (virologie)</term>
<term>Capra (métabolisme)</term>
<term>Capra (virologie)</term>
<term>Cellules Vero</term>
<term>Chameaux (métabolisme)</term>
<term>Chameaux (virologie)</term>
<term>Coronavirus (métabolisme)</term>
<term>Coronavirus (pathogénicité)</term>
<term>Cricetinae</term>
<term>Dipeptidyl peptidase 4 (métabolisme)</term>
<term>Furets (métabolisme)</term>
<term>Furets (virologie)</term>
<term>Humains</term>
<term>Liaison aux protéines</term>
<term>Lignée cellulaire</term>
<term>Lignée cellulaire tumorale</term>
<term>Macaca mulatta (métabolisme)</term>
<term>Macaca mulatta (virologie)</term>
<term>Moyen Orient</term>
<term>Ovis (métabolisme)</term>
<term>Ovis (virologie)</term>
<term>Primates (métabolisme)</term>
<term>Primates (virologie)</term>
<term>Récepteurs viraux (métabolisme)</term>
<term>Réplication virale (génétique)</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
<term>Spécificité d'hôte</term>
<term>Tropisme viral</term>
<term>Virus respiratoires syncytiaux (métabolisme)</term>
<term>Virus respiratoires syncytiaux (pathogénicité)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Dipeptidyl Peptidase 4</term>
<term>Receptors, Virus</term>
</keywords>
<keywords scheme="MESH" type="geographic" xml:lang="en">
<term>Middle East</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Virus Replication</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Réplication virale</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Camelus</term>
<term>Coronavirus</term>
<term>Ferrets</term>
<term>Goats</term>
<term>Livestock</term>
<term>Macaca mulatta</term>
<term>Primates</term>
<term>Respiratory Syncytial Viruses</term>
<term>Sheep</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Bétail</term>
<term>Capra</term>
<term>Chameaux</term>
<term>Coronavirus</term>
<term>Dipeptidyl peptidase 4</term>
<term>Furets</term>
<term>Macaca mulatta</term>
<term>Ovis</term>
<term>Primates</term>
<term>Récepteurs viraux</term>
<term>Virus respiratoires syncytiaux</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en">
<term>Coronavirus</term>
<term>Respiratory Syncytial Viruses</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr">
<term>Coronavirus</term>
<term>Virus respiratoires syncytiaux</term>
</keywords>
<keywords scheme="MESH" qualifier="virologie" xml:lang="fr">
<term>Bétail</term>
<term>Capra</term>
<term>Chameaux</term>
<term>Furets</term>
<term>Macaca mulatta</term>
<term>Ovis</term>
<term>Primates</term>
</keywords>
<keywords scheme="MESH" qualifier="virology" xml:lang="en">
<term>Camelus</term>
<term>Ferrets</term>
<term>Goats</term>
<term>Livestock</term>
<term>Macaca mulatta</term>
<term>Primates</term>
<term>Sheep</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Cattle</term>
<term>Cell Line</term>
<term>Cell Line, Tumor</term>
<term>Cricetinae</term>
<term>Host Specificity</term>
<term>Humans</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Protein Binding</term>
<term>Vero Cells</term>
<term>Viral Tropism</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Animaux</term>
<term>Bovins</term>
<term>Cellules Vero</term>
<term>Cricetinae</term>
<term>Humains</term>
<term>Liaison aux protéines</term>
<term>Lignée cellulaire</term>
<term>Lignée cellulaire tumorale</term>
<term>Moyen Orient</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
<term>Spécificité d'hôte</term>
<term>Tropisme viral</term>
</keywords>
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<front>
<div type="abstract" xml:lang="en">Middle East respiratory syndrome coronavirus (MERS-CoV) emerged in 2012. Recently, the MERS-CoV receptor dipeptidyl peptidase 4 (DPP4) was identified and the specific interaction of the receptor-binding domain (RBD) of MERS-CoV spike protein and DPP4 was determined by crystallography. Animal studies identified rhesus macaques but not hamsters, ferrets, or mice to be susceptible for MERS-CoV. Here, we investigated the role of DPP4 in this observed species tropism. Cell lines of human and nonhuman primate origin were permissive of MERS-CoV, whereas hamster, ferret, or mouse cell lines were not, despite the presence of DPP4. Expression of human DPP4 in nonsusceptible BHK and ferret cells enabled MERS-CoV replication, whereas expression of hamster or ferret DPP4 did not. Modeling the binding energies of MERS-CoV spike protein RBD to DPP4 of human (susceptible) or hamster (nonsusceptible) identified five amino acid residues involved in the DPP4-RBD interaction. Expression of hamster DPP4 containing the five human DPP4 amino acids rendered BHK cells susceptible to MERS-CoV, whereas expression of human DPP4 containing the five hamster DPP4 amino acids did not. Using the same approach, the potential of MERS-CoV to utilize the DPP4s of common Middle Eastern livestock was investigated. Modeling of the DPP4 and MERS-CoV RBD interaction predicted the ability of MERS-CoV to bind the DPP4s of camel, goat, cow, and sheep. Expression of the DPP4s of these species on BHK cells supported MERS-CoV replication. This suggests, together with the abundant DPP4 presence in the respiratory tract, that these species might be able to function as a MERS-CoV intermediate reservoir.</div>
