Combined live oral priming and intramuscular boosting regimen with Rotarix® and a nanoparticle-based trivalent rotavirus vaccine evaluated in gnotobiotic pig models of G4P[6] and G1P[8] human rotavirus infection

Human rotavirus (HRV) is the causative agent of severe dehydrating diarrhea in children under the age of five, resulting in up to 215,000 deaths each year. These deaths almost exclusively occur in low- and middle-income countries where vaccine efficacy is the lowest due to chronic malnutrition, gut...

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Main Authors: Hensley, Casey, Nyblade, Charlotte, Zhou, Peng, Parreño, Gladys Viviana, Ramesh, Ashwin, Frazier, Annie, Frazier, Maggie, Garrison, Sarah, Fantasia-Davis, Ariana, Cai, Ruiqing, Huang, Peng-Wei, Xia, Ming, Tan, Ming, Yuan, Lijuan
Format: info:ar-repo/semantics/artículo
Language:Inglés
Published: MDPI 2023
Subjects:
Online Access:http://hdl.handle.net/20.500.12123/15201
https://www.mdpi.com/2076-393X/11/5/927
https://doi.org/10.3390/vaccines11050927
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author Hensley, Casey
Nyblade, Charlotte
Zhou, Peng
Parreño, Gladys Viviana
Ramesh, Ashwin
Frazier, Annie
Frazier, Maggie
Garrison, Sarah
Fantasia-Davis, Ariana
Cai, Ruiqing
Huang, Peng-Wei
Xia, Ming
Tan, Ming
Yuan, Lijuan
author_browse Cai, Ruiqing
Fantasia-Davis, Ariana
Frazier, Annie
Frazier, Maggie
Garrison, Sarah
Hensley, Casey
Huang, Peng-Wei
Nyblade, Charlotte
Parreño, Gladys Viviana
Ramesh, Ashwin
Tan, Ming
Xia, Ming
Yuan, Lijuan
Zhou, Peng
author_facet Hensley, Casey
Nyblade, Charlotte
Zhou, Peng
Parreño, Gladys Viviana
Ramesh, Ashwin
Frazier, Annie
Frazier, Maggie
Garrison, Sarah
Fantasia-Davis, Ariana
Cai, Ruiqing
Huang, Peng-Wei
Xia, Ming
Tan, Ming
Yuan, Lijuan
author_sort Hensley, Casey
collection INTA Digital
description Human rotavirus (HRV) is the causative agent of severe dehydrating diarrhea in children under the age of five, resulting in up to 215,000 deaths each year. These deaths almost exclusively occur in low- and middle-income countries where vaccine efficacy is the lowest due to chronic malnutrition, gut dysbiosis, and concurrent enteric viral infection. Parenteral vaccines for HRV are particularly attractive as they avoid many of the concerns associated with currently used live oral vaccines. In this study, a two-dose intramuscular (IM) regimen of the trivalent, nanoparticle-based, nonreplicating HRV vaccine (trivalent S60-VP8*), utilizing the shell (S) domain of the capsid of norovirus as an HRV VP8* antigen display platform, was evaluated for immunogenicity and protective efficacy against P[6] and P[8] HRV using gnotobiotic pig models. A prime–boost strategy using one dose of the oral Rotarix® vaccine, followed by one dose of the IM trivalent nanoparticle vaccine was also evaluated. Both regimens were highly immunogenic in inducing serum virus neutralizing, IgG, and IgA antibodies. The two vaccine regimens failed to confer significant protection against diarrhea; however, the prime–boost regimen significantly shortened the duration of virus shedding in pigs challenged orally with the virulent Wa (G1P[8]) HRV and significantly shortened the mean duration of virus shedding, mean peak titer, and area under the curve of virus shedding after challenge with Arg (G4P[6]) HRV. Prime–boost-vaccinated pigs challenged with P[8] HRV had significantly higher P[8]-specific IgG antibody-secreting cells (ASCs) in the spleen post-challenge. Prime–boost-vaccinated pigs challenged with P[6] HRV had significantly higher numbers of P[6]- and P[8]-specific IgG ASCs in the ileum, as well as significantly higher numbers of P[8]-specific IgA ASCs in the spleen post-challenge. These results suggest the promise of and warrant further investigation into the oral priming and parenteral boosting strategy for future HRV vaccines.
