Recombinant Receptor-Binding Domains of Multiple Middle East Respiratory Syndrome Coronaviruses (MERS-CoVs) Induce Cross-Neutralizing Antibodies against Divergent Human and Camel MERS-CoVs and Antibody Escape Mutants.
Identifieur interne : 000F14 ( PubMed/Corpus ); précédent : 000F13; suivant : 000F15Recombinant Receptor-Binding Domains of Multiple Middle East Respiratory Syndrome Coronaviruses (MERS-CoVs) Induce Cross-Neutralizing Antibodies against Divergent Human and Camel MERS-CoVs and Antibody Escape Mutants.
Auteurs : Wanbo Tai ; Yufei Wang ; Craig A. Fett ; Guangyu Zhao ; Fang Li ; Stanley Perlman ; Shibo Jiang ; Yusen Zhou ; Lanying DuSource :
- Journal of virology [ 1098-5514 ] ; 2017.
English descriptors
- KwdEn :
- Animals, Antibodies, Neutralizing (biosynthesis), Antibodies, Neutralizing (chemistry), Antibodies, Viral (biosynthesis), Antibodies, Viral (chemistry), Binding Sites, Camelus, Coronavirus Infections (immunology), Coronavirus Infections (prevention & control), Coronavirus Infections (virology), Cross Reactions, Dipeptidyl Peptidase 4 (chemistry), Dipeptidyl Peptidase 4 (genetics), Dipeptidyl Peptidase 4 (immunology), Female, Gene Expression, Humans, Immune Evasion, Mice, Mice, Inbred BALB C, Middle East Respiratory Syndrome Coronavirus (genetics), Middle East Respiratory Syndrome Coronavirus (immunology), Models, Molecular, Mutation, Neutralization Tests, Plasmids (chemistry), Plasmids (metabolism), Protein Binding, Protein Interaction Domains and Motifs, Protein Structure, Secondary, Receptors, Virus (chemistry), Receptors, Virus (genetics), Receptors, Virus (immunology), Recombinant Proteins (chemistry), Recombinant Proteins (genetics), Recombinant Proteins (immunology), Spike Glycoprotein, Coronavirus (chemistry), Spike Glycoprotein, Coronavirus (genetics), Spike Glycoprotein, Coronavirus (immunology), Vaccination, Viral Vaccines (administration & dosage), Viral Vaccines (biosynthesis).
- MESH :
- chemical , administration & dosage : Viral Vaccines.
- chemical , biosynthesis : Antibodies, Neutralizing, Antibodies, Viral, Viral Vaccines.
- chemical , chemistry : Antibodies, Neutralizing, Antibodies, Viral, Dipeptidyl Peptidase 4, Receptors, Virus, Recombinant Proteins, Spike Glycoprotein, Coronavirus.
- chemical , genetics : Dipeptidyl Peptidase 4, Receptors, Virus, Recombinant Proteins, Spike Glycoprotein, Coronavirus.
- chemistry : Plasmids.
- genetics : Middle East Respiratory Syndrome Coronavirus.
- immunology : Coronavirus Infections, Dipeptidyl Peptidase 4, Middle East Respiratory Syndrome Coronavirus, Receptors, Virus, Recombinant Proteins, Spike Glycoprotein, Coronavirus.
- metabolism : Plasmids.
- prevention & control : Coronavirus Infections.
- virology : Coronavirus Infections.
- Animals, Binding Sites, Camelus, Cross Reactions, Female, Gene Expression, Humans, Immune Evasion, Mice, Mice, Inbred BALB C, Models, Molecular, Mutation, Neutralization Tests, Protein Binding, Protein Interaction Domains and Motifs, Protein Structure, Secondary, Vaccination.
