Identifying the Role of E2 Domains on Alphavirus Neutralization and Protective Immune Responses
Chikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral mediators of protective immunity against alphaviruses are poorly understood, highlighted by the lack of a licensed human vaccine for any member of this v...
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| Published in | PLoS neglected tropical diseases Vol. 9; no. 10; p. e0004163 |
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| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
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United States
Public Library of Science
01.10.2015
Public Library of Science (PLoS) |
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| Abstract | Chikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral mediators of protective immunity against alphaviruses are poorly understood, highlighted by the lack of a licensed human vaccine for any member of this virus genus. The alphavirus E2, the receptor-binding envelope protein, is considered to be the predominant target of the protective host immune response. Although envelope protein domains have been studied for vaccine and neutralization in flaviviruses, their role in alphaviruses is less characterized. Here, we describe the role of the alphavirus E2 domains in neutralization and protection through the use of chimeric viruses.
Four chimeric viruses were constructed in which individual E2 domains of CHIKV were replaced with the corresponding domain from Semliki Forest virus (SFV) (ΔDomA/ΔDomB/ΔDomC/ ΔDomA+B). Vaccination studies in mice (both live and inactivated virus) revealed that domain B was the primary determinant of neutralization. Neutralization studies with CHIKV immune serum from humans were consistent with mouse studies, as ΔDomB was poorly neutralized.
Using chimeric viruses, it was determined that the alphavirus E2 domain B was the critical target of neutralizing antibodies in both mice and humans. Therefore, chimeric viruses may have more relevance for vaccine discovery than peptide-based approaches, which only detect linear epitopes. This study provides new insight into the role of alphavirus E2 domains on neutralization determinants and may be useful for the design of novel therapeutic technologies. |
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| AbstractList | Chikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral mediators of protective immunity against alphaviruses are poorly understood, highlighted by the lack of a licensed human vaccine for any member of this virus genus. The alphavirus E2, the receptor-binding envelope protein, is considered to be the predominant target of the protective host immune response. Although envelope protein domains have been studied for vaccine and neutralization in flaviviruses, their role in alphaviruses is less characterized. Here, we describe the role of the alphavirus E2 domains in neutralization and protection through the use of chimeric viruses.
Four chimeric viruses were constructed in which individual E2 domains of CHIKV were replaced with the corresponding domain from Semliki Forest virus (SFV) (ΔDomA/ΔDomB/ΔDomC/ ΔDomA+B). Vaccination studies in mice (both live and inactivated virus) revealed that domain B was the primary determinant of neutralization. Neutralization studies with CHIKV immune serum from humans were consistent with mouse studies, as ΔDomB was poorly neutralized.
Using chimeric viruses, it was determined that the alphavirus E2 domain B was the critical target of neutralizing antibodies in both mice and humans. Therefore, chimeric viruses may have more relevance for vaccine discovery than peptide-based approaches, which only detect linear epitopes. This study provides new insight into the role of alphavirus E2 domains on neutralization determinants and may be useful for the design of novel therapeutic technologies. BACKGROUNDChikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral mediators of protective immunity against alphaviruses are poorly understood, highlighted by the lack of a licensed human vaccine for any member of this virus genus. The alphavirus E2, the receptor-binding envelope protein, is considered to be the predominant target of the protective host immune response. Although envelope protein domains have been studied for vaccine and neutralization in flaviviruses, their role in alphaviruses is less characterized. Here, we describe the role of the alphavirus E2 domains in neutralization and protection through the use of chimeric viruses. METHODOLOGY/PRINCIPAL FINDINGSFour chimeric viruses were constructed in which individual E2 domains of CHIKV were replaced with the corresponding domain from Semliki Forest virus (SFV) (ΔDomA/ΔDomB/ΔDomC/ ΔDomA+B). Vaccination studies in mice (both live and inactivated virus) revealed that domain B was the primary determinant of neutralization. Neutralization studies with