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Alveolar macrophage-expressed Plet1 is a driver of lung epithelial repair after viral pneumonia

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  • Learta Pervizaj-Oruqaj

    (University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL)
    Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI))

  • Balachandar Selvakumar

    (University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL)
    Max Planck Institute for Heart and Lung Research
    Instituto de Investigación en Biomedicina de Buenos Aires (IBioBA))

  • Maximiliano Ruben Ferrero

    (University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL)
    Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI)
    Max Planck Institute for Heart and Lung Research)

  • Monika Heiner

    (University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL)
    Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI))

  • Christina Malainou

    (University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL)
    Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI))

  • Rolf David Glaser

    (Justus Liebig University
    Justus Liebig University)

  • Jochen Wilhelm

    (Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI)
    University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL))

  • Marek Bartkuhn

    (Justus Liebig University
    Justus Liebig University)

  • Astrid Weiss

    (Excellence Cluster Cardio-Pulmonary Institute (CPI)
    University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL))

  • Ioannis Alexopoulos

    (University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL)
    Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI))

  • Biruta Witte

    (University Hospital of Giessen)

  • Stefan Gattenlöhner

    (University Hospital of Giessen)

  • István Vadász

    (Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI)
    University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL))

  • Rory Edward Morty

    (University Hospital Heidelberg, Member of the German Center for Lung Research (DZL))

  • Werner Seeger

    (Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI)
    Max Planck Institute for Heart and Lung Research
    Instituto de Investigación en Biomedicina de Buenos Aires (IBioBA))

  • Ralph Theo Schermuly

    (Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI)
    University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL))

  • Ana Ivonne Vazquez-Armendariz

    (University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL)
    Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI)
    University of Bonn, Transdisciplinary Research Area Life and Health, Organoid Biology, Life & Medical Sciences Institute)

  • Susanne Herold

    (University Hospital Giessen, Justus Liebig University, Member of the German Center for Lung Research (DZL)
    Justus Liebig University
    Excellence Cluster Cardio-Pulmonary Institute (CPI))

Abstract

Influenza A virus (IAV) infection mobilizes bone marrow-derived macrophages (BMDM) that gradually undergo transition to tissue-resident alveolar macrophages (TR-AM) in the inflamed lung. Combining high-dimensional single-cell transcriptomics with complex lung organoid modeling, in vivo adoptive cell transfer, and BMDM-specific gene targeting, we found that transitioning (“regenerative”) BMDM and TR-AM highly express Placenta-expressed transcript 1 (Plet1). We reveal that Plet1 is released from alveolar macrophages, and acts as important mediator of macrophage-epithelial cross-talk during lung repair by inducing proliferation of alveolar epithelial cells and re-sealing of the epithelial barrier. Intratracheal administration of recombinant Plet1 early in the disease course attenuated viral lung injury and rescued mice from otherwise fatal disease, highlighting its therapeutic potential.

Suggested Citation

  • Learta Pervizaj-Oruqaj & Balachandar Selvakumar & Maximiliano Ruben Ferrero & Monika Heiner & Christina Malainou & Rolf David Glaser & Jochen Wilhelm & Marek Bartkuhn & Astrid Weiss & Ioannis Alexopou, 2024. "Alveolar macrophage-expressed Plet1 is a driver of lung epithelial repair after viral pneumonia," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44421-6
    DOI: 10.1038/s41467-023-44421-6
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    1. Rogan A. Grant & Luisa Morales-Nebreda & Nikolay S. Markov & Suchitra Swaminathan & Melissa Querrey & Estefany R. Guzman & Darryl A. Abbott & Helen K. Donnelly & Alvaro Donayre & Isaac A. Goldberg & Z, 2021. "Circuits between infected macrophages and T cells in SARS-CoV-2 pneumonia," Nature, Nature, vol. 590(7847), pages 635-641, February.
    2. Astrid Weiss & Moritz Christian Neubauer & Dinesh Yerabolu & Baktybek Kojonazarov & Beate Christiane Schlueter & Lavinia Neubert & Danny Jonigk & Nelli Baal & Clemens Ruppert & Peter Dorfmuller & Soni, 2019. "Targeting cyclin-dependent kinases for the treatment of pulmonary arterial hypertension," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    3. Rania Dagher & Alan M. Copenhaver & Valerie Besnard & Aaron Berlin & Fatima Hamidi & Marielle Maret & Jingya Wang & Xiaotao Qu & Yashaswi Shrestha & Jincheng Wu & Gregory Gautier & Rajiv Raja & Michel, 2020. "IL-33-ST2 axis regulates myeloid cell differentiation and activation enabling effective club cell regeneration," Nature Communications, Nature, vol. 11(1), pages 1-19, December.
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