Abstract
Middle East respiratory syndrome coronavirus (MERS-CoV) binds to cellular receptor dipeptidyl peptidase 4 (DPP4) via the spike (S) protein receptor-binding domain (RBD). The RBD contains critical neutralizing epitopes and serves as an important vaccine target. Since RBD mutations occur in different MERS-CoV isolates and antibody escape mutants, cross-neutralization of divergent MERS-CoV strains by RBD-induced antibodies remains unknown. Here, we constructed four recombinant RBD (rRBD) proteins with single or multiple mutations detected in representative human MERS-CoV strains from the 2012, 2013, 2014, and 2015 outbreaks, respectively, and one rRBD protein with multiple changes derived from camel MERS-CoV strains. Like the RBD of prototype EMC2012 (EMC-RBD), all five RBDs maintained good antigenicity and functionality, the ability to bind RBD-specific neutralizing monoclonal antibodies (MAbs) and the DPP4 receptor, and high immunogenicity, able to elicit S-specific antibodies. They induced potent neutralizing antibodies cross-neutralizing 17 MERS pseudoviruses expressing S proteins of representative human and camel MERS-CoV strains identified during the 2012-2015 outbreaks, 5 MAb escape MERS-CoV mutants, and 2 live human MERS-CoV strains. We then constructed two RBDs mutated in multiple key residues in the receptor-binding motif (RBM) of RBD and demonstrated their strong cross-reactivity with anti-EMC-RBD antibodies. These RBD mutants with diminished DPP4 binding also led to virus attenuation, suggesting that immunoevasion after RBD immunization is accompanied by loss of viral fitness. Therefore, this study demonstrates that MERS-CoV RBD is an important vaccine target able to induce highly potent and broad-spectrum neutralizing antibodies against infection by divergent circulating human and camel MERS-CoV strains.
DOI: 10.1128/JVI.01651-16
PubMed: 27795425
Links to Exploration step
pubmed:27795425Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Recombinant Receptor-Binding Domains of Multiple Middle East Respiratory Syndrome Coronaviruses (MERS-CoVs) Induce Cross-Neutralizing Antibodies against Divergent Human and Camel MERS-CoVs and Antibody Escape Mutants.</title><author><name sortKey="Tai, Wanbo" sort="Tai, Wanbo" uniqKey="Tai W" first="Wanbo" last="Tai">Wanbo Tai</name><affiliation><nlm:affiliation>Lindsley F. Kimball Research Institute, New York Blood Center, New York, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Yufei" sort="Wang, Yufei" uniqKey="Wang Y" first="Yufei" last="Wang">Yufei Wang</name><affiliation><nlm:affiliation>Lindsley F. Kimball Research Institute, New York Blood Center, New York, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Fett, Craig A" sort="Fett, Craig A" uniqKey="Fett C" first="Craig A" last="Fett">Craig A. Fett</name><affiliation><nlm:affiliation>Department of Microbiology, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Zhao, Guangyu" sort="Zhao, Guangyu" uniqKey="Zhao G" first="Guangyu" last="Zhao">Guangyu Zhao</name><affiliation><nlm:affiliation>State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Fang" sort="Li, Fang" uniqKey="Li F" first="Fang" last="Li">Fang Li</name><affiliation><nlm:affiliation>Department of Pharmacology, University of Minnesota Medical School, Minneapolis, Minnesota, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name><affiliation><nlm:affiliation>Department of Microbiology, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Jiang, Shibo" sort="Jiang, Shibo" uniqKey="Jiang S" first="Shibo" last="Jiang">Shibo Jiang</name><affiliation><nlm:affiliation>Lindsley F. Kimball Research Institute, New York Blood Center, New York, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Zhou, Yusen" sort="Zhou, Yusen" uniqKey="Zhou Y" first="Yusen" last="Zhou">Yusen Zhou</name><affiliation><nlm:affiliation>State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China yszhou@bmi.ac.cn ldu@nybc.org.</nlm:affiliation></affiliation></author><author><name sortKey="Du, Lanying" sort="Du, Lanying" uniqKey="Du L" first="Lanying" last="Du">Lanying Du</name><affiliation><nlm:affiliation>Lindsley F. 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Kimball Research Institute, New York Blood Center, New York, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Yufei" sort="Wang, Yufei" uniqKey="Wang Y" first="Yufei" last="Wang">Yufei Wang</name><affiliation><nlm:affiliation>Lindsley F. Kimball Research Institute, New York Blood Center, New York, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Fett, Craig A" sort="Fett, Craig A" uniqKey="Fett C" first="Craig A" last="Fett">Craig A. Fett</name><affiliation><nlm:affiliation>Department of Microbiology, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Zhao, Guangyu" sort="Zhao, Guangyu" uniqKey="Zhao G" first="Guangyu" last="Zhao">Guangyu