Single-cell-resolved interspecies comparison shows a shared inflammatory axis and a dominant neutrophil-endothelial program in severe COVID-19

Stefan Peidli; Geraldine Nouailles; Emanuel Wyler; Julia M. Adler; Sandra Kunder; Anne Voß; Julia Kazmierski; Fabian Pott; Peter Pennitz; Dylan Postmus; Luiz Gustavo Teixeira Alves; Christine Goffinet; Achim D. Gruber; Nils Blüthgen; Martin Witzenrath; Jakob Trimpert; Markus Landthaler; Samantha D. Praktiknjo

Cell Reports (Jun 2024)

Single-cell-resolved interspecies comparison shows a shared inflammatory axis and a dominant neutrophil-endothelial program in severe COVID-19

Stefan Peidli,
Geraldine Nouailles,
Emanuel Wyler,
Julia M. Adler,
Sandra Kunder,
Anne Voß,
Julia Kazmierski,
Fabian Pott,
Peter Pennitz,
Dylan Postmus,
Luiz Gustavo Teixeira Alves,
Christine Goffinet,
Achim D. Gruber,
Nils Blüthgen,
Martin Witzenrath,
Jakob Trimpert,
Markus Landthaler,
Samantha D. Praktiknjo

Affiliations

Stefan Peidli: Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Pathology, Berlin, Germany; Institute for Biology, Humboldt-Universität zu Berlin, Berlin, Germany
Geraldine Nouailles: Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Infectious Diseases, Respiratory Medicine and Critical Care, Berlin, Germany
Emanuel Wyler: Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany
Julia M. Adler: Institut für Virologie, Freie Universität Berlin, Berlin, Germany
Sandra Kunder: Institute of Veterinary Pathology, Freie Universität Berlin, Berlin, Germany
Anne Voß: Institute of Veterinary Pathology, Freie Universität Berlin, Berlin, Germany
Julia Kazmierski: Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Virology, Berlin, Germany; Berlin Institute of Health at Charité – Universitätsmedizin Berlin, Berlin, Germany
Fabian Pott: Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Virology, Berlin, Germany; Berlin Institute of Health at Charité – Universitätsmedizin Berlin, Berlin, Germany
Peter Pennitz: Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Infectious Diseases, Respiratory Medicine and Critical Care, Berlin, Germany
Dylan Postmus: Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Virology, Berlin, Germany; Berlin Institute of Health at Charité – Universitätsmedizin Berlin, Berlin, Germany
Luiz Gustavo Teixeira Alves: Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany
Christine Goffinet: Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Virology, Berlin, Germany; Berlin Institute of Health at Charité – Universitätsmedizin Berlin, Berlin, Germany
Achim D. Gruber: Institute of Veterinary Pathology, Freie Universität Berlin, Berlin, Germany
Nils Blüthgen: Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Pathology, Berlin, Germany; Institute for Biology, Humboldt-Universität zu Berlin, Berlin, Germany
Martin Witzenrath: Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Infectious Diseases, Respiratory Medicine and Critical Care, Berlin, Germany; German Center for Lung Research (DZL), Berlin, Germany
Jakob Trimpert: Institut für Virologie, Freie Universität Berlin, Berlin, Germany; Department of Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS, USA
Markus Landthaler: Institute for Biology, Humboldt-Universität zu Berlin, Berlin, Germany; Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany
Samantha D. Praktiknjo: Berlin Institute of Health at Charité – Universitätsmedizin Berlin, Berlin, Germany; Corresponding author

Journal volume & issue: Vol. 43, no. 6
p. 114328

Abstract

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Summary: A key issue for research on COVID-19 pathogenesis is the lack of biopsies from patients and of samples at the onset of infection. To overcome these hurdles, hamsters were shown to be useful models for studying this disease. Here, we further leverage the model to molecularly survey the disease progression from time-resolved single-cell RNA sequencing data collected from healthy and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-infected Syrian and Roborovski hamster lungs. We compare our data to human COVID-19 studies, including bronchoalveolar lavage, nasal swab, and postmortem lung tissue, and identify a shared axis of inflammation dominated by macrophages, neutrophils, and endothelial cells, which we show to be transient in Syrian and terminal in Roborovski hamsters. Our data suggest that, following SARS-CoV-2 infection, commitment to a type 1- or type 3-biased immunity determines moderate versus severe COVID-19 outcomes, respectively.

Published in Cell Reports

ISSN: 2211-1247 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Science: Biology (General)
Website: http://www.cell.com/cell-reports/home

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