CHIKV immune serum from humans were consistent with mouse studies, as ΔDomB was poorly neutralized. CONCLUSIONS/SIGNIFICANCEUsing chimeric viruses, it was determined that the alphavirus E2 domain B was the critical target of neutralizing antibodies in both mice and humans. Therefore, chimeric viruses may have more relevance for vaccine discovery than peptide-based approaches, which only detect linear epitopes. This study provides new insight into the role of alphavirus E2 domains on neutralization determinants and may be useful for the design of novel therapeutic technologies. Chikungunya virus (CHIKV) is the cause of an ongoing explosive outbreak of arthritic disease in the Americas. Related alphaviruses cause human/animal disease globally, yet no vaccines or antivirals exist for human use. Although numerous candidate vaccines and therapies are being developed, little is known about the specific viral targets of an effective host immune response. Previous studies have used peptide or monoclonal antibody approaches, which can have serious limitations. Chimeric viruses between closely related species are proven tools to study a variety of viral characteristics. Using this approach, we developed a panel of viruses, which highlight the importance of the alphavirus domain B in protection in mice and serum neutralization in humans. Previous work on flaviviruses has shown that subunit approaches can be effective for vaccination and diagnostic purposes. Thus, the use of E2 domains as vaccine antigens and in clinical diagnostics for alphaviruses warrants further study. Background Chikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral mediators of protective immunity against alphaviruses are poorly understood, highlighted by the lack of a licensed human vaccine for any member of this virus genus. The alphavirus E2, the receptor-binding envelope protein, is considered to be the predominant target of the protective host immune response. Although envelope protein domains have been studied for vaccine and neutralization in flaviviruses, their role in alphaviruses is less characterized. Here, we describe the role of the alphavirus E2 domains in neutralization and protection through the use of chimeric viruses. Methodology/Principal Findings Four chimeric viruses were constructed in which individual E2 domains of CHIKV were replaced with the corresponding domain from Semliki Forest virus (SFV) (ΔDomA/ΔDomB/ ΔDomC/ΔDomA+B). Vaccination studies in mice (both live and inactivated virus) revealed that domain B was the primary determinant of neutralization. Neutralization studies with CHIKV immune serum from humans were consistent with mouse studies, as ΔDomB was poorly neutralized. Conclusions/Significance Using chimeric viruses, it was determined that the alphavirus E2 domain B was the critical target of neutralizing antibodies in both mice and humans. Therefore, chimeric viruses may have more relevance for vaccine discovery than peptide-based approaches, which only detect linear epitopes. This study provides new insight into the role of alphavirus E2 domains on neutralization determinants and may be useful for the design of novel therapeutic technologies. Chikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral mediators of protective immunity against alphaviruses are poorly understood, highlighted by the lack of a licensed human vaccine for any member of this virus genus. The alphavirus E2, the receptor-binding envelope protein, is considered to be the predominant target of the protective host immune response. Although envelope protein domains have been studied for vaccine and neutralization in flaviviruses, their role in alphaviruses is less characterized. Here, we describe the role of the alphavirus E2 domains in neutralization and protection through the use of chimeric viruses. Four chimeric viruses were constructed in which individual E2 domains of CHIKV were replaced with the corresponding domain from Semliki Forest virus (SFV) (ΔDomA/ΔDomB/ ΔDomC/ΔDomA+B). Vaccination studies in mice (both live and inactivated virus) revealed that domain B was the primary determinant of neutralization. Neutralization studies with CHIKV immune serum from humans were consistent with mouse studies, as ΔDomB was poorly neutralized. Using chimeric viruses, it was determined that the alphavirus E2 domain B was the critical target of neutralizing antibodies in both mice and humans. Therefore, chimeric viruses may have more relevance for vaccine discovery than peptide-based approaches, which only detect linear epitopes. This study provides new insight into the role of alphavirus E2 domains on neutralization determinants and may be useful for the design of novel therapeutic technologies. Background Chikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral mediators of protective immunity against alphaviruses are poorly understood, highlighted by the lack of a licensed human vaccine for