Immunization with SARS Coronavirus Vaccines Leads to Pulmonary Immunopathology on Challenge with the SARS Virus
Identifieur interne : 000A56 ( Pmc/Checkpoint ); précédent : 000A55; suivant : 000A57Immunization with SARS Coronavirus Vaccines Leads to Pulmonary Immunopathology on Challenge with the SARS Virus
Auteurs : Chien-Te Tseng [États-Unis] ; Elena Sbrana [États-Unis] ; Naoko Iwata-Yoshikawa [États-Unis] ; Patrick C. Newman [États-Unis] ; Tania Garron [États-Unis] ; Robert L. Atmar [États-Unis] ; Clarence J. Peters [États-Unis] ; Robert B. Couch [États-Unis]Source :
- PLoS ONE [ 1932-6203 ] ; 2012.
Abstract
Severe acute respiratory syndrome (SARS) emerged in China in 2002 and spread to other countries before brought under control. Because of a concern for reemergence or a deliberate release of the SARS coronavirus, vaccine development was initiated. Evaluations of an inactivated whole virus vaccine in ferrets and nonhuman primates and a virus-like-particle vaccine in mice induced protection against infection but challenged animals exhibited an immunopathologic-type lung disease.
Four candidate vaccines for humans with or without alum adjuvant were evaluated in a mouse model of SARS, a VLP vaccine, the vaccine given to ferrets and NHP, another whole virus vaccine and an rDNA-produced S protein. Balb/c or C57BL/6 mice were vaccinated IM on day 0 and 28 and sacrificed for serum antibody measurements or challenged with live virus on day 56. On day 58, challenged mice were sacrificed and lungs obtained for virus and histopathology.
All vaccines induced serum neutralizing antibody with increasing dosages and/or alum significantly increasing responses. Significant reductions of SARS-CoV two days after challenge was seen for all vaccines and prior live SARS-CoV. All mice exhibited histopathologic changes in lungs two days after challenge including all animals vaccinated (Balb/C and C57BL/6) or given live virus, influenza vaccine, or PBS suggesting infection occurred in all. Histopathology seen in animals given one of the SARS-CoV vaccines was uniformly a Th2-type immunopathology with prominent eosinophil infiltration, confirmed with special eosinophil stains. The pathologic changes seen in all control groups lacked the eosinophil prominence.
These SARS-CoV vaccines all induced antibody and protection against infection with SARS-CoV. However, challenge of mice given any of the vaccines led to occurrence of Th2-type immunopathology suggesting hypersensitivity to SARS-CoV components was induced. Caution in proceeding to application of a SARS-CoV vaccine in humans is indicated.
Url:
DOI: 10.1371/journal.pone.0035421
PubMed: 22536382
PubMed Central: 3335060
Affiliations:
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Peters</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Center for Biodefense and Emerging Disease, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Biodefense and Emerging Disease, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Couch, Robert B" sort="Couch, Robert B" uniqKey="Couch R" first="Robert B." last="Couch">Robert B. 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Newman</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Garron, Tania" sort="Garron, Tania" uniqKey="Garron T" first="Tania" last="Garron">Tania Garron</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Atmar, Robert L" sort="Atmar, Robert L" uniqKey="Atmar R" first="Robert L." last="Atmar">Robert L. Atmar</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Department of Medicine, Baylor College of Medicine, Houston, Texas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Medicine, Baylor College of Medicine, Houston, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Peters, Clarence J" sort="Peters, Clarence J" uniqKey="Peters C" first="Clarence J." last="Peters">Clarence J. Peters</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Center for Biodefense and Emerging Disease, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Biodefense and Emerging Disease, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Couch, Robert B" sort="Couch, Robert B" uniqKey="Couch R" first="Robert B." last="Couch">Robert B. Couch</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Department of Medicine, Baylor College of Medicine, Houston, Texas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Medicine, Baylor College of Medicine, Houston, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Severe acute respiratory syndrome (SARS) emerged in China in 2002 and spread to other countries before brought under control. Because of a concern for reemergence or a deliberate release of the SARS coronavirus, vaccine development was initiated. Evaluations of an inactivated whole virus vaccine in ferrets and nonhuman primates and a virus-like-particle vaccine in mice induced protection against infection but challenged animals exhibited an immunopathologic-type lung disease.