Detection of post-vaccination enhanced dengue virus infection in macaques: An improved model for early assessment of dengue vaccines
The need for improved dengue vaccines remains since the only licensed vaccine, Dengvaxia, shows variable efficacy depending on the infecting dengue virus (DENV) type, and increases the risk of hospitalization for severe dengue in children not exposed to DENV before vaccination. Here, we developed a...
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| Veröffentlicht in: | PLoS pathogens 2019-04, Vol.15 (4), p.e1007721-e1007721 |
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| creator | Borges, Maria Beatriz Marchevsky, Renato Sergio Carvalho Pereira, Renata da Silva Mendes, Ygara Almeida Mendes, Luiz Gustavo Diniz-Mendes, Leonardo Cruz, Michael A Tahmaoui, Ouafaâ Baudart, Sébastien Freire, Marcos Homma, Akira Schneider-Ohrum, Kirsten Vaughn, David W Vanloubbeeck, Yannick Lorin, Clarisse Malice, Marie-Pierre Caride, Elena Warter, Lucile |
| description | The need for improved dengue vaccines remains since the only licensed vaccine, Dengvaxia, shows variable efficacy depending on the infecting dengue virus (DENV) type, and increases the risk of hospitalization for severe dengue in children not exposed to DENV before vaccination. Here, we developed a tetravalent dengue purified and inactivated vaccine (DPIV) candidate and characterized, in rhesus macaques, its immunogenicity and efficacy to control DENV infection by analyzing, after challenge, both viral replication and changes in biological markers associated with dengue in humans. Although DPIV elicited cross-type and long-lasting DENV-neutralizing antibody responses, it failed to control DENV infection. Increased levels of viremia/RNAemia (correlating with serum capacity at enhancing DENV infection in vitro), AST, IL-10, IL-18 and IFN-γ, and decreased levels of IL-12 were detected in some vaccinated compared to non-vaccinated monkeys, indicating the vaccination may have triggered antibody-dependent enhancement of DENV infection. The dengue macaque model has been considered imperfect due to the lack of DENV-associated clinical signs. However, here we show that post-vaccination enhanced DENV infection can be detected in this model when integrating several parameters, including characterization of DENV-enhancing antibodies, viremia/RNAemia, and biomarkers relevant to dengue in humans. This improved dengue macaque model may be crucial for early assessment of efficacy and safety of future dengue vaccines. |
| doi_str_mv | 10.1371/journal.ppat.1007721 |
| format | Article |
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Here, we developed a tetravalent dengue purified and inactivated vaccine (DPIV) candidate and characterized, in rhesus macaques, its immunogenicity and efficacy to control DENV infection by analyzing, after challenge, both viral replication and changes in biological markers associated with dengue in humans. Although DPIV elicited cross-type and long-lasting DENV-neutralizing antibody responses, it failed to control DENV infection. Increased levels of viremia/RNAemia (correlating with serum capacity at enhancing DENV infection in vitro), AST, IL-10, IL-18 and IFN-γ, and decreased levels of IL-12 were detected in some vaccinated compared to non-vaccinated monkeys, indicating the vaccination may have triggered antibody-dependent enhancement of DENV infection. The dengue macaque model has been considered imperfect due to the lack of DENV-associated clinical signs. However, here we show that post-vaccination enhanced DENV infection can be detected in this model when integrating several parameters, including characterization of DENV-enhancing antibodies, viremia/RNAemia, and biomarkers relevant to dengue in humans. This improved dengue macaque model may be crucial for early assessment of efficacy and safety of future dengue vaccines.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1007721</identifier><identifier>PMID: 31009499</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Antibodies ; Antibodies, Neutralizing - immunology ; Antibodies, Viral - immunology ; Antibody-Dependent Enhancement ; Biological markers ; Biology and life sciences ; Biomarkers ; Candidates ; Child health ; Cytokines ; Dengue ; Dengue - immunology ; Dengue - prevention & control ; Dengue - virology ; Dengue fever ; Dengue hemorrhagic fever ; Dengue vaccines ; Dengue Vaccines - administration & dosage ; Dengue Vaccines - immunology ; Dengue virus ; Dengue Virus - immunology ; Disease Models, Animal ; Effectiveness ; Female ; Immunogenicity ; Immunoglobulins ; Infection ; Infections ; Interleukin 10 ; Interleukin 12 ; Interleukin 18 ; Macaca mulatta ; Macaques ; Male ; Medicine and Health Sciences ; Monkeys ; Prevention ; R&D ; Research & development ; Risk factors ; Safety and security measures ; Supervision ; Treatment outcome ; Vaccination ; Vaccines ; Vaccines, Inactivated - immunology ; Vector-borne diseases ; Viral diseases ; Viremia ; Viremia - immunology ; Viremia - virology ; Virus diseases ; Virus replication ; Viruses ; γ-Interferon</subject><ispartof>PLoS pathogens, 2019-04, Vol.15 (4), p.e1007721-e1007721</ispartof><rights>COPYRIGHT 2019 Public Library of Science</rights><rights>2019 Borges et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2019 Borges et al 2019 Borges et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c727t-305f7f3b22217b59be1a46b99bc133af5cd6021401def4d82fd6306e77bf4a4d3</citedby><cites>FETCH-LOGICAL-c727t-305f7f3b22217b59be1a46b99bc133af5cd6021401def4d82fd6306e77bf4a4d3</cites><orcidid>0000-0002-1396-1690 ; 0000-0001-9334-1979 ; 0000-0001-5220-7079 ; 0000-0001-7419-9284 ; 0000-0002-0618-9196</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6497418/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6497418/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53770,53772,79347,79348</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31009499$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Best, Sonja</contributor><creatorcontrib>Borges, Maria Beatriz</creatorcontrib><creatorcontrib>Marchevsky, Renato Sergio</creatorcontrib><creatorcontrib>Carvalho Pereira, Renata</creatorcontrib><creatorcontrib>da Silva Mendes, Ygara</creatorcontrib><creatorcontrib>Almeida Mendes, Luiz Gustavo</creatorcontrib><creatorcontrib>Diniz-Mendes, Leonardo</creatorcontrib><creatorcontrib>Cruz, Michael A</creatorcontrib><creatorcontrib>Tahmaoui, Ouafaâ</creatorcontrib><creatorcontrib>Baudart, Sébastien</creatorcontrib><creatorcontrib>Freire, Marcos</creatorcontrib><creatorcontrib>Homma, Akira</creatorcontrib><creatorcontrib>Schneider-Ohrum, Kirsten</creatorcontrib><creatorcontrib>Vaughn, David W</creatorcontrib><creatorcontrib>Vanloubbeeck, Yannick</creatorcontrib><creatorcontrib>Lorin, Clarisse</creatorcontrib><creatorcontrib>Malice, Marie-Pierre</creatorcontrib><creatorcontrib>Caride, Elena</creatorcontrib><creatorcontrib>Warter, Lucile</creatorcontrib><title>Detection of post-vaccination enhanced dengue virus infection in macaques: An improved model for early assessment of dengue vaccines</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>The need for improved dengue vaccines remains since the only licensed vaccine, Dengvaxia, shows variable efficacy depending on the infecting dengue virus (DENV) type, and increases the risk of hospitalization for severe dengue in children not exposed to DENV before vaccination. Here, we developed a tetravalent dengue purified and inactivated vaccine (DPIV) candidate and characterized, in rhesus macaques, its immunogenicity and efficacy to control DENV infection by analyzing, after challenge, both viral replication and changes in biological markers associated with dengue in humans. Although DPIV elicited cross-type and long-lasting DENV-neutralizing antibody responses, it failed to control DENV infection. Increased levels of viremia/RNAemia (correlating with serum capacity at enhancing DENV infection in vitro), AST, IL-10, IL-18 and IFN-γ, and decreased levels of IL-12 were detected in some vaccinated compared to non-vaccinated monkeys, indicating the vaccination may have triggered antibody-dependent enhancement of DENV infection. The dengue macaque model has been considered imperfect due to the lack of DENV-associated clinical signs. However, here we show that post-vaccination enhanced DENV infection can be detected in this model when integrating several parameters, including characterization of DENV-enhancing antibodies, viremia/RNAemia, and biomarkers relevant to dengue in humans. This improved dengue macaque model may be crucial for early assessment of efficacy and safety of future dengue vaccines.</description><subject>Analysis</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Antibodies, Neutralizing - immunology</subject><subject>Antibodies, Viral - immunology</subject><subject>Antibody-Dependent Enhancement</subject><subject>Biological markers</subject><subject>Biology and life sciences</subject><subject>Biomarkers</subject><subject>Candidates</subject><subject>Child health</subject><subject>Cytokines</subject><subject>Dengue</subject><subject>Dengue - immunology</subject><subject>Dengue - prevention & control</subject><subject>Dengue - virology</subject><subject>Dengue fever</subject><subject>Dengue hemorrhagic fever</subject><subject>Dengue vaccines</subject><subject>Dengue Vaccines - administration & dosage</subject><subject>Dengue Vaccines - immunology</subject><subject>Dengue virus</subject><subject>Dengue Virus - immunology</subject><subject>Disease Models, Animal</subject><subject>Effectiveness</subject><subject>Female</subject><subject>Immunogenicity</subject><subject>Immunoglobulins</subject><subject>Infection</subject><subject>Infections</subject><subject>Interleukin 10</subject><subject>Interleukin 