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Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection

The crosstalk between the immune system and microbiota drives an amazingly complex mutualistic symbiosis. In mammals, the upper respiratory tract acts as a gateway for pathogen invasion, and the dynamic interaction between microbiota and mucosal immunity on its surface can effectively prevent diseas...

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Autores principales: Wu, Zheng-Ben, Meng, Kai-Feng, Ding, Li-Guo, Wu, Sha, Han, Guang-Kun, Zhai, Xue, Sun, Ru-Han, Yu, Yong-yao, Ji, Wei, Xu, Zhen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8601392/
https://www.ncbi.nlm.nih.gov/pubmed/34804060
http://dx.doi.org/10.3389/fimmu.2021.769775
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author Wu, Zheng-Ben
Meng, Kai-Feng
Ding, Li-Guo
Wu, Sha
Han, Guang-Kun
Zhai, Xue
Sun, Ru-Han
Yu, Yong-yao
Ji, Wei
Xu, Zhen
author_facet Wu, Zheng-Ben
Meng, Kai-Feng
Ding, Li-Guo
Wu, Sha
Han, Guang-Kun
Zhai, Xue
Sun, Ru-Han
Yu, Yong-yao
Ji, Wei
Xu, Zhen
author_sort Wu, Zheng-Ben
collection PubMed
description The crosstalk between the immune system and microbiota drives an amazingly complex mutualistic symbiosis. In mammals, the upper respiratory tract acts as a gateway for pathogen invasion, and the dynamic interaction between microbiota and mucosal immunity on its surface can effectively prevent disease development. However, the relationship between virus-mediated mucosal immune responses and microbes in lower vertebrates remains uncharacterized. In this study, we successfully constructed an infection model by intraperitoneally injecting common carp (Cyprinus carpio) with spring viremia of carp virus (SVCV). In addition to the detection of the SVCV in the nose and pharynx of common carp, we also identified obvious histopathological changes following viral infection. Moreover, numerous immune-related genes were significantly upregulated in the nose and pharynx at the peak of SVCV infection, after which the expression levels decreased to levels similar to those of the control group. Transcriptome sequencing results revealed that pathways associated with bacterial infection in the Toll-like receptor pathway and the Nod-like receptor pathway were activated in addition to the virus-related Rig-I-like receptor pathway after SVCV infection, suggesting that viral infection may be followed by opportunistic bacterial infection in these mucosal tissues. Using 16S rRNA gene sequencing, we further identified an upward trend in pathogenic bacteria on the mucosal surface of the nose and pharynx 4 days after SVCV infection, after which these tissues eventually reached new homeostasis. Taken together, our results suggest that the dynamic interaction between mucosal immunity and microbiota promotes the host to a new ecological state.
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spelling pubmed-86013922021-11-19 Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection Wu, Zheng-Ben Meng, Kai-Feng Ding, Li-Guo Wu, Sha Han, Guang-Kun Zhai, Xue Sun, Ru-Han Yu, Yong-yao Ji, Wei Xu, Zhen Front Immunol Immunology The crosstalk between the immune system and microbiota drives an amazingly complex mutualistic symbiosis. In mammals, the upper respiratory tract acts as a gateway for pathogen invasion, and the dynamic interaction between microbiota and mucosal immunity on its surface can effectively prevent disease development. However, the relationship between virus-mediated mucosal immune responses and microbes in lower vertebrates remains uncharacterized. In this study, we successfully constructed an infection model by intraperitoneally injecting common carp (Cyprinus carpio) with spring viremia of carp virus (SVCV). In addition to the detection of the SVCV in the nose and pharynx of common carp, we also identified obvious histopathological changes following viral infection. Moreover, numerous immune-related genes were significantly upregulated in the nose and pharynx at the peak of SVCV infection, after which the expression levels decreased to levels similar to those of the control group. Transcriptome sequencing results revealed that pathways associated with bacterial infection in the Toll-like receptor pathway and the Nod-like receptor pathway were activated in addition to the virus-related Rig-I-like receptor pathway after SVCV infection, suggesting that viral infection may be followed by opportunistic bacterial infection in these mucosal tissues. Using 16S rRNA gene sequencing, we further identified an upward trend in pathogenic bacteria on the mucosal surface of the nose and pharynx 4 days after SVCV infection, after which these tissues eventually reached new homeostasis. Taken together, our results suggest that the dynamic interaction between mucosal immunity and microbiota promotes the host to a new ecological state. Frontiers Media S.A. 2021-11-04 /pmc/articles/PMC8601392/ /pubmed/34804060 http://dx.doi.org/10.3389/fimmu.2021.769775 Text en Copyright © 2021 Wu, Meng, Ding, Wu, Han, Zhai, Sun, Yu, Ji and Xu https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Wu, Zheng-Ben
Meng, Kai-Feng
Ding, Li-Guo
Wu, Sha
Han, Guang-Kun
Zhai, Xue
Sun, Ru-Han
Yu, Yong-yao
Ji, Wei
Xu, Zhen
Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection
title Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection
title_full Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection
title_fullStr Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection
title_full_unstemmed Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection
title_short Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection
title_sort dynamic interaction between mucosal immunity and microbiota drives nose and pharynx homeostasis of common carp (cyprinus carpio) after svcv infection
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8601392/
https://www.ncbi.nlm.nih.gov/pubmed/34804060
http://dx.doi.org/10.3389/fimmu.2021.769775
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