Peritoneal Cells Mediate Immune Responses and Cross-Protection Against Influenza A Virus

Intraperitoneal inoculation with live influenza A virus confers protection against intranasal infections in mice and ferrets. However, the responses of peritoneal cells to influenza A virus have not been investigated. Here we show that intraperitoneal inoculation with A/WSN/1933 (H1N1) virus induced...

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Main Authors: Avishekh Gautam, Byoung Kwon Park, Te Ha Kim, Madhav Akauliya, Dongbum Kim, Sony Maharjan, Joongwon Park, Jinsoo Kim, Hanseul Lee, Man-Seong Park, Younghee Lee, Hyung-Joo Kwon
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fimmu.2019.01160/full
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author Avishekh Gautam
Byoung Kwon Park
Te Ha Kim
Madhav Akauliya
Dongbum Kim
Sony Maharjan
Joongwon Park
Jinsoo Kim
Hanseul Lee
Man-Seong Park
Younghee Lee
Hyung-Joo Kwon
Hyung-Joo Kwon
author_facet Avishekh Gautam
Byoung Kwon Park
Te Ha Kim
Madhav Akauliya
Dongbum Kim
Sony Maharjan
Joongwon Park
Jinsoo Kim
Hanseul Lee
Man-Seong Park
Younghee Lee
Hyung-Joo Kwon
Hyung-Joo Kwon
author_sort Avishekh Gautam
collection DOAJ
description Intraperitoneal inoculation with live influenza A virus confers protection against intranasal infections in mice and ferrets. However, the responses of peritoneal cells to influenza A virus have not been investigated. Here we show that intraperitoneal inoculation with A/WSN/1933 (H1N1) virus induced virus-reactive IgG production in the peritoneal cavity in mice. The infection resulted in substantial but transient B cell and macrophage depletion along with massive neutrophil infiltration, but virus growth was not detected. Influenza A viruses bound to α-2,6-linked sialic acids of B cells and macrophages and induced apoptotic death of peritoneal cavity cells. However, re-infection with A/WSN/1933 virus did not have adverse effects on immune cells most likely because of the neutralizing antibodies produced in response to the first exposure. Infection of BALB/c mice with A/WSN/1933 induced cross-protection against an otherwise lethal intraperitoneal dose of A/Hongkong/4801/2014 (H3N2) virus. This information suggests that immunological responses in the peritoneal cavity can induce effective defense against future virus infection. Considering the unexpected potent immunoregulatory activity of the peritoneal cells against influenza viruses, we suggest that comparative studies on various immune reactions after infection through different routes may contribute to better selection of vaccination routes in development of efficacious influenza vaccines.
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spelling doaj.art-b80efe3fb8004d6bacb09b8763ac63412022-12-21T18:51:24ZengFrontiers Media S.A.Frontiers in Immunology1664-32242019-05-011010.3389/fimmu.2019.01160435976Peritoneal Cells Mediate Immune Responses and Cross-Protection Against Influenza A VirusAvishekh Gautam0Byoung Kwon Park1Te Ha Kim2Madhav Akauliya3Dongbum Kim4Sony Maharjan5Joongwon Park6Jinsoo Kim7Hanseul Lee8Man-Seong Park9Younghee Lee10Hyung-Joo Kwon11Hyung-Joo Kwon12Department of Microbiology, College of Medicine, Hallym University, Chuncheon, South KoreaCenter for Medical Science Research, College of Medicine, Hallym University, Chuncheon, South KoreaDepartment of Microbiology, College of Medicine, Hallym University, Chuncheon, South KoreaDepartment of Microbiology, College of Medicine, Hallym University, Chuncheon, South KoreaCenter for Medical Science Research, College of Medicine, Hallym University, Chuncheon, South KoreaCenter for Medical Science Research, College of Medicine, Hallym University, Chuncheon, South KoreaDepartment of Microbiology, College of Medicine, Hallym University, Chuncheon, South KoreaDepartment of Microbiology, College of Medicine, Hallym University, Chuncheon, South KoreaDepartment of Microbiology, College of Medicine, Hallym University, Chuncheon, South KoreaDepartment of Microbiology, College of Medicine, and the Institute for Viral Diseases, Korea University, Seoul, South KoreaDepartment of Biochemistry, College of Natural Sciences, Chungbuk National University, Cheongju, South KoreaDepartment of Microbiology, College of Medicine, Hallym University, Chuncheon, South KoreaCenter for Medical Science Research, College of Medicine, Hallym University, Chuncheon, South KoreaIntraperitoneal inoculation with live influenza A virus confers protection against intranasal infections in mice and ferrets. However, the responses of peritoneal cells to influenza A virus have not been investigated. Here we show that intraperitoneal inoculation with A/WSN/1933 (H1N1) virus induced virus-reactive IgG production in the peritoneal cavity in mice. The infection resulted in substantial but transient B cell and macrophage depletion along with massive neutrophil infiltration, but virus growth was not detected. Influenza A viruses bound to α-2,6-linked sialic acids of B cells and macrophages and induced apoptotic death of peritoneal cavity cells. However, re-infection with A/WSN/1933 virus did not have adverse effects on immune cells most likely because of the neutralizing antibodies produced in response to the first exposure. Infection of BALB/c mice with A/WSN/1933 induced cross-protection against an otherwise lethal intraperitoneal dose of A/Hongkong/4801/2014 (H3N2) virus. This information suggests that immunological responses in the peritoneal cavity can induce effective defense against future virus infection. Considering the unexpected potent immunoregulatory activity of the peritoneal cells against influenza viruses, we suggest that comparative studies on various immune reactions after infection through different routes may contribute to better selection of vaccination routes in development of efficacious influenza vaccines.https://www.frontiersin.org/article/10.3389/fimmu.2019.01160/fullapoptosiscross protectioninfluenza A virusneutralizing antibodyperitoneal cells
spellingShingle Avishekh Gautam
Byoung Kwon Park
Te Ha Kim
Madhav Akauliya
Dongbum Kim
Sony Maharjan
Joongwon Park
Jinsoo Kim
Hanseul Lee
Man-Seong Park
Younghee Lee
Hyung-Joo Kwon
Hyung-Joo Kwon
Peritoneal Cells Mediate Immune Responses and Cross-Protection Against Influenza A Virus
Frontiers in Immunology
apoptosis
cross protection
influenza A virus
neutralizing antibody
peritoneal cells
title Peritoneal Cells Mediate Immune Responses and Cross-Protection Against Influenza A Virus
title_full Peritoneal Cells Mediate Immune Responses and Cross-Protection Against Influenza A Virus
title_fullStr Peritoneal Cells Mediate Immune Responses and Cross-Protection Against Influenza A Virus
title_full_unstemmed Peritoneal Cells Mediate Immune Responses and Cross-Protection Against Influenza A Virus
title_short Peritoneal Cells Mediate Immune Responses and Cross-Protection Against Influenza A Virus
title_sort peritoneal cells mediate immune responses and cross protection against influenza a virus
topic apoptosis
cross protection
influenza A virus
neutralizing antibody
peritoneal cells
url https://www.frontiersin.org/article/10.3389/fimmu.2019.01160/full
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