</front>
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<DateCompleted>
<Year>2014</Year>
<Month>09</Month>
<Day>25</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>03</Month>
<Day>20</Day>
</DateRevised>
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<JournalIssue CitedMedium="Internet">
<Volume>88</Volume>
<Issue>16</Issue>
<PubDate>
<Year>2014</Year>
<Month>Aug</Month>
</PubDate>
</JournalIssue>
<Title>Journal of virology</Title>
<ISOAbbreviation>J. Virol.</ISOAbbreviation>
</Journal>
<ArticleTitle>Host species restriction of Middle East respiratory syndrome coronavirus through its receptor, dipeptidyl peptidase 4.</ArticleTitle>
<Pagination>
<MedlinePgn>9220-32</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1128/JVI.00676-14</ELocationID>
<Abstract>
<AbstractText Label="UNLABELLED">Middle East respiratory syndrome coronavirus (MERS-CoV) emerged in 2012. Recently, the MERS-CoV receptor dipeptidyl peptidase 4 (DPP4) was identified and the specific interaction of the receptor-binding domain (RBD) of MERS-CoV spike protein and DPP4 was determined by crystallography. Animal studies identified rhesus macaques but not hamsters, ferrets, or mice to be susceptible for MERS-CoV. Here, we investigated the role of DPP4 in this observed species tropism. Cell lines of human and nonhuman primate origin were permissive of MERS-CoV, whereas hamster, ferret, or mouse cell lines were not, despite the presence of DPP4. Expression of human DPP4 in nonsusceptible BHK and ferret cells enabled MERS-CoV replication, whereas expression of hamster or ferret DPP4 did not. Modeling the binding energies of MERS-CoV spike protein RBD to DPP4 of human (susceptible) or hamster (nonsusceptible) identified five amino acid residues involved in the DPP4-RBD interaction. Expression of hamster DPP4 containing the five human DPP4 amino acids rendered BHK cells susceptible to MERS-CoV, whereas expression of human DPP4 containing the five hamster DPP4 amino acids did not. Using the same approach, the potential of MERS-CoV to utilize the DPP4s of common Middle Eastern livestock was investigated. Modeling of the DPP4 and MERS-CoV RBD interaction predicted the ability of MERS-CoV to bind the DPP4s of camel, goat, cow, and sheep. Expression of the DPP4s of these species on BHK cells supported MERS-CoV replication. This suggests, together with the abundant DPP4 presence in the respiratory tract, that these species might be able to function as a MERS-CoV intermediate reservoir.</AbstractText>
<AbstractText Label="IMPORTANCE" NlmCategory="OBJECTIVE">The ongoing outbreak of Middle East respiratory syndrome coronavirus (MERS-CoV) has caused 701 laboratory-confirmed cases to date, with 249 fatalities. Although bats and dromedary camels have been identified as potential MERS-CoV hosts, the virus has so far not been isolated from any species other than humans. The inability of MERS-CoV to infect commonly used animal models, such as hamster, mice, and ferrets, indicates the presence of a species barrier. We show that the MERS-CoV receptor DPP4 plays a pivotal role in the observed species tropism of MERS-CoV and subsequently identified the amino acids in DPP4 responsible for this restriction. Using a combined modeling and experimental approach, we predict that, based on the ability of MERS-CoV to utilize the DPP4 of common Middle East livestock species, such as camels, goats, sheep, and cows, these form a potential MERS-CoV intermediate host reservoir species.</AbstractText>
<CopyrightInformation>Copyright © 2014, American Society for Microbiology. All Rights Reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>van Doremalen</LastName>
<ForeName>Neeltje</ForeName>
<Initials>N</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Miazgowicz</LastName>
<ForeName>Kerri L</ForeName>
<Initials>KL</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Milne-Price</LastName>
<ForeName>Shauna</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bushmaker</LastName>
<ForeName>Trenton</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Robertson</LastName>
<ForeName>Shelly</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Scott</LastName>
<ForeName>Dana</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>Rocky Mountain Veterinary Branch, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kinne</LastName>
<ForeName>Joerg</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Central Veterinary Research Laboratories, Dubai, Dubai, United Arab Emirates.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>McLellan</LastName>
<ForeName>Jason S</ForeName>
<Initials>JS</Initials>
<AffiliationInfo>
<Affiliation>Department of Biochemistry, Geisel School of Medicine at Dartmouth, Hanover, New Hampshire, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhu</LastName>
<ForeName>Jiang</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Department of Immunology and Microbial Science and Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, California, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Munster</LastName>
<ForeName>Vincent J</ForeName>