12</subject><subject>Interleukin 18</subject><subject>Macaca mulatta</subject><subject>Macaques</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Monkeys</subject><subject>Prevention</subject><subject>R&D</subject><subject>Research & development</subject><subject>Risk factors</subject><subject>Safety and security measures</subject><subject>Supervision</subject><subject>Treatment outcome</subject><subject>Vaccination</subject><subject>Vaccines</subject><subject>Vaccines, Inactivated - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Borges, Maria Beatriz</au><au>Marchevsky, Renato Sergio</au><au>Carvalho Pereira, Renata</au><au>da Silva Mendes, Ygara</au><au>Almeida Mendes, Luiz Gustavo</au><au>Diniz-Mendes, Leonardo</au><au>Cruz, Michael A</au><au>Tahmaoui, Ouafaâ</au><au>Baudart, Sébastien</au><au>Freire, Marcos</au><au>Homma, Akira</au><au>Schneider-Ohrum, Kirsten</au><au>Vaughn, David W</au><au>Vanloubbeeck, Yannick</au><au>Lorin, Clarisse</au><au>Malice, Marie-Pierre</au><au>Caride, Elena</au><au>Warter, Lucile</au><au>Best, Sonja</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Detection of post-vaccination enhanced dengue virus infection in macaques: An improved model for early assessment of dengue vaccines</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2019-04-22</date><risdate>2019</risdate><volume>15</volume><issue>4</issue><spage>e1007721</spage><epage>e1007721</epage><pages>e1007721-e1007721</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>The need for improved dengue vaccines remains since the only licensed vaccine, Dengvaxia, shows variable efficacy depending on the infecting dengue virus (DENV) type, and increases the risk of hospitalization for severe dengue in children not exposed to DENV before vaccination. Here, we developed a tetravalent dengue purified and inactivated vaccine (DPIV) candidate and characterized, in rhesus macaques, its immunogenicity and efficacy to control DENV infection by analyzing, after challenge, both viral replication and changes in biological markers associated with dengue in humans. Although DPIV elicited cross-type and long-lasting DENV-neutralizing antibody responses, it failed to control DENV infection. Increased levels of viremia/RNAemia (correlating with serum capacity at enhancing DENV infection in vitro), AST, IL-10, IL-18 and IFN-γ, and decreased levels of IL-12 were detected in some vaccinated compared to non-vaccinated monkeys, indicating the vaccination may have triggered antibody-dependent enhancement of DENV infection. The dengue macaque model has been considered imperfect due to the lack of DENV-associated clinical signs. However, here we show that post-vaccination enhanced DENV infection can be detected in this model when integrating several parameters, including characterization of DENV-enhancing antibodies, viremia/RNAemia, and biomarkers relevant to dengue in humans. This improved dengue macaque model may be crucial for early assessment of efficacy and safety of future dengue vaccines.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31009499</pmid><doi>10.1371/journal.ppat.1007721</doi><orcidid>https://orcid.org/0000-0002-1396-1690</orcidid><orcidid>https://orcid.org/0000-0001-9334-1979</orcidid><orcidid>https://orcid.org/0000-0001-5220-7079</orcidid><orcidid>https://orcid.org/0000-0001-7419-9284</orcidid><orcidid>https://orcid.org/0000-0002-0618-9196</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1553-7374 |
| ispartof | PLoS pathogens, 2019-04, Vol.15 (4), p.e1007721-e1007721 |
| issn | 1553-7374 1553-7366 1553-7374 |
| language | eng |
| recordid | cdi_plos_journals_2251140892 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; PubMed Central Open Access; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Analysis Animals Antibodies Antibodies, Neutralizing - immunology Antibodies, Viral - immunology Antibody-Dependent Enhancement Biological markers Biology and life sciences Biomarkers Candidates Child health Cytokines Dengue Dengue - immunology Dengue - prevention & control Dengue - virology Dengue fever Dengue hemorrhagic fever Dengue vaccines Dengue Vaccines - administration & dosage Dengue Vaccines - immunology Dengue virus Dengue Virus - immunology Disease Models, Animal Effectiveness Female Immunogenicity Immunoglobulins Infection Infections Interleukin 10 Interleukin 12 Interleukin 18 Macaca mulatta Macaques Male Medicine and Health Sciences Monkeys Prevention R&D Research & development Risk factors Safety and security measures Supervision Treatment outcome Vaccination Vaccines Vaccines, Inactivated - immunology Vector-borne diseases Viral diseases Viremia Viremia - immunology Viremia - virology Virus diseases Virus replication Viruses γ-Interferon |
| title | Detection of post-vaccination enhanced dengue virus infection in macaques: An improved model for early assessment of dengue vaccines |
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