Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigs

Autores
Nyblade, Charlotte; Zhou, Peng; Frazier, Maggie; Frazier, Annie; Hensley, Casey; Fantasia-Davis, Ariana; Shahrudin, Shabihah; Hoffer, Miranda; Agbemabiese, Chantal Ama; LaRue, Lauren; Barro, Mario; Patton, John T.; Parreño, Gladys Viviana; Yuan, Lijuan
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Human rotavirus (HRV) is a leading cause of viral gastroenteritis in children across the globe. The virus has long been established as a pathogen of the gastrointestinal tract, targeting small intestine epithelial cells and leading to diarrhea, nausea, and vomiting. Recently, this classical infection pathway was challenged by the findings that murine strains of rotavirus can infect the salivary glands of pups and dams and transmit via saliva from pups to dams during suckling. Here, we aimed to determine if HRV was also capable of infecting salivary glands and spreading in saliva using a gnotobiotic (Gn) pig model of HRV infection and disease. Gn pigs were orally inoculated with various strains of HRV, and virus shedding was monitored for several days post-inoculation. HRV was shed nasally and in feces in all inoculated pigs. Infectious HRV was detected in the saliva of four piglets. Structural and non-structural HRV proteins, as well as the HRV genome, were detected in the intestinal and facial tissues of inoculated pigs. The pigs developed high IgM antibody responses in serum and small intestinal contents at 10 days post-inoculation. Additionally, inoculated pigs had HRV-specific IgM antibody-secreting cells present in the ileum, tonsils, and facial lymphoid tissues. Taken together, these findings indicate that HRV can replicate in salivary tissues and prime immune responses in both intestinal and facial lymphoid tissues of Gn pigs.
Instituto de Virología
Fil: Nyblade, Charlotte. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Zhou, Peng. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Frazier, Maggie. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Frazier, Annie. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Hensley, Casey. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Fantasia-Davis, Ariana. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Shahrudin, Shabihah. Indiana University. Department of Biology; Estados Unidos
Fil: Hoffer, Miranda. Indiana University. Department of Biology; Estados Unidos
Fil: Agbemabiese, Chantal Ama. Indiana University. Department of Biology; Estados Unidos
Fil: LaRue, Lauren. GIVAX Inc.; Estados Unidos
Fil: Barro, Mario. GIVAX Inc.; Estados Unidos
Fil: Patton, John T. Indiana University. Department of Biology; Estados Unidos
Fil: Parreño, Gladys Viviana. Virginia Polytechnic Institute and State University. 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: Yuan, Lijuan. Virginia Polytechnic Institute and State University. Center for Emerging, Zoonotic, and Arthropod‑Borne Pathogens; Estados Unidos
Fuente
Viruses 15 (9) : 1864 (Agosto 2023)
Materia
Rotavirus
Gnotobiotic Animals
Swine
Salivary Glands
Immune Response
Animales Notobióticos
Cerdo
Glándulas Salivales
Respuesta Inmunológica
Human Rotavirus Infection
Infección por Rotavirus Humano
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by-nc-sa/4.0/
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
oai:localhost:20.500.12123/15204
Acceder
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oai_identifier_str oai:localhost:20.500.12123/15204
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network_name_str INTA Digital (INTA)
spelling Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigsNyblade, CharlotteZhou, PengFrazier, MaggieFrazier, AnnieHensley, CaseyFantasia-Davis, ArianaShahrudin, ShabihahHoffer, MirandaAgbemabiese, Chantal AmaLaRue, LaurenBarro, MarioPatton, John T.Parreño, Gladys VivianaYuan, LijuanRotavirusGnotobiotic AnimalsSwineSalivary GlandsImmune ResponseAnimales NotobióticosCerdoGlándulas SalivalesRespuesta InmunológicaHuman Rotavirus InfectionInfección por Rotavirus HumanoHuman rotavirus (HRV) is a leading cause of viral gastroenteritis in children across the globe. The virus has long been established as a pathogen of the gastrointestinal tract, targeting small intestine epithelial cells and leading to diarrhea, nausea, and vomiting. Recently, this classical infection pathway was challenged by the findings that murine strains of rotavirus can infect the salivary glands of pups and dams and transmit via saliva from pups