<Initials>VJ</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA vincent.munster@nih.gov.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<Agency>Intramural NIH HHS</Agency>
<Country>United States</Country>
</Grant>
</GrantList>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D052060">Research Support, N.I.H., Intramural</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2014</Year>
<Month>06</Month>
<Day>04</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>J Virol</MedlineTA>
<NlmUniqueID>0113724</NlmUniqueID>
<ISSNLinking>0022-538X</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011991">Receptors, Virus</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C078034">coronavirus receptors</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 3.4.14.5</RegistryNumber>
<NameOfSubstance UI="D018819">Dipeptidyl Peptidase 4</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002162" MajorTopicYN="N">Camelus</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002417" MajorTopicYN="N">Cattle</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002460" MajorTopicYN="N">Cell Line</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D045744" MajorTopicYN="N">Cell Line, Tumor</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017934" MajorTopicYN="N">Coronavirus</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000472" MajorTopicYN="Y">pathogenicity</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006224" MajorTopicYN="N">Cricetinae</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018819" MajorTopicYN="N">Dipeptidyl Peptidase 4</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005289" MajorTopicYN="N">Ferrets</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006041" MajorTopicYN="N">Goats</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D058507" MajorTopicYN="Y">Host Specificity</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D058751" MajorTopicYN="N">Livestock</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008253" MajorTopicYN="N">Macaca mulatta</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008810" MajorTopicYN="N">Mice, Inbred C57BL</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008877" MajorTopicYN="N" Type="Geographic">Middle East</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011323" MajorTopicYN="N">Primates</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011485" MajorTopicYN="N">Protein Binding</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011991" MajorTopicYN="N">Receptors, Virus</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012136" MajorTopicYN="N">Respiratory Syncytial Viruses</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000472" MajorTopicYN="Y">pathogenicity</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012756" MajorTopicYN="N">Sheep</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014709" MajorTopicYN="N">Vero Cells</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D056189" MajorTopicYN="N">Viral Tropism</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014779" MajorTopicYN="N">Virus Replication</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
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<Year>2014</Year>
<Month>6</Month>
<Day>6</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="pubmed">
<Year>2014</Year>
<Month>6</Month>
<Day>6</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2014</Year>
<Month>9</Month>
<Day>26</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
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<affiliations>
<list>
<country>
<li>Émirats arabes unis</li>
<li>États-Unis</li>
</country>
<region>
<li>Californie</li>
<li>Montana</li>
<li>New Hampshire</li>
</region>
</list>
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</noCountry>
<country name="États-Unis">
<region name="Montana">
<name sortKey="Van Doremalen, Neeltje" sort="Van Doremalen, Neeltje" uniqKey="Van Doremalen N" first="Neeltje" last="Van Doremalen">Neeltje Van Doremalen</name>
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<name sortKey="Bushmaker, Trenton" sort="Bushmaker, Trenton" uniqKey="Bushmaker T" first="Trenton" last="Bushmaker">Trenton Bushmaker</name>
<name sortKey="Mclellan, Jason S" sort="Mclellan, Jason S" uniqKey="Mclellan J" first="Jason S" last="Mclellan">Jason S. Mclellan</name>
<name sortKey="Miazgowicz, Kerri L" sort="Miazgowicz, Kerri L" uniqKey="Miazgowicz K" first="Kerri L" last="Miazgowicz">Kerri L. Miazgowicz</name>
<name sortKey="Milne Price, Shauna" sort="Milne Price, Shauna" uniqKey="Milne Price S" first="Shauna" last="Milne-Price">Shauna Milne-Price</name>
<name sortKey="Robertson, Shelly" sort="Robertson, Shelly" uniqKey="Robertson S" first="Shelly" last="Robertson">Shelly Robertson</name>
<name sortKey="Scott, Dana" sort="Scott, Dana" uniqKey="Scott D" first="Dana" last="Scott">Dana Scott</name>
<name sortKey="Zhu, Jiang" sort="Zhu, Jiang" uniqKey="Zhu J" first="Jiang" last="Zhu">Jiang Zhu</name>
</country>
<country name="Émirats arabes unis">
<noRegion>
<name sortKey="Kinne, Joerg" sort="Kinne, Joerg" uniqKey="Kinne J" first="Joerg" last="Kinne">Joerg Kinne</name>
</noRegion>
</country>
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