</p></sec><sec><title>Design</title><p>Four candidate vaccines for humans with or without alum adjuvant were evaluated in a mouse model of SARS, a VLP vaccine, the vaccine given to ferrets and NHP, another whole virus vaccine and an rDNA-produced S protein. Balb/c or C57BL/6 mice were vaccinated IM on day 0 and 28 and sacrificed for serum antibody measurements or challenged with live virus on day 56. On day 58, challenged mice were sacrificed and lungs obtained for virus and histopathology.</p></sec><sec><title>Results</title><p>All vaccines induced serum neutralizing antibody with increasing dosages and/or alum significantly increasing responses. Significant reductions of SARS-CoV two days after challenge was seen for all vaccines and prior live SARS-CoV. All mice exhibited histopathologic changes in lungs two days after challenge including all animals vaccinated (Balb/C and C57BL/6) or given live virus, influenza vaccine, or PBS suggesting infection occurred in all. Histopathology seen in animals given one of the SARS-CoV vaccines was uniformly a Th2-type immunopathology with prominent eosinophil infiltration, confirmed with special eosinophil stains. The pathologic changes seen in all control groups lacked the eosinophil prominence.</p></sec><sec><title>Conclusions</title><p>These SARS-CoV vaccines all induced antibody and protection against infection with SARS-CoV. However, challenge of mice given any of the vaccines led to occurrence of Th2-type immunopathology suggesting hypersensitivity to SARS-CoV components was induced. Caution in proceeding to application of a SARS-CoV vaccine in humans is indicated.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Tsang, Kw" uniqKey="Tsang K">KW Tsang</name></author><author><name sortKey="Ho, Pl" uniqKey="Ho P">PL Ho</name></author><author><name sortKey="Ooi, Cg" uniqKey="Ooi C">CG Ooi</name></author><author><name sortKey="Yee, Wk" uniqKey="Yee W">WK Yee</name></author><author><name sortKey="Wang, T" uniqKey="Wang T">T Wang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Poutanen, Sm" uniqKey="Poutanen S">SM Poutanen</name></author><author><name sortKey="Low, D" uniqKey="Low D">D Low</name></author><author><name sortKey="Henry, B" uniqKey="Henry B">B Henry</name></author><author><name sortKey="Finkelstein, S" uniqKey="Finkelstein S">S Finkelstein</name></author><author><name sortKey="Rose, D" uniqKey="Rose D">D 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">22536382</article-id><article-id pub-id-type="pmc">3335060</article-id><article-id pub-id-type="publisher-id">PONE-D-12-03114</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0035421</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immunopathology</subject></subj-group></subj-group><subj-group><subject>Microbiology</subject><subj-group><subject>Immunity</subject><subj-group><subject>Immunizations</subject></subj-group></subj-group><subj-group><subject>Virology</subject><subj-group><subject>Animal Models of Infection</subject><subject>Viral Vaccines</subject></subj-group></subj-group></subj-group><subj-group><subject>Model Organisms</subject><subj-group><subject>Animal Models</subject><subj-group><subject>Mouse</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Medicine</subject><subj-group><subject>Infectious Diseases</subject><subj-group><subject>Viral Diseases</subject><subj-group><subject>SARS</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Immunization with SARS Coronavirus Vaccines Leads to Pulmonary Immunopathology on Challenge with the SARS Virus</article-title><alt-title alt-title-type="running-head">SARS Vaccine Pre-Clinical Evaluations</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Tseng</surname><given-names>Chien-Te</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sbrana</surname><given-names>Elena</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Iwata-Yoshikawa</surname><given-names>Naoko</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Newman</surname><given-names>Patrick C.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Garron</surname><given-names>Tania</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Atmar</surname><given-names>Robert L.</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Peters</surname><given-names>Clarence J.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Couch</surname><given-names>Robert B.</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Center for Biodefense and Emerging Disease, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line></aff><aff id="aff3"><label>3</label><addr-line>Department of Medicine, Baylor College of Medicine, Houston, Texas, United States of America</addr-line></aff><aff id="aff4"><label>4</label><addr-line>Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Poehlmann</surname><given-names>Stefan</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1">German Primate Center, Germany</aff><author-notes><corresp id="cor1">* E-mail: <email>rcouch@bcm.edu</email></corresp><fn fn-type="con"><p>Conceived and designed the experiments: RBC CJP C-TT. Performed the experiments: C-TT ES NI-Y PCN TG. Analyzed the data: RLA RBC C-TT. Contributed reagents/materials/analysis tools: RBC C-TT RLA ES. Wrote the paper: RBC C-TT ES.