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institution Instituto Nacional de Tecnología Agropecuaria (INTA -Argentina)
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spelling INTA152012023-09-13T14:02:11Z Combined live oral priming and intramuscular boosting regimen with Rotarix® and a nanoparticle-based trivalent rotavirus vaccine evaluated in gnotobiotic pig models of G4P[6] and G1P[8] human rotavirus infection Hensley, Casey Nyblade, Charlotte Zhou, Peng Parreño, Gladys Viviana Ramesh, Ashwin Frazier, Annie Frazier, Maggie Garrison, Sarah Fantasia-Davis, Ariana Cai, Ruiqing Huang, Peng-Wei Xia, Ming Tan, Ming Yuan, Lijuan Rotavirus Nanoparticles Gnotobiotic Animals Swine Vaccines Nanopartículas Animales Notobióticos Cerdo Vacuna Human Rotavirus Infection Infección por Rotavirus Humano Human rotavirus (HRV) is the causative agent of severe dehydrating diarrhea in children under the age of five, resulting in up to 215,000 deaths each year. These deaths almost exclusively occur in low- and middle-income countries where vaccine efficacy is the lowest due to chronic malnutrition, gut dysbiosis, and concurrent enteric viral infection. Parenteral vaccines for HRV are particularly attractive as they avoid many of the concerns associated with currently used live oral vaccines. In this study, a two-dose intramuscular (IM) regimen of the trivalent, nanoparticle-based, nonreplicating HRV vaccine (trivalent S60-VP8*), utilizing the shell (S) domain of the capsid of norovirus as an HRV VP8* antigen display platform, was evaluated for immunogenicity and protective efficacy against P[6] and P[8] HRV using gnotobiotic pig models. A prime–boost strategy using one dose of the oral Rotarix® vaccine, followed by one dose of the IM trivalent nanoparticle vaccine was also evaluated. Both regimens were highly immunogenic in inducing serum virus neutralizing, IgG, and IgA antibodies. The two vaccine regimens failed to confer significant protection against diarrhea; however, the prime–boost regimen significantly shortened the duration of virus shedding in pigs challenged orally with the virulent Wa (G1P[8]) HRV and significantly shortened the mean duration of virus shedding, mean peak titer, and area under the curve of virus shedding after challenge with Arg (G4P[6]) HRV. Prime–boost-vaccinated pigs challenged with P[8] HRV had significantly higher P[8]-specific IgG antibody-secreting cells (ASCs) in the spleen post-challenge. Prime–boost-vaccinated pigs challenged with P[6] HRV had significantly higher numbers of P[6]- and P[8]-specific IgG ASCs in the ileum, as well as significantly higher numbers of P[8]-specific IgA ASCs in the spleen post-challenge. These results suggest the promise of and warrant further investigation into the oral priming and parenteral boosting strategy for future HRV vaccines. Instituto de Virología Fil: Hensley, Casey. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos Fil: Nyblade, Charlotte. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos Fil: Zhou, Peng. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos Fil: Parreño, Gladys Viviana. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos Fil: Parreño, Gladys Viviana. Instituto Nacional de Tecnología Agropecuaria (INTA). INCUINTA. Instituto de Virologia e Innovaciones Tecnologicas (IVIT); Argentina Fil: Parreño, Gladys Viviana. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Ramesh, Ashwin. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos Fil: Frazier, Annie. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos Fil: Frazier, Maggie. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos Fil: Garrison, Sarah. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos Fil: Fantasia-Davis, Ariana. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos Fil: Cai, Ruiqing. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos Fil: Huang, Peng-Wei. Cincinnati Children’s Hospital Medical Center. Division of Infectious Diseases; Estados Unidos Fil: Xia, Ming. Cincinnati Children’s Hospital Medical Center. Division of Infectious Diseases; Estados Unidos Fil: Tan, Ming. Cincinnati Children’s Hospital Medical Center. Division of Infectious Diseases; Estados Unidos Fil: Tan, Ming. University of Cincinnati College of Medicine. Department of Pediatrics; Estados Unidos Fil: Yuan, Lijuan. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos 2023-09-13T13:57:21Z 2023-09-13T13:57:21Z 2023-05 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion http://hdl.handle.net/20.500.12123/15201 https://www.mdpi.com/2076-393X/11/5/927 2076-393X https://doi.org/10.3390/vaccines11050927 eng info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by-nc-sa/4.0/ Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) application/pdf MDPI Vaccines 11 (5) : 927 (Mayo 2023)
spellingShingle Rotavirus
Nanoparticles
Gnotobiotic Animals
Swine
Vaccines
Nanopartículas
Animales Notobióticos
Cerdo
Vacuna
Human Rotavirus Infection
Infección por Rotavirus Humano
Hensley, Casey
Nyblade, Charlotte
Zhou, Peng
Parreño, Gladys Viviana
Ramesh, Ashwin
Frazier, Annie
Frazier, Maggie
Garrison, Sarah
Fantasia-Davis, Ariana
Cai, Ruiqing
Huang, Peng-Wei
Xia, Ming
Tan, Ming
Yuan, Lijuan
Combined live oral priming and intramuscular boosting regimen with Rotarix® and a nanoparticle-based trivalent rotavirus vaccine evaluated in gnotobiotic pig models of G4P[6] and G1P[8] human rotavirus infection
title Combined live oral priming and intramuscular boosting regimen with Rotarix® and a nanoparticle-based trivalent rotavirus vaccine evaluated in gnotobiotic pig models of G4P[6] and G1P[8] human rotavirus infection
title_full Combined live oral priming and intramuscular boosting regimen with Rotarix® and a nanoparticle-based trivalent rotavirus vaccine evaluated in gnotobiotic pig models of G4P[6] and G1P[8] human rotavirus infection
title_fullStr Combined live oral priming and intramuscular boosting regimen with Rotarix® and a nanoparticle-based trivalent rotavirus vaccine evaluated in gnotobiotic pig models of G4P[6] and G1P[8] human rotavirus infection
title_full_unstemmed Combined live oral priming and intramuscular boosting regimen with Rotarix® and a nanoparticle-based trivalent rotavirus vaccine evaluated in gnotobiotic pig models of G4P[6] and G1P[8] human rotavirus infection
title_short Combined live oral priming and intramuscular boosting regimen with Rotarix® and a nanoparticle-based trivalent rotavirus vaccine evaluated in gnotobiotic pig models of G4P[6] and G1P[8] human rotavirus infection
title_sort combined live oral priming and intramuscular boosting regimen with rotarix r and a nanoparticle based trivalent rotavirus vaccine evaluated in gnotobiotic pig models of g4p 6 and g1p 8 human rotavirus infection
topic Rotavirus
Nanoparticles
Gnotobiotic Animals
Swine
Vaccines
Nanopartículas
Animales Notobióticos
Cerdo
Vacuna
Human Rotavirus Infection
Infección por Rotavirus Humano
url http://hdl.handle.net/20.500.12123/15201
https://www.mdpi.com/2076-393X/11/5/927
https://doi.org/10.3390/vaccines11050927
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