Zhao</name><affiliation><nlm:affiliation>State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Fang" sort="Li, Fang" uniqKey="Li F" first="Fang" last="Li">Fang Li</name><affiliation><nlm:affiliation>Department of Pharmacology, University of Minnesota Medical School, Minneapolis, Minnesota, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Perlman, Stanley" sort="Perlman, Stanley" uniqKey="Perlman S" first="Stanley" last="Perlman">Stanley Perlman</name><affiliation><nlm:affiliation>Department of Microbiology, University of Iowa, Iowa City, Iowa, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Jiang, Shibo" sort="Jiang, Shibo" uniqKey="Jiang S" first="Shibo" last="Jiang">Shibo Jiang</name><affiliation><nlm:affiliation>Lindsley F. Kimball Research Institute, New York Blood Center, New York, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Zhou, Yusen" sort="Zhou, Yusen" uniqKey="Zhou Y" first="Yusen" last="Zhou">Yusen Zhou</name><affiliation><nlm:affiliation>State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China yszhou@bmi.ac.cn ldu@nybc.org.</nlm:affiliation></affiliation></author><author><name sortKey="Du, Lanying" sort="Du, Lanying" uniqKey="Du L" first="Lanying" last="Du">Lanying Du</name><affiliation><nlm:affiliation>Lindsley F. Kimball Research Institute, New York Blood Center, New York, New York, USA yszhou@bmi.ac.cn ldu@nybc.org.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Journal of virology</title><idno type="eISSN">1098-5514</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Antibodies, Neutralizing (biosynthesis)</term><term>Antibodies, Neutralizing (chemistry)</term><term>Antibodies, Viral (biosynthesis)</term><term>Antibodies, Viral (chemistry)</term><term>Binding Sites</term><term>Camelus</term><term>Coronavirus Infections (immunology)</term><term>Coronavirus Infections (prevention & control)</term><term>Coronavirus Infections (virology)</term><term>Cross Reactions</term><term>Dipeptidyl Peptidase 4 (chemistry)</term><term>Dipeptidyl Peptidase 4 (genetics)</term><term>Dipeptidyl Peptidase 4 (immunology)</term><term>Female</term><term>Gene Expression</term><term>Humans</term><term>Immune Evasion</term><term>Mice</term><term>Mice, Inbred BALB C</term><term>Middle East Respiratory Syndrome Coronavirus (genetics)</term><term>Middle East Respiratory Syndrome Coronavirus (immunology)</term><term>Models, Molecular</term><term>Mutation</term><term>Neutralization Tests</term><term>Plasmids (chemistry)</term><term>Plasmids (metabolism)</term><term>Protein Binding</term><term>Protein Interaction Domains and Motifs</term><term>Protein Structure, Secondary</term><term>Receptors, Virus (chemistry)</term><term>Receptors, Virus (genetics)</term><term>Receptors, Virus (immunology)</term><term>Recombinant Proteins (chemistry)</term><term>Recombinant Proteins (genetics)</term><term>Recombinant Proteins (immunology)</term><term>Spike Glycoprotein, Coronavirus (chemistry)</term><term>Spike Glycoprotein, Coronavirus (genetics)</term><term>Spike Glycoprotein, Coronavirus (immunology)</term><term>Vaccination</term><term>Viral Vaccines (administration & dosage)</term><term>Viral Vaccines (biosynthesis)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="administration & dosage" xml:lang="en"><term>Viral Vaccines</term></keywords><keywords scheme="MESH" type="chemical" qualifier="biosynthesis" xml:lang="en"><term>Antibodies, Neutralizing</term><term>Antibodies, Viral</term><term>Viral Vaccines</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Antibodies, Neutralizing</term><term>Antibodies, Viral</term><term>Dipeptidyl Peptidase 4</term><term>Receptors, Virus</term><term>Recombinant Proteins</term><term>Spike Glycoprotein, Coronavirus</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Dipeptidyl Peptidase 4</term><term>Receptors, Virus</term><term>Recombinant Proteins</term><term>Spike Glycoprotein, Coronavirus</term></keywords><keywords scheme="MESH" qualifier="chemistry" xml:lang="en"><term>Plasmids</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Middle East Respiratory Syndrome Coronavirus</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Coronavirus Infections</term><term>Dipeptidyl Peptidase 4</term><term>Middle East Respiratory Syndrome Coronavirus</term><term>Receptors, Virus</term><term>Recombinant Proteins</term><term>Spike Glycoprotein, Coronavirus</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Plasmids</term></keywords><keywords scheme="MESH" qualifier="prevention & control" xml:lang="en"><term>Coronavirus Infections</term></keywords><keywords scheme="MESH" qualifier="virology" xml:lang="en"><term>Coronavirus Infections</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Binding Sites</term><term>Camelus</term><term>Cross Reactions</term><term>Female</term><term>Gene Expression</term><term>Humans</term><term>Immune Evasion</term><term>Mice</term><term>Mice, Inbred BALB C</term><term>Models, Molecular</term><term>Mutation</term><term>Neutralization