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Temporal omics analysis in Syrian hamsters unravel cellular effector responses to moderate COVID-19

Author

Listed:
  • Geraldine Nouailles

    (Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Division of Pulmonary Inflammation
    Berlin Institute of Health (BIH))

  • Emanuel Wyler

    (Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC))

  • Peter Pennitz

    (Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Division of Pulmonary Inflammation)

  • Dylan Postmus

    (Berlin Institute of Health (BIH)
    Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Virology)

  • Daria Vladimirova

    (Freie Universität Berlin)

  • Julia Kazmierski

    (Berlin Institute of Health (BIH)
    Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Virology)

  • Fabian Pott

    (Berlin Institute of Health (BIH)
    Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Virology)

  • Kristina Dietert

    (Freie Universität Berlin
    Freie Universität Berlin)

  • Michael Muelleder

    (Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Core Facility – High-Throughput Mass Spectrometry)

  • Vadim Farztdinov

    (Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Core Facility – High-Throughput Mass Spectrometry)

  • Benedikt Obermayer

    (Berlin Institute of Health at Charité – Universitätsmedizin Berlin, Core Unit Bioinformatics)

  • Sandra-Maria Wienhold

    (Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Division of Pulmonary Inflammation)

  • Sandro Andreotti

    (Freie Universität Berlin)

  • Thomas Hoefler

    (Freie Universität Berlin)

  • Birgit Sawitzki

    (Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Immunology)

  • Christian Drosten

    (Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Virology)

  • Leif E. Sander

    (Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Infectious Diseases and Respiratory Medicine)

  • Norbert Suttorp

    (Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Infectious Diseases and Respiratory Medicine)

  • Markus Ralser

    (The Francis Crick Institute, Molecular Biology of Metabolism Laboratory
    Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Biochemistry)

  • Dieter Beule

    (Berlin Institute of Health at Charité – Universitätsmedizin Berlin, Core Unit Bioinformatics)

  • Achim D. Gruber

    (Freie Universität Berlin)

  • Christine Goffinet

    (Berlin Institute of Health (BIH)
    Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Virology)

  • Markus Landthaler

    (Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC)
    IRI Life Sciences, Institute for Biology, Humboldt-Universität zu Berlin)

  • Jakob Trimpert

    (Freie Universität Berlin)

  • Martin Witzenrath

    (Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Division of Pulmonary Inflammation
    Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Infectious Diseases and Respiratory Medicine
    German Center for Lung Research (DZL))

Abstract

In COVID-19, immune responses are key in determining disease severity. However, cellular mechanisms at the onset of inflammatory lung injury in SARS-CoV-2 infection, particularly involving endothelial cells, remain ill-defined. Using Syrian hamsters as a model for moderate COVID-19, we conduct a detailed longitudinal analysis of systemic and pulmonary cellular responses, and corroborate it with datasets from COVID-19 patients. Monocyte-derived macrophages in lungs exert the earliest and strongest transcriptional response to infection, including induction of pro-inflammatory genes, while epithelial cells show weak alterations. Without evidence for productive infection, endothelial cells react, depending on cell subtypes, by strong and early expression of anti-viral, pro-inflammatory, and T cell recruiting genes. Recruitment of cytotoxic T cells as well as emergence of IgM antibodies precede viral clearance at day 5 post infection. Investigating SARS-CoV-2 infected Syrian hamsters thus identifies cell type-specific effector functions, providing detailed insights into pathomechanisms of COVID-19 and informing therapeutic strategies.

Suggested Citation

  • Geraldine Nouailles & Emanuel Wyler & Peter Pennitz & Dylan Postmus & Daria Vladimirova & Julia Kazmierski & Fabian Pott & Kristina Dietert & Michael Muelleder & Vadim Farztdinov & Benedikt Obermayer , 2021. "Temporal omics analysis in Syrian hamsters unravel cellular effector responses to moderate COVID-19," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-25030-7
    DOI: 10.1038/s41467-021-25030-7
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    Cited by:

    1. Sara Sunshine & Andreas S. Puschnik & Joseph M. Replogle & Matthew T. Laurie & Jamin Liu & Beth Shoshana Zha & James K. Nuñez & Janie R. Byrum & Aidan H. McMorrow & Matthew B. Frieman & Juliane Winkle, 2023. "Systematic functional interrogation of SARS-CoV-2 host factors using Perturb-seq," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Wei Qiao & Hui En Lau & Huizhi Xie & Vincent Kwok-Man Poon & Chris Chung-Sing Chan & Hin Chu & Shuofeng Yuan & Terrence Tsz-Tai Yuen & Kenn Ka-Heng Chik & Jessica Oi-Ling Tsang & Chris Chun-Yiu Chan &, 2022. "SARS-CoV-2 infection induces inflammatory bone loss in golden Syrian hamsters," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Laura Heydemann & Małgorzata Ciurkiewicz & Georg Beythien & Kathrin Becker & Klaus Schughart & Stephanie Stanelle-Bertram & Berfin Schaumburg & Nancy Mounogou-Kouassi & Sebastian Beck & Martin Zickler, 2023. "Hamster model for post-COVID-19 alveolar regeneration offers an opportunity to understand post-acute sequelae of SARS-CoV-2," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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