Inflammatory conditions shape phenotypic and functional characteristics of lung-resident memory T cells in mice

Abstract Lung tissue-resident memory T cells (TRM) are critical for the local control of respiratory tract infections caused by influenza A viruses (IAV). Here we compare TRM populations induced by intranasal adenoviral vector vaccines encoding hemagglutinin and nucleoprotein (NP) with those induced...

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Main Authors: Anna Schmidt, Jana Fuchs, Mark Dedden, Katharina Kocher, Christine Schülein, Julian Hübner, Ana Vieira Antão, Pascal Irrgang, Friederike Oltmanns, Vera Viherlehto, Natascha Leicht, Ralf Joachim Rieker, Carol Geppert, Uwe Appelt, Sebastian Zundler, Kilian Schober, Dennis Lapuente, Matthias Tenbusch
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-58931-y
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author Anna Schmidt
Jana Fuchs
Mark Dedden
Katharina Kocher
Christine Schülein
Julian Hübner
Ana Vieira Antão
Pascal Irrgang
Friederike Oltmanns
Vera Viherlehto
Natascha Leicht
Ralf Joachim Rieker
Carol Geppert
Uwe Appelt
Sebastian Zundler
Kilian Schober
Dennis Lapuente
Matthias Tenbusch
author_facet Anna Schmidt
Jana Fuchs
Mark Dedden
Katharina Kocher
Christine Schülein
Julian Hübner
Ana Vieira Antão
Pascal Irrgang
Friederike Oltmanns
Vera Viherlehto
Natascha Leicht
Ralf Joachim Rieker
Carol Geppert
Uwe Appelt
Sebastian Zundler
Kilian Schober
Dennis Lapuente
Matthias Tenbusch
author_sort Anna Schmidt
collection DOAJ
description Abstract Lung tissue-resident memory T cells (TRM) are critical for the local control of respiratory tract infections caused by influenza A viruses (IAV). Here we compare TRM populations induced by intranasal adenoviral vector vaccines encoding hemagglutinin and nucleoprotein (NP) with those induced by an H1N1 infection in BALB/c mice. While vaccine-induced TRM express high levels of CD103 and persist longer in the lung parenchyma, short-lived, H1N1-induced TRM have a transcriptome associated with higher cytotoxic potential and distinct transcriptional profile as shown by single-cell RNA sequencing. In both the vaccine and H1N1 groups, NP-specific CD8+ T cells expand during heterologous influenza virus infection and protect the mice from disease. Meanwhile, lung inflammation in response to an infection with unrelated respiratory syncytial virus do not influence the fate of pre-existing TRM. Our preclinical work thus confirms that inflammatory conditions in the tissue shape the phenotypic and functional characteristics of TRM to serve relevant informations for optimizing mucosal vaccines.
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spelling doaj-art-e2c4e0b9519f4bb8b252b5a2d2d30fe02025-08-20T02:17:48ZengNature PortfolioNature Communications2041-17232025-04-0116111810.1038/s41467-025-58931-yInflammatory conditions shape phenotypic and functional characteristics of lung-resident memory T cells in miceAnna Schmidt0Jana Fuchs1Mark Dedden2Katharina Kocher3Christine Schülein4Julian Hübner5Ana Vieira Antão6Pascal Irrgang7Friederike Oltmanns8Vera Viherlehto9Natascha Leicht10Ralf Joachim Rieker11Carol Geppert12Uwe Appelt13Sebastian Zundler14Kilian Schober15Dennis Lapuente16Matthias Tenbusch17Friedrich-Alexander-Universität Erlangen-Nürnberg, University Hospital Erlangen, Institute of Clinical and Molecular VirologyFriedrich-Alexander-Universität Erlangen-Nürnberg, University Hospital Erlangen, Institute of Clinical and Molecular VirologyDepartment of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-Universität Erlangen-NürnbergMikrobiologisches Institut – Klinische Mikrobiologie, Immunologie und Hygiene, Universitätsklinikum Erlangen und Friedrich-Alexander-Universität Erlangen-NürnbergMikrobiologisches Institut – Klinische Mikrobiologie, Immunologie und Hygiene, Universitätsklinikum Erlangen und Friedrich-Alexander-Universität Erlangen-NürnbergFriedrich-Alexander-Universität