Tests</term><term>Protein Binding</term><term>Protein Interaction Domains and Motifs</term><term>Protein Structure, Secondary</term><term>Vaccination</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Middle East respiratory syndrome coronavirus (MERS-CoV) binds to cellular receptor dipeptidyl peptidase 4 (DPP4) via the spike (S) protein receptor-binding domain (RBD). The RBD contains critical neutralizing epitopes and serves as an important vaccine target. Since RBD mutations occur in different MERS-CoV isolates and antibody escape mutants, cross-neutralization of divergent MERS-CoV strains by RBD-induced antibodies remains unknown. Here, we constructed four recombinant RBD (rRBD) proteins with single or multiple mutations detected in representative human MERS-CoV strains from the 2012, 2013, 2014, and 2015 outbreaks, respectively, and one rRBD protein with multiple changes derived from camel MERS-CoV strains. Like the RBD of prototype EMC2012 (EMC-RBD), all five RBDs maintained good antigenicity and functionality, the ability to bind RBD-specific neutralizing monoclonal antibodies (MAbs) and the DPP4 receptor, and high immunogenicity, able to elicit S-specific antibodies. They induced potent neutralizing antibodies cross-neutralizing 17 MERS pseudoviruses expressing S proteins of representative human and camel MERS-CoV strains identified during the 2012-2015 outbreaks, 5 MAb escape MERS-CoV mutants, and 2 live human MERS-CoV strains. We then constructed two RBDs mutated in multiple key residues in the receptor-binding motif (RBM) of RBD and demonstrated their strong cross-reactivity with anti-EMC-RBD antibodies. These RBD mutants with diminished DPP4 binding also led to virus attenuation, suggesting that immunoevasion after RBD immunization is accompanied by loss of viral fitness. Therefore, this study demonstrates that MERS-CoV RBD is an important vaccine target able to induce highly potent and broad-spectrum neutralizing antibodies against infection by divergent circulating human and camel MERS-CoV strains.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">27795425</PMID><DateCompleted><Year>2017</Year><Month>05</Month><Day>15</Day></DateCompleted><DateRevised><Year>2019</Year><Month>03</Month><Day>29</Day></DateRevised><Article PubModel="Electronic-Print"><Journal><ISSN IssnType="Electronic">1098-5514</ISSN><JournalIssue CitedMedium="Internet"><Volume>91</Volume><Issue>1</Issue><PubDate><Year>2017</Year><Month>Jan</Month><Day>01</Day></PubDate></JournalIssue><Title>Journal of virology</Title><ISOAbbreviation>J. Virol.</ISOAbbreviation></Journal><ArticleTitle>Recombinant Receptor-Binding Domains of Multiple Middle East Respiratory Syndrome Coronaviruses (MERS-CoVs) Induce Cross-Neutralizing Antibodies against Divergent Human and Camel MERS-CoVs and Antibody Escape Mutants.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">e01651-16</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1128/JVI.01651-16</ELocationID><Abstract><AbstractText>Middle East respiratory syndrome coronavirus (MERS-CoV) binds to cellular receptor dipeptidyl peptidase 4 (DPP4) via the spike (S) protein receptor-binding domain (RBD). The RBD contains critical neutralizing epitopes and serves as an important vaccine target. Since RBD mutations occur in different MERS-CoV isolates and antibody escape mutants, cross-neutralization of divergent MERS-CoV strains by RBD-induced antibodies remains unknown. Here, we constructed four recombinant RBD (rRBD) proteins with single or multiple mutations detected in representative human MERS-CoV strains from the 2012, 2013, 2014, and 2015 outbreaks, respectively, and one rRBD protein with multiple changes derived from camel MERS-CoV strains. Like the RBD of prototype EMC2012 (EMC-RBD), all five RBDs maintained good antigenicity and functionality, the ability to bind RBD-specific neutralizing monoclonal antibodies (MAbs) and the DPP4 receptor, and high immunogenicity, able to elicit S-specific antibodies. They induced potent neutralizing antibodies cross-neutralizing 17 MERS pseudoviruses expressing S proteins of representative human and camel MERS-CoV strains identified during the 2012-2015 outbreaks, 5 MAb escape MERS-CoV mutants, and 2 live human MERS-CoV strains. We then constructed two RBDs mutated in multiple key residues in the receptor-binding motif (RBM) of RBD and demonstrated their strong cross-reactivity with anti-EMC-RBD antibodies. These RBD mutants with diminished DPP4 binding also led to virus attenuation, suggesting that immunoevasion after RBD immunization is accompanied by loss of viral fitness. Therefore, this study demonstrates that MERS-CoV RBD is an important vaccine target able to induce highly potent and broad-spectrum neutralizing antibodies against infection by divergent circulating human and camel MERS-CoV strains.