Microneedle array delivered recombinant coronavirus vaccines: Immunogenicity and rapid translational development.
Identifieur interne : 000390 ( PubMed/Checkpoint ); précédent : 000389; suivant : 000391Microneedle array delivered recombinant coronavirus vaccines: Immunogenicity and rapid translational development.
Auteurs : Eun Kim [États-Unis] ; Geza Erdos [États-Unis] ; Shaohua Huang [États-Unis] ; Thomas W. Kenniston [États-Unis] ; Stephen C. Balmert [États-Unis] ; Cara Donahue Carey [États-Unis] ; V Stalin Raj [Pays-Bas] ; Michael W. Epperly [États-Unis] ; William B. Klimstra [États-Unis] ; Bart L. Haagmans [Pays-Bas] ; Emrullah Korkmaz [États-Unis] ; Louis D. Falo [États-Unis] ; Andrea Gambotto [États-Unis]Source :
- EBioMedicine [ 2352-3964 ] ; 2020.
Abstract
Coronaviruses pose a serious threat to global health as evidenced by Severe Acute Respiratory Syndrome (SARS), Middle East Respiratory Syndrome (MERS), and COVID-19. SARS Coronavirus (SARS-CoV), MERS Coronavirus (MERS-CoV), and the novel coronavirus, previously dubbed 2019-nCoV, and now officially named SARS-CoV-2, are the causative agents of the SARS, MERS, and COVID-19 disease outbreaks, respectively. Safe vaccines that rapidly induce potent and long-lasting virus-specific immune responses against these infectious agents are urgently needed. The coronavirus spike (S) protein, a characteristic structural component of the viral envelope, is considered a key target for vaccines for the prevention of coronavirus infection.
DOI: 10.1016/j.ebiom.2020.102743
PubMed: 32249203
Affiliations:
- Pays-Bas, États-Unis
- Hollande-Méridionale, Pennsylvanie
- Pittsburgh, Rotterdam
- Université de Pittsburgh
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Kenniston</name><affiliation wicri:level="2"><nlm:affiliation>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Balmert, Stephen C" sort="Balmert, Stephen C" uniqKey="Balmert S" first="Stephen C" last="Balmert">Stephen C. 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Epperly</name><affiliation wicri:level="4"><nlm:affiliation>Department of Radiation Oncology, University of Pittsburgh, Pittsburgh, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Radiation Oncology, University of Pittsburgh, Pittsburgh, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université de Pittsburgh</orgName></affiliation></author><author><name sortKey="Klimstra, William B" sort="Klimstra, William B" uniqKey="Klimstra W" first="William B" last="Klimstra">William B. Klimstra</name><affiliation wicri:level="4"><nlm:affiliation>Center for Vaccine Research, Department of Immunology, University of Pittsburgh, Pittsburgh, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Vaccine Research, Department of Immunology, University of Pittsburgh, Pittsburgh, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université de Pittsburgh</orgName></affiliation></author><author><name sortKey="Haagmans, Bart L" sort="Haagmans, Bart L" uniqKey="Haagmans B" first="Bart L" last="Haagmans">Bart L. Haagmans</name><affiliation wicri:level="3"><nlm:affiliation>Department of Viroscience, Erasmus Medical Center Rotterdam, Rotterdam, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Department of Viroscience, Erasmus Medical Center Rotterdam, Rotterdam</wicri:regionArea><placeName><settlement type="city">Rotterdam</settlement><region nuts="2" type="province">Hollande-Méridionale</region></placeName></affiliation></author><author><name sortKey="Korkmaz, Emrullah" sort="Korkmaz, Emrullah" uniqKey="Korkmaz E" first="Emrullah" last="Korkmaz">Emrullah Korkmaz</name><affiliation wicri:level="2"><nlm:affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA 15231, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA 15231</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Falo, Louis D" sort="Falo, Louis D" uniqKey="Falo L" first="Louis D" last="Falo">Louis D. Falo</name><affiliation wicri:level="2"><nlm:affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA 15231, USA; Clinical and Translational Science Institute, University of Pittsburgh, Pittsburgh, PA 15213, USA; The McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, PA 15219, USA. 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Electronic address: gambottoa@upmc.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32249203</idno><idno type="pmid">32249203</idno><idno type="doi">10.1016/j.ebiom.2020.102743</idno><idno type="wicri:Area/PubMed/Corpus">000347</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">000347</idno><idno type="wicri:Area/PubMed/Curation">000347</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Curation">000347</idno><idno type="wicri:Area/PubMed/Checkpoint">000390</idno><idno type="wicri:explorRef" wicri:stream="Checkpoint" wicri:step="PubMed">000390</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Microneedle array delivered recombinant coronavirus vaccines: Immunogenicity and rapid translational development.