to dams during suckling. Here, we aimed to determine if HRV was also capable of infecting salivary glands and spreading in saliva using a gnotobiotic (Gn) pig model of HRV infection and disease. Gn pigs were orally inoculated with various strains of HRV, and virus shedding was monitored for several days post-inoculation. HRV was shed nasally and in feces in all inoculated pigs. Infectious HRV was detected in the saliva of four piglets. Structural and non-structural HRV proteins, as well as the HRV genome, were detected in the intestinal and facial tissues of inoculated pigs. The pigs developed high IgM antibody responses in serum and small intestinal contents at 10 days post-inoculation. Additionally, inoculated pigs had HRV-specific IgM antibody-secreting cells present in the ileum, tonsils, and facial lymphoid tissues. Taken together, these findings indicate that HRV can replicate in salivary tissues and prime immune responses in both intestinal and facial lymphoid tissues of Gn pigs.Instituto de VirologíaFil: Nyblade, Charlotte. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados UnidosFil: Zhou, Peng. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados UnidosFil: Frazier, Maggie. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados UnidosFil: Frazier, Annie. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados UnidosFil: Hensley, Casey. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados UnidosFil: Fantasia-Davis, Ariana. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados UnidosFil: Shahrudin, Shabihah. Indiana University. Department of Biology; Estados UnidosFil: Hoffer, Miranda. Indiana University. Department of Biology; Estados UnidosFil: Agbemabiese, Chantal Ama. Indiana University. Department of Biology; Estados UnidosFil: LaRue, Lauren. GIVAX Inc.; Estados UnidosFil: Barro, Mario. GIVAX Inc.; Estados UnidosFil: Patton, John T. Indiana University. Department of Biology; Estados UnidosFil: Parreño, Gladys Viviana. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados UnidosFil: Parreño, Gladys Viviana. Instituto Nacional de Tecnología Agropecuaria (INTA). INCUINTA. Instituto de Virologia e Innovaciones Tecnologicas (IVIT); ArgentinaFil: Parreño, Gladys Viviana. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Yuan, Lijuan. Virginia Polytechnic Institute and State University. Center for Emerging, Zoonotic, and Arthropod‑Borne Pathogens; Estados UnidosMDPI2023-09-14T10:24:23Z2023-09-14T10:24:23Z2023-08info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12123/15204https://www.mdpi.com/1999-4915/15/9/18641999-4915https://doi.org/10.3390/v15091864Viruses 15 (9) : 1864 (Agosto 2023)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by-nc-sa/4.0/Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)2025-09-29T13:46:05Zoai:localhost:20.500.12123/15204instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-09-29 13:46:05.901INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
dc.title.none.fl_str_mv Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigs
title Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigs
spellingShingle Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigs
Nyblade, Charlotte
Rotavirus
Gnotobiotic Animals
Swine
Salivary Glands
Immune Response
Animales Notobióticos
Cerdo
Glándulas Salivales
Respuesta Inmunológica
Human Rotavirus Infection
Infección por Rotavirus Humano
title_short Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigs
title_full Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigs
title_fullStr Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigs
title_full_unstemmed Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigs
title_sort Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigs
dc.creator.none.fl_str_mv Nyblade, Charlotte
Zhou, Peng
Frazier, Maggie
Frazier, Annie
Hensley, Casey
Fantasia-Davis, Ariana
Shahrudin, Shabihah
Hoffer, Miranda
Agbemabiese, Chantal Ama
LaRue, Lauren
Barro, Mario
Patton, John T.
Parreño, Gladys Viviana
Yuan, Lijuan
author Nyblade, Charlotte
author_facet Nyblade, Charlotte
Zhou, Peng
Frazier, Maggie
Frazier, Annie
Hensley, Casey
Fantasia-Davis, Ariana
Shahrudin, Shabihah
Hoffer, Miranda
Agbemabiese, Chantal Ama
LaRue, Lauren
Barro, Mario
Patton, John T.
Parreño, Gladys Viviana
Yuan, Lijuan
author_role author
author2 Zhou, Peng
Frazier, Maggie
Frazier, Annie
Hensley, Casey
Fantasia-Davis, Ariana
Shahrudin, Shabihah
Hoffer, Miranda
Agbemabiese, Chantal Ama
LaRue, Lauren
Barro, Mario
Patton, John T.