</p></fn></author-notes><pub-date pub-type="collection"><year>2012</year></pub-date><pub-date pub-type="epub"><day>20</day><month>4</month><year>2012</year></pub-date><volume>7</volume><issue>4</issue><elocation-id>e35421</elocation-id><history><date date-type="received"><day>31</day><month>1</month><year>2012</year></date><date date-type="accepted"><day>15</day><month>3</month><year>2012</year></date></history><permissions><copyright-statement>Tseng et al.</copyright-statement><copyright-year>2012</copyright-year><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.</license-p></license></permissions><abstract><sec><title>Background</title><p>Severe acute respiratory syndrome (SARS) emerged in China in 2002 and spread to other countries before brought under control. Because of a concern for reemergence or a deliberate release of the SARS coronavirus, vaccine development was initiated. Evaluations of an inactivated whole virus vaccine in ferrets and nonhuman primates and a virus-like-particle vaccine in mice induced protection against infection but challenged animals exhibited an immunopathologic-type lung disease.</p></sec><sec><title>Design</title><p>Four candidate vaccines for humans with or without alum adjuvant were evaluated in a mouse model of SARS, a VLP vaccine, the vaccine given to ferrets and NHP, another whole virus vaccine and an rDNA-produced S protein. Balb/c or C57BL/6 mice were vaccinated IM on day 0 and 28 and sacrificed for serum antibody measurements or challenged with live virus on day 56. On day 58, challenged mice were sacrificed and lungs obtained for virus and histopathology.</p></sec><sec><title>Results</title><p>All vaccines induced serum neutralizing antibody with increasing dosages and/or alum significantly increasing responses. Significant reductions of SARS-CoV two days after challenge was seen for all vaccines and prior live SARS-CoV. All mice exhibited histopathologic changes in lungs two days after challenge including all animals vaccinated (Balb/C and C57BL/6) or given live virus, influenza vaccine, or PBS suggesting infection occurred in all. Histopathology seen in animals given one of the SARS-CoV vaccines was uniformly a Th2-type immunopathology with prominent eosinophil infiltration, confirmed with special eosinophil stains. The pathologic changes seen in all control groups lacked the eosinophil prominence.</p></sec><sec><title>Conclusions</title><p>These SARS-CoV vaccines all induced antibody and protection against infection with SARS-CoV. However, challenge of mice given any of the vaccines led to occurrence of Th2-type immunopathology suggesting hypersensitivity to SARS-CoV components was induced. Caution in proceeding to application of a SARS-CoV vaccine in humans is indicated.</p></sec></abstract><counts><page-count count="13"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>États-Unis</li></country><region><li>Texas</li></region></list><tree><country name="États-Unis"><region name="Texas"><name sortKey="Tseng, Chien Te" sort="Tseng, Chien Te" uniqKey="Tseng C" first="Chien-Te" last="Tseng">Chien-Te Tseng</name></region><name sortKey="Atmar, Robert L" sort="Atmar, Robert L" uniqKey="Atmar R" first="Robert L." last="Atmar">Robert L. Atmar</name><name sortKey="Atmar, Robert L" sort="Atmar, Robert L" uniqKey="Atmar R" first="Robert L." last="Atmar">Robert L. Atmar</name><name sortKey="Couch, Robert B" sort="Couch, Robert B" uniqKey="Couch R" first="Robert B." last="Couch">Robert B. Couch</name><name sortKey="Couch, Robert B" sort="Couch, Robert B" uniqKey="Couch R" first="Robert B." last="Couch">Robert B. Couch</name><name sortKey="Garron, Tania" sort="Garron, Tania" uniqKey="Garron T" first="Tania" last="Garron">Tania Garron</name><name sortKey="Iwata Yoshikawa, Naoko" sort="Iwata Yoshikawa, Naoko" uniqKey="Iwata Yoshikawa N" first="Naoko" last="Iwata-Yoshikawa">Naoko Iwata-Yoshikawa</name><name sortKey="Iwata Yoshikawa, Naoko" sort="Iwata Yoshikawa, Naoko" uniqKey="Iwata Yoshikawa N" first="Naoko" last="Iwata-Yoshikawa">Naoko Iwata-Yoshikawa</name><name sortKey="Newman, Patrick C" sort="Newman, Patrick C" uniqKey="Newman P" first="Patrick C." last="Newman">Patrick C. Newman</name><name sortKey="Peters, Clarence J" sort="Peters, Clarence J" uniqKey="Peters C" first="Clarence J." last="Peters">Clarence J. Peters</name><name sortKey="Peters, Clarence J" sort="Peters, Clarence J" uniqKey="Peters C" first="Clarence J." last="Peters">Clarence J. Peters</name><name sortKey="Sbrana, Elena" sort="Sbrana, Elena" uniqKey="Sbrana E" first="Elena" last="Sbrana">Elena Sbrana</name><name sortKey="Tseng, Chien Te" sort="Tseng, Chien Te" uniqKey="Tseng C" first="Chien-Te" last="Tseng">Chien-Te Tseng</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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