</title><author><name sortKey="Kim, Eun" sort="Kim, Eun" uniqKey="Kim E" first="Eun" last="Kim">Eun Kim</name><affiliation wicri:level="2"><nlm:affiliation>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Erdos, Geza" sort="Erdos, Geza" uniqKey="Erdos G" first="Geza" last="Erdos">Geza Erdos</name><affiliation wicri:level="2"><nlm:affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Huang, Shaohua" sort="Huang, Shaohua" uniqKey="Huang S" first="Shaohua" last="Huang">Shaohua Huang</name><affiliation wicri:level="2"><nlm:affiliation>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Kenniston, Thomas W" sort="Kenniston, Thomas W" uniqKey="Kenniston T" first="Thomas W" last="Kenniston">Thomas W. Kenniston</name><affiliation wicri:level="2"><nlm:affiliation>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Balmert, Stephen C" sort="Balmert, Stephen C" uniqKey="Balmert S" first="Stephen C" last="Balmert">Stephen C. Balmert</name><affiliation wicri:level="2"><nlm:affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Carey, Cara Donahue" sort="Carey, Cara Donahue" uniqKey="Carey C" first="Cara Donahue" last="Carey">Cara Donahue Carey</name><affiliation wicri:level="2"><nlm:affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Raj, V Stalin" sort="Raj, V Stalin" uniqKey="Raj V" first="V Stalin" last="Raj">V Stalin Raj</name><affiliation wicri:level="3"><nlm:affiliation>Department of Viroscience, Erasmus Medical Center Rotterdam, Rotterdam, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Department of Viroscience, Erasmus Medical Center Rotterdam, Rotterdam</wicri:regionArea><placeName><settlement type="city">Rotterdam</settlement><region nuts="2" type="province">Hollande-Méridionale</region></placeName></affiliation></author><author><name sortKey="Epperly, Michael W" sort="Epperly, Michael W" uniqKey="Epperly M" first="Michael W" last="Epperly">Michael W. Epperly</name><affiliation wicri:level="4"><nlm:affiliation>Department of Radiation Oncology, University of Pittsburgh, Pittsburgh, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Radiation Oncology, University of Pittsburgh, Pittsburgh, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université de Pittsburgh</orgName></affiliation></author><author><name sortKey="Klimstra, William B" sort="Klimstra, William B" uniqKey="Klimstra W" first="William B" last="Klimstra">William B. Klimstra</name><affiliation wicri:level="4"><nlm:affiliation>Center for Vaccine Research, Department of Immunology, University of Pittsburgh, Pittsburgh, PA 15213, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Vaccine Research, Department of Immunology, University of Pittsburgh, Pittsburgh, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université de Pittsburgh</orgName></affiliation></author><author><name sortKey="Haagmans, Bart L" sort="Haagmans, Bart L" uniqKey="Haagmans B" first="Bart L" last="Haagmans">Bart L. Haagmans</name><affiliation wicri:level="3"><nlm:affiliation>Department of Viroscience, Erasmus Medical Center Rotterdam, Rotterdam, the Netherlands.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>Department of Viroscience, Erasmus Medical Center Rotterdam, Rotterdam</wicri:regionArea><placeName><settlement type="city">Rotterdam</settlement><region nuts="2" type="province">Hollande-Méridionale</region></placeName></affiliation></author><author><name sortKey="Korkmaz, Emrullah" sort="Korkmaz, Emrullah" uniqKey="Korkmaz E" first="Emrullah" last="Korkmaz">Emrullah Korkmaz</name><affiliation wicri:level="2"><nlm:affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA 15231, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA 15231</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Falo, Louis D" sort="Falo, Louis D" uniqKey="Falo L" first="Louis D" last="Falo">Louis D. Falo</name><affiliation wicri:level="2"><nlm:affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA 15231, USA; Clinical and Translational Science Institute, University of Pittsburgh, Pittsburgh, PA 15213, USA; The McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, PA 15219, USA. Electronic address: lof2@pitt.