Parreño, Gladys Viviana
Yuan, Lijuan
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Rotavirus
Gnotobiotic Animals
Swine
Salivary Glands
Immune Response
Animales Notobióticos
Cerdo
Glándulas Salivales
Respuesta Inmunológica
Human Rotavirus Infection
Infección por Rotavirus Humano
topic Rotavirus
Gnotobiotic Animals
Swine
Salivary Glands
Immune Response
Animales Notobióticos
Cerdo
Glándulas Salivales
Respuesta Inmunológica
Human Rotavirus Infection
Infección por Rotavirus Humano
dc.description.none.fl_txt_mv Human rotavirus (HRV) is a leading cause of viral gastroenteritis in children across the globe. The virus has long been established as a pathogen of the gastrointestinal tract, targeting small intestine epithelial cells and leading to diarrhea, nausea, and vomiting. Recently, this classical infection pathway was challenged by the findings that murine strains of rotavirus can infect the salivary glands of pups and dams and transmit via saliva from pups to dams during suckling. Here, we aimed to determine if HRV was also capable of infecting salivary glands and spreading in saliva using a gnotobiotic (Gn) pig model of HRV infection and disease. Gn pigs were orally inoculated with various strains of HRV, and virus shedding was monitored for several days post-inoculation. HRV was shed nasally and in feces in all inoculated pigs. Infectious HRV was detected in the saliva of four piglets. Structural and non-structural HRV proteins, as well as the HRV genome, were detected in the intestinal and facial tissues of inoculated pigs. The pigs developed high IgM antibody responses in serum and small intestinal contents at 10 days post-inoculation. Additionally, inoculated pigs had HRV-specific IgM antibody-secreting cells present in the ileum, tonsils, and facial lymphoid tissues. Taken together, these findings indicate that HRV can replicate in salivary tissues and prime immune responses in both intestinal and facial lymphoid tissues of Gn pigs.
Instituto de Virología
Fil: Nyblade, Charlotte. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Zhou, Peng. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Frazier, Maggie. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Frazier, Annie. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Hensley, Casey. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Fantasia-Davis, Ariana. Virginia Polytechnic Institute and State University. Virginia-Maryland College of Veterinary Medicine. Department of Biomedical Sciences and Pathobiology; Estados Unidos
Fil: Shahrudin, Shabihah. Indiana University. Department of Biology; Estados Unidos
Fil: Hoffer, Miranda. Indiana University. Department of Biology; Estados Unidos
Fil: Agbemabiese, Chantal Ama. Indiana University. Department of Biology; Estados Unidos
Fil: LaRue, Lauren. GIVAX Inc.; Estados Unidos
Fil: Barro, Mario. GIVAX Inc.; Estados Unidos
Fil: Patton, John T. Indiana University. Department of Biology; Estados Unidos
Fil: Parreño, Gladys Viviana. Virginia Polytechnic Institute and State University. 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: Yuan, Lijuan. Virginia Polytechnic Institute and State University. Center for Emerging, Zoonotic, and Arthropod‑Borne Pathogens; Estados Unidos
description Human rotavirus (HRV) is a leading cause of viral gastroenteritis in children across the globe. The virus has long been established as a pathogen of the gastrointestinal tract, targeting small intestine epithelial cells and leading to diarrhea, nausea, and vomiting. Recently, this classical infection pathway was challenged by the findings that murine strains of rotavirus can infect the salivary glands of pups and dams and transmit via saliva from pups to dams during suckling. Here, we aimed to determine if HRV was also capable of infecting salivary glands and spreading in saliva using a gnotobiotic (Gn) pig model of HRV infection and disease. Gn pigs were orally inoculated with various strains of HRV, and virus shedding was monitored for several days post-inoculation. HRV was shed nasally and in feces in all inoculated pigs. Infectious HRV was detected in the saliva of four piglets. Structural and non-structural HRV proteins, as well as the HRV genome, were detected in the intestinal and facial tissues of inoculated pigs. The pigs developed high IgM antibody responses in serum and small intestinal contents at 10 days post-inoculation. Additionally, inoculated pigs had HRV-specific IgM antibody-secreting cells present in the ileum, tonsils, and facial lymphoid tissues. Taken together, these findings indicate that HRV can replicate in salivary tissues and prime immune responses in both intestinal and facial lymphoid tissues of Gn pigs.
publishDate 2023
dc.date.none.fl_str_mv 2023-09-14T10:24:23Z
2023-09-14T10:24:23Z
2023-08
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
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status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12123/15204
https://www.mdpi.com/1999-4915/15/9/1864
1999-4915
https://doi.org/10.3390/v15091864
url http://hdl.handle.net/20.500.12123/15204
https://www.mdpi.com/1999-4915/15/9/1864
https://doi.org/10.3390/v15091864
identifier_str_mv 1999-4915
dc.language.none.fl_str_mv eng
language eng
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
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Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv MDPI
publisher.none.fl_str_mv MDPI
dc.source.none.fl_str_mv Viruses 15 (9) : 1864 (Agosto 2023)
reponame:INTA Digital (INTA)
instname:Instituto Nacional de Tecnología Agropecuaria
reponame_str INTA Digital (INTA)
collection INTA Digital (INTA)
instname_str Instituto Nacional de Tecnología Agropecuaria
repository.name.fl_str_mv INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuaria
repository.mail.fl_str_mv tripaldi.nicolas@inta.gob.ar
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