Erlangen-Nürnberg, University Hospital Erlangen, Institute of Clinical and Molecular VirologyFriedrich-Alexander-Universität Erlangen-Nürnberg, University Hospital Erlangen, Institute of Clinical and Molecular VirologyFriedrich-Alexander-Universität Erlangen-Nürnberg, University Hospital Erlangen, Institute of Clinical and Molecular VirologyFriedrich-Alexander-Universität Erlangen-Nürnberg, University Hospital Erlangen, Institute of Clinical and Molecular VirologyFriedrich-Alexander-Universität Erlangen-Nürnberg, University Hospital Erlangen, Institute of Clinical and Molecular VirologyInstitute of Pathology, University Hospital Erlangen and Friedrich-Alexander-Universität Erlangen-NürnbergInstitute of Pathology, University Hospital Erlangen and Friedrich-Alexander-Universität Erlangen-NürnbergInstitute of Pathology, University Hospital Erlangen and Friedrich-Alexander-Universität Erlangen-NürnbergIZKF, Nikolaus-Fiebiger-Centre of Molecular Medicine, Friedrich-Alexander-Universität Erlangen-NürnbergDepartment of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-Universität Erlangen-NürnbergMikrobiologisches Institut – Klinische Mikrobiologie, Immunologie und Hygiene, Universitätsklinikum Erlangen und Friedrich-Alexander-Universität Erlangen-NürnbergFriedrich-Alexander-Universität Erlangen-Nürnberg, University Hospital Erlangen, Institute of Clinical and Molecular VirologyFriedrich-Alexander-Universität Erlangen-Nürnberg, University Hospital Erlangen, Institute of Clinical and Molecular VirologyAbstract Lung tissue-resident memory T cells (TRM) are critical for the local control of respiratory tract infections caused by influenza A viruses (IAV). Here we compare TRM populations induced by intranasal adenoviral vector vaccines encoding hemagglutinin and nucleoprotein (NP) with those induced by an H1N1 infection in BALB/c mice. While vaccine-induced TRM express high levels of CD103 and persist longer in the lung parenchyma, short-lived, H1N1-induced TRM have a transcriptome associated with higher cytotoxic potential and distinct transcriptional profile as shown by single-cell RNA sequencing. In both the vaccine and H1N1 groups, NP-specific CD8+ T cells expand during heterologous influenza virus infection and protect the mice from disease. Meanwhile, lung inflammation in response to an infection with unrelated respiratory syncytial virus do not influence the fate of pre-existing TRM. Our preclinical work thus confirms that inflammatory conditions in the tissue shape the phenotypic and functional characteristics of TRM to serve relevant informations for optimizing mucosal vaccines.https://doi.org/10.1038/s41467-025-58931-y
spellingShingle Anna Schmidt
Jana Fuchs
Mark Dedden
Katharina Kocher
Christine Schülein
Julian Hübner
Ana Vieira Antão
Pascal Irrgang
Friederike Oltmanns
Vera Viherlehto
Natascha Leicht
Ralf Joachim Rieker
Carol Geppert
Uwe Appelt
Sebastian Zundler
Kilian Schober
Dennis Lapuente
Matthias Tenbusch
Inflammatory conditions shape phenotypic and functional characteristics of lung-resident memory T cells in mice
Nature Communications
title Inflammatory conditions shape phenotypic and functional characteristics of lung-resident memory T cells in mice
title_full Inflammatory conditions shape phenotypic and functional characteristics of lung-resident memory T cells in mice
title_fullStr Inflammatory conditions shape phenotypic and functional characteristics of lung-resident memory T cells in mice
title_full_unstemmed Inflammatory conditions shape phenotypic and functional characteristics of lung-resident memory T cells in mice
title_short Inflammatory conditions shape phenotypic and functional characteristics of lung-resident memory T cells in mice
title_sort inflammatory conditions shape phenotypic and functional characteristics of lung resident memory t cells in mice
url https://doi.org/10.1038/s41467-025-58931-y
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