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA 15231, USA; Clinical and Translational Science Institute, University of Pittsburgh, Pittsburgh, PA 15213, USA; The McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, PA 15219</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Gambotto, Andrea" sort="Gambotto, Andrea" uniqKey="Gambotto A" first="Andrea" last="Gambotto">Andrea Gambotto</name><affiliation wicri:level="2"><nlm:affiliation>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213, USA. Electronic address: gambottoa@upmc.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author></analytic><series><title level="j">EBioMedicine</title><idno type="eISSN">2352-3964</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Coronaviruses pose a serious threat to global health as evidenced by Severe Acute Respiratory Syndrome (SARS), Middle East Respiratory Syndrome (MERS), and COVID-19. SARS Coronavirus (SARS-CoV), MERS Coronavirus (MERS-CoV), and the novel coronavirus, previously dubbed 2019-nCoV, and now officially named SARS-CoV-2, are the causative agents of the SARS, MERS, and COVID-19 disease outbreaks, respectively. Safe vaccines that rapidly induce potent and long-lasting virus-specific immune responses against these infectious agents are urgently needed. The coronavirus spike (S) protein, a characteristic structural component of the viral envelope, is considered a key target for vaccines for the prevention of coronavirus infection.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32249203</PMID><DateRevised><Year>2020</Year><Month>04</Month><Day>17</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">2352-3964</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Apr</Month><Day>01</Day></PubDate></JournalIssue><Title>EBioMedicine</Title><ISOAbbreviation>EBioMedicine</ISOAbbreviation></Journal><ArticleTitle>Microneedle array delivered recombinant coronavirus vaccines: Immunogenicity and rapid translational development.</ArticleTitle><Pagination><MedlinePgn>102743</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S2352-3964(20)30118-3</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.ebiom.2020.102743</ELocationID><Abstract><AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">Coronaviruses pose a serious threat to global health as evidenced by Severe Acute Respiratory Syndrome (SARS), Middle East Respiratory Syndrome (MERS), and COVID-19. SARS Coronavirus (SARS-CoV), MERS Coronavirus (MERS-CoV), and the novel coronavirus, previously dubbed 2019-nCoV, and now officially named SARS-CoV-2, are the causative agents of the SARS, MERS, and COVID-19 disease outbreaks, respectively. Safe vaccines that rapidly induce potent and long-lasting virus-specific immune responses against these infectious agents are urgently needed. The coronavirus spike (S) protein, a characteristic structural component of the viral envelope, is considered a key target for vaccines for the prevention of coronavirus infection.</AbstractText><AbstractText Label="METHODS" NlmCategory="METHODS">We first generated codon optimized MERS-S1 subunit vaccines fused with a foldon trimerization domain to mimic the native viral structure. In variant constructs, we engineered immune stimulants (RS09 or flagellin, as TLR4 or TLR5 agonists, respectively) into this trimeric design. We comprehensively tested the pre-clinical immunogenicity of MERS-CoV vaccines in mice when delivered subcutaneously by traditional needle injection, or intracutaneously by dissolving microneedle arrays (MNAs) by evaluating virus specific IgG antibodies in the serum of vaccinated mice by ELISA and using virus neutralization assays. Driven by the urgent need for COVID-19 vaccines, we utilized this strategy to rapidly develop MNA SARS-CoV-2 subunit vaccines and tested their pre-clinical immunogenicity in vivo by exploiting our substantial experience with MNA MERS-CoV vaccines.</AbstractText><AbstractText Label="FINDINGS" NlmCategory="RESULTS">Here we describe the development of MNA delivered MERS-CoV vaccines and their pre-clinical immunogenicity. Specifically, MNA delivered MERS-S1 subunit vaccines elicited strong and long-lasting antigen-specific antibody responses. Building on our ongoing efforts to develop MERS-CoV vaccines, promising immunogenicity of MNA-delivered MERS-CoV vaccines, and our experience with MNA fabrication and delivery, including clinical trials, we rapidly designed and produced clinically-translatable MNA SARS-CoV-2 subunit vaccines within 4 weeks of the identification of the SARS-CoV-2 S1 sequence. Most importantly, these MNA delivered SARS-CoV-2 S1 subunit vaccines elicited potent antigen-specific antibody responses that were evident beginning 2 weeks after immunization.