</AbstractText><AbstractText Label="IMPORTANCE" NlmCategory="OBJECTIVE">MERS-CoV was first identified in June 2012 and has since spread in humans and camels. Mutations in its spike (S) protein receptor-binding domain (RBD), a key vaccine target, have been identified, raising concerns over the efficacy of RBD-based MERS vaccines against circulating human and camel MERS-CoV strains. Here, we constructed five vaccine candidates, designated 2012-RBD, 2013-RBD, 2014-RBD, 2015-RBD, and Camel-RBD, containing single or multiple mutations in the RBD of representative human and camel MERS-CoV strains during the 2012-2015 outbreaks. These RBD-based vaccine candidates maintained good functionality, antigenicity, and immunogenicity, and they induced strong cross-neutralizing antibodies against infection by divergent pseudotyped and live MERS-CoV strains, as well as antibody escape MERS-CoV mutants. This study provides impetus for further development of a safe, highly effective, and broad-spectrum RBD-based subunit vaccine to prevent MERS-CoV infection.</AbstractText><CopyrightInformation>Copyright © 2016 American Society for Microbiology.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Tai</LastName><ForeName>Wanbo</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Lindsley F. Kimball Research Institute, New York Blood Center, New York, New York, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yufei</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Lindsley F. Kimball Research Institute, New York Blood Center, New York, New York, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fett</LastName><ForeName>Craig A</ForeName><Initials>CA</Initials><AffiliationInfo><Affiliation>Department of Microbiology, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhao</LastName><ForeName>Guangyu</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Fang</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, University of Minnesota Medical School, Minneapolis, Minnesota, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Perlman</LastName><ForeName>Stanley</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Microbiology, University of Iowa, Iowa City, Iowa, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jiang</LastName><ForeName>Shibo</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Lindsley F. Kimball Research Institute, New York Blood Center, New York, New York, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Medical Molecular Virology of Ministries of Education and Health, Basic Medical College and Institute of Medical Microbiology, Fudan University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhou</LastName><ForeName>Yusen</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China yszhou@bmi.ac.cn ldu@nybc.org.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Du</LastName><ForeName>Lanying</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Lindsley F. Kimball Research Institute, New York Blood Center, New York, New York, USA yszhou@bmi.ac.cn ldu@nybc.org.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>R01 AI098775</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 AI089728</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 AI110700</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R21 AI109094</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>U01 AI124260</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 AI129269</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>P01 AI060699</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>12</Month><Day>16</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="D057134">Antibodies, Neutralizing</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000914">Antibodies, Viral</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D011991">Receptors, Virus</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D011994">Recombinant Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D064370">Spike Glycoprotein, Coronavirus</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D014765">Viral Vaccines</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.4.14.5</RegistryNumber><NameOfSubstance UI="C042807">DPP4 protein, human</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="D057134" MajorTopicYN="N">Antibodies, Neutralizing</DescriptorName><QualifierName UI="Q000096" MajorTopicYN="Y">biosynthesis</QualifierName><QualifierName UI="Q000737" 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UI="D017433" MajorTopicYN="N">Protein Structure, Secondary</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D011991" MajorTopicYN="N">Receptors, Virus</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011994" MajorTopicYN="N">Recombinant Proteins</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D064370" MajorTopicYN="N">Spike Glycoprotein, Coronavirus</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000276" 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