Single-cell analysis reveals lasting immunological consequences of influenza infection and respiratory immunization in the pig lung.

The pig is a natural host for influenza viruses and integrally involved in virus evolution through interspecies transmissions between humans and swine. Swine have many physiological, anatomical, and immunological similarities to humans, and are an excellent model for human influenza. Here, we employ...

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Main Authors: Andrew Muir, Basudev Paudyal, Selma Schmidt, Ehsan Sedaghat-Rostami, Soumendu Chakravarti, Sonia Villanueva-Hernández, Katy Moffat, Noemi Polo, Nicos Angelopoulos, Anna Schmidt, Matthias Tenbusch, Graham Freimanis, Wilhelm Gerner, Arianne C Richard, Elma Tchilian
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-07-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1011910
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author Andrew Muir
Basudev Paudyal
Selma Schmidt
Ehsan Sedaghat-Rostami
Soumendu Chakravarti
Sonia Villanueva-Hernández
Katy Moffat
Noemi Polo
Nicos Angelopoulos
Anna Schmidt
Matthias Tenbusch
Graham Freimanis
Wilhelm Gerner
Arianne C Richard
Elma Tchilian
author_facet Andrew Muir
Basudev Paudyal
Selma Schmidt
Ehsan Sedaghat-Rostami
Soumendu Chakravarti
Sonia Villanueva-Hernández
Katy Moffat
Noemi Polo
Nicos Angelopoulos
Anna Schmidt
Matthias Tenbusch
Graham Freimanis
Wilhelm Gerner
Arianne C Richard
Elma Tchilian
author_sort Andrew Muir
collection DOAJ
description The pig is a natural host for influenza viruses and integrally involved in virus evolution through interspecies transmissions between humans and swine. Swine have many physiological, anatomical, and immunological similarities to humans, and are an excellent model for human influenza. Here, we employed single cell RNA-sequencing (scRNA-seq) and flow cytometry to characterize the major leukocyte subsets in bronchoalveolar lavage (BAL), twenty-one days after H1N1pdm09 infection or respiratory immunization with an adenoviral vector vaccine expressing hemagglutinin and nucleoprotein with or without IL-1β. Mapping scRNA-seq clusters from BAL onto those previously described in peripheral blood facilitated annotation and highlighted differences between tissue resident and circulating immune cells. ScRNA-seq data and functional assays revealed lasting impacts of immune challenge on BAL populations. First, mucosal administration of IL-1β reduced the number of functionally active Treg cells. Second, influenza infection upregulated IFI6 in BAL cells and decreased their susceptibility to virus replication in vitro. Our data provide a reference map of porcine BAL cells and reveal lasting immunological consequences of influenza infection and respiratory immunization in a highly relevant large animal model for respiratory virus infection.
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institution Kabale University
issn 1553-7366
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language English
publishDate 2024-07-01
publisher Public Library of Science (PLoS)
record_format Article
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spelling doaj-art-bc240ee05da74cccb8d07006bf4911f82025-08-20T03:25:46ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742024-07-01207e101191010.1371/journal.ppat.1011910Single-cell analysis reveals lasting immunological consequences of influenza infection and respiratory immunization in the pig lung.Andrew MuirBasudev PaudyalSelma SchmidtEhsan Sedaghat-RostamiSoumendu ChakravartiSonia Villanueva-HernándezKaty MoffatNoemi PoloNicos AngelopoulosAnna SchmidtMatthias TenbuschGraham FreimanisWilhelm GernerArianne C RichardElma TchilianThe pig is a natural host for influenza viruses and integrally involved in virus evolution through interspecies transmissions between humans and swine. Swine have many physiological, anatomical, and immunological similarities to humans, and are an excellent model for human influenza. Here, we employed single cell RNA-sequencing (scRNA-seq) and flow cytometry to characterize the major leukocyte subsets in bronchoalveolar lavage (BAL), twenty-one days after H1N1pdm09 infection or respiratory immunization with an adenoviral vector vaccine expressing hemagglutinin and nucleoprotein with or without IL-1β. Mapping scRNA-seq clusters from BAL onto those previously described in peripheral blood facilitated annotation and highlighted differences between tissue resident and circulating immune cells. ScRNA-seq data and functional assays revealed lasting impacts of immune challenge on BAL populations. First, mucosal administration of IL-1β reduced the number of functionally active Treg cells. Second, influenza infection upregulated IFI6 in BAL cells and decreased their susceptibility to virus replication in vitro. Our data provide a reference map of porcine BAL cells and reveal lasting immunological consequences of influenza infection and respiratory immunization in a highly relevant large animal model for respiratory virus infection.https://doi.org/10.1371/journal.ppat.1011910
spellingShingle Andrew Muir
Basudev Paudyal
Selma Schmidt
Ehsan Sedaghat-Rostami
Soumendu Chakravarti
Sonia Villanueva-Hernández
Katy Moffat
Noemi Polo
Nicos Angelopoulos
Anna Schmidt
Matthias Tenbusch
Graham Freimanis
Wilhelm Gerner
Arianne C Richard
Elma Tchilian
Single-cell analysis reveals lasting immunological consequences of influenza infection and respiratory immunization in the pig lung.
PLoS Pathogens
title Single-cell analysis reveals lasting immunological consequences of influenza infection and respiratory immunization in the pig lung.
title_full Single-cell analysis reveals lasting immunological consequences of influenza infection and respiratory immunization in the pig lung.
title_fullStr Single-cell analysis reveals lasting immunological consequences of influenza infection and respiratory immunization in the pig lung.
title_full_unstemmed Single-cell analysis reveals lasting immunological consequences of influenza infection and respiratory immunization in the pig lung.
title_short Single-cell analysis reveals lasting immunological consequences of influenza infection and respiratory immunization in the pig lung.
title_sort single cell analysis reveals lasting immunological consequences of influenza infection and respiratory immunization in the pig lung
url https://doi.org/10.1371/journal.ppat.1011910
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