</AbstractText><AbstractText Label="INTERPRETATION" NlmCategory="CONCLUSIONS">MNA delivery of coronaviruses-S1 subunit vaccines is a promising immunization strategy against coronavirus infection. Progressive scientific and technological efforts enable quicker responses to emerging pandemics. Our ongoing efforts to develop MNA-MERS-S1 subunit vaccines enabled us to rapidly design and produce MNA SARS-CoV-2 subunit vaccines capable of inducing potent virus-specific antibody responses. Collectively, our results support the clinical development of MNA delivered recombinant protein subunit vaccines against SARS, MERS, COVID-19, and other emerging infectious diseases.</AbstractText><CopyrightInformation>Copyright © 2020 The Author(s). Published by Elsevier B.V. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Eun</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Erdos</LastName><ForeName>Geza</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Huang</LastName><ForeName>Shaohua</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kenniston</LastName><ForeName>Thomas W</ForeName><Initials>TW</Initials><AffiliationInfo><Affiliation>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Balmert</LastName><ForeName>Stephen C</ForeName><Initials>SC</Initials><AffiliationInfo><Affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Carey</LastName><ForeName>Cara Donahue</ForeName><Initials>CD</Initials><AffiliationInfo><Affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Raj</LastName><ForeName>V Stalin</ForeName><Initials>VS</Initials><AffiliationInfo><Affiliation>Department of Viroscience, Erasmus Medical Center Rotterdam, Rotterdam, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Epperly</LastName><ForeName>Michael W</ForeName><Initials>MW</Initials><AffiliationInfo><Affiliation>Department of Radiation Oncology, University of Pittsburgh, Pittsburgh, PA 15213, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Klimstra</LastName><ForeName>William B</ForeName><Initials>WB</Initials><AffiliationInfo><Affiliation>Center for Vaccine Research, Department of Immunology, University of Pittsburgh, Pittsburgh, PA 15213, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Haagmans</LastName><ForeName>Bart L</ForeName><Initials>BL</Initials><AffiliationInfo><Affiliation>Department of Viroscience, Erasmus Medical Center Rotterdam, Rotterdam, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Korkmaz</LastName><ForeName>Emrullah</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA 15231, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Falo</LastName><ForeName>Louis D</ForeName><Initials>LD</Initials><Suffix>Jr</Suffix><AffiliationInfo><Affiliation>Department of Dermatology, University of Pittsburgh School of Medicine, W1150 Biomedical Science Tower, 200 Lothrop St., Pittsburgh, PA 15213, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA 15231, USA; Clinical and Translational Science Institute, University of Pittsburgh, Pittsburgh, PA 15213, USA; The McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, PA 15219, USA. Electronic address: lof2@pitt.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gambotto</LastName><ForeName>Andrea</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, W1148 Biomedical Science Tower, 200 Lothrop St., Pennsylvania, PA 15213, USA. Electronic address: gambottoa@upmc.edu.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>R21 AI114264</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 AR071277</GrantID><Acronym>AR</Acronym><Agency>NIAMS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 AR074285</GrantID><Acronym>AR</Acronym><Agency>NIAMS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>T32 CA175294</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 AR068249</GrantID><Acronym>AR</Acronym><Agency>NIAMS NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>04</Month><Day>01</Day></ArticleDate></Article><MedlineJournalInfo><Country>Netherlands</Country><MedlineTA>EBioMedicine</MedlineTA><NlmUniqueID>101647039</NlmUniqueID><ISSNLinking>2352-3964</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">COVID-19</Keyword><Keyword MajorTopicYN="N">MERS-CoV S1</Keyword><Keyword MajorTopicYN="N">Microneedle array</Keyword><Keyword MajorTopicYN="N">SARS-CoV-2</Keyword><Keyword MajorTopicYN="N">Subunit vaccines</Keyword><Keyword MajorTopicYN="N">Trimerization</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>03</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>03</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>03</Month><Day>18</Day></PubMedPubDate><PubMedPubDate 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