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

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 infectio...

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Main Authors: 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
Format: info:ar-repo/semantics/artículo
Language:Inglés
Published: MDPI 2023
Subjects:
Online Access:http://hdl.handle.net/20.500.12123/15204
https://www.mdpi.com/1999-4915/15/9/1864
https://doi.org/10.3390/v15091864
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author 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_browse Agbemabiese, Chantal Ama
Barro, Mario
Fantasia-Davis, Ariana
Frazier, Annie
Frazier, Maggie
Hensley, Casey
Hoffer, Miranda
LaRue, Lauren
Nyblade, Charlotte
Parreño, Gladys Viviana
Patton, John T.
Shahrudin, Shabihah
Yuan, Lijuan
Zhou, Peng
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_sort Nyblade, Charlotte
collection INTA Digital
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.
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institution Instituto Nacional de Tecnología Agropecuaria (INTA -Argentina)
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publishDateRange 2023
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spelling INTA152042023-09-14T10:31:03Z Human rotavirus replicates in salivary glands and primes immune responses in facial and intestinal lymphoid tissues of gnotobiotic pigs 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 Rotavirus Gnotobiotic Animals Swine Salivary Glands Immune Response Animales Notobióticos Cerdo Glándulas Salivales Respuesta Inmunológica Human Rotavirus Infection Infección por Rotavirus Humano 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 2023-09-14T10:24:23Z 2023-09-14T10:24:23Z 2023-08 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion 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 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 Viruses 15 (9) : 1864 (Agosto 2023)
spellingShingle Rotavirus
Gnotobiotic Animals
Swine
Salivary Glands
Immune Response
Animales Notobióticos
Cerdo
Glándulas Salivales
Respuesta Inmunológica
Human Rotavirus Infection
Infección por Rotavirus Humano
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
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
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_short 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
topic Rotavirus
Gnotobiotic Animals
Swine
Salivary Glands
Immune Response
Animales Notobióticos
Cerdo
Glándulas Salivales
Respuesta Inmunológica
Human Rotavirus Infection
Infección por Rotavirus Humano
url http://hdl.handle.net/20.500.12123/15204
https://www.mdpi.com/1999-4915/15/9/1864
https://doi.org/10.3390/v15091864
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