any member of this virus genus. The alphavirus E2, the receptor-binding envelope protein, is considered to be the predominant target of the protective host immune response. Although envelope protein domains have been studied for vaccine and neutralization in flaviviruses, their role in alphaviruses is less characterized. Here, we describe the role of the alphavirus E2 domains in neutralization and protection through the use of chimeric viruses. Methodology/Principal Findings Four chimeric viruses were constructed in which individual E2 domains of CHIKV were replaced with the corresponding domain from Semliki Forest virus (SFV) ([delta]DomA/[delta]DomB/[delta]DomC/ [delta]DomA+B). Vaccination studies in mice (both live and inactivated virus) revealed that domain B was the primary determinant of neutralization. Neutralization studies with CHIKV immune serum from humans were consistent with mouse studies, as [delta]DomB was poorly neutralized. Conclusions/Significance Using chimeric viruses, it was determined that the alphavirus E2 domain B was the critical target of neutralizing antibodies in both mice and humans. Therefore, chimeric viruses may have more relevance for vaccine discovery than peptide-based approaches, which only detect linear epitopes. This study provides new insight into the role of alphavirus E2 domains on neutralization determinants and may be useful for the design of novel therapeutic technologies. |
| Audience | Academic |
| Author | Osorio, Jorge E Kamlangdee, Attapon Weger-Lucarelli, James Aliota, Matthew T |
| AuthorAffiliation | University of Texas Medical Branch, UNITED STATES Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin, United States of America |
| AuthorAffiliation_xml | – name: Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin, United States of America – name: University of Texas Medical Branch, UNITED STATES |
| Author_xml | – sequence: 1 givenname: James surname: Weger-Lucarelli fullname: Weger-Lucarelli, James organization: Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin, United States of America – sequence: 2 givenname: Matthew T surname: Aliota fullname: Aliota, Matthew T organization: Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin, United States of America – sequence: 3 givenname: Attapon surname: Kamlangdee fullname: Kamlangdee, Attapon organization: Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin, United States of America – sequence: 4 givenname: Jorge E surname: Osorio fullname: Osorio, Jorge E organization: Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin, United States of America |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26473963$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2015 Public Library of Science 2015 Weger-Lucarelli et al 2015 Weger-Lucarelli et al 2015 Public Library of Science. 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 credited: Weger-Lucarelli J, Aliota MT, Kamlangdee A, Osorio JE (2015) Identifying the Role of E2 Domains on Alphavirus Neutralization and Protective Immune Responses. PLoS Negl Trop Dis 9(10): e0004163. doi:10.1371/journal.pntd.0004163 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: JWL JEO. Performed the experiments: JWL MTA AK. Analyzed the data: JWL MTA AK. Contributed reagents/materials/analysis tools: JWL MTA JEO. Wrote the paper: JWL MTA JEO. The authors have declared that no competing interests exist. |
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| Snippet | Chikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral mediators of... Background Chikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral... BACKGROUNDChikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral... Chikungunya virus (CHIKV) is the cause of an ongoing explosive outbreak of arthritic disease in the Americas. Related alphaviruses cause human/animal disease... Background Chikungunya virus (CHIKV) and other alphaviruses are the etiologic agents of numerous diseases in both humans and animals. Despite this, the viral... |
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| SubjectTerms | Animal diseases Animals Antibodies, Neutralizing - blood Antibodies, Viral - blood Antigenic determinants Antigens Candidates Care and treatment Chikungunya fever Chikungunya virus - immunology Cytokines Development and progression Epidemics Epitope Mapping Genetic aspects Genomes Humans Immune response Immunoglobulins Male Mice, Inbred C57BL Mutation Neutralization Tests Protein binding Protein Structure, Tertiary Proteins Recombination, Genetic Risk factors Semliki forest virus - genetics Studies Vaccines Vaccines, Synthetic - administration & dosage Vaccines, Synthetic - immunology Viral Envelope Proteins - immunology Viruses |
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| Title | Identifying the Role of E2 Domains on Alphavirus Neutralization and Protective Immune Responses |
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