Single cell spatial analysis reveals inflammatory foci of immature neutrophil and CD8 T cells in COVID-19 lungs

Praveen Weeratunga, Laura Denney, Joshua A. Bull, Emmanouela Repapi, Martin Sergeant, Rachel Etherington, Chaitanya Vuppussetty, Gareth D. H. Turner, Colin Clelland, Jeongmin Woo, Amy Cross, Fadi Issa, Carlos Eduardo Andrea, Ignacio Melero Bermejo, David Sims, Simon McGowan, Yasemin-Xiomara Zurke, David J. Ahern, Eddie C. Gamez, Justin Whalley, Duncan Richards, Paul Klenerman, Claudia Monaco, Irina A. Udalova, Tao Dong, Agne Antanaviciute, Graham Ogg, Julian C. Knight, Helen M. Byrne, Stephen Taylor () and Ling-Pei Ho ()
Additional contact information
Praveen Weeratunga: MRC Translational Immunology Discovery Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Laura Denney: MRC Translational Immunology Discovery Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Joshua A. Bull: University of Oxford
Emmanouela Repapi: MRC WIMM Computational Biology Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Martin Sergeant: MRC WIMM Computational Biology Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Rachel Etherington: MRC Translational Immunology Discovery Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Chaitanya Vuppussetty: MRC Translational Immunology Discovery Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Gareth D. H. Turner: Oxford University Hospitals NHS Foundation Trust
Colin Clelland: Anatomic Pathology, Weill Cornell Medical College
Jeongmin Woo: MRC Translational Immunology Discovery Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Amy Cross: University of Oxford
Fadi Issa: University of Oxford
Carlos Eduardo Andrea: Navarra Institute for Health Research
Ignacio Melero Bermejo: Navarra Institute for Health Research
David Sims: MRC WIMM Computational Biology Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Simon McGowan: MRC WIMM Computational Biology Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Yasemin-Xiomara Zurke: Kennedy Institute for Rheumatology, University of Oxford
David J. Ahern: Kennedy Institute for Rheumatology, University of Oxford
Eddie C. Gamez: Wellcome Centre for Human Genetics, Nuffield Department of Medicine, University of Oxford
Justin Whalley: Wellcome Centre for Human Genetics, Nuffield Department of Medicine, University of Oxford
Duncan Richards: University of Oxford
Paul Klenerman: University of Oxford
Claudia Monaco: Kennedy Institute for Rheumatology, University of Oxford
Irina A. Udalova: Kennedy Institute for Rheumatology, University of Oxford
Tao Dong: MRC Translational Immunology Discovery Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Agne Antanaviciute: MRC Translational Immunology Discovery Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Graham Ogg: MRC Translational Immunology Discovery Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Julian C. Knight: Wellcome Centre for Human Genetics, Nuffield Department of Medicine, University of Oxford
Helen M. Byrne: University of Oxford
Stephen Taylor: MRC WIMM Computational Biology Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford
Ling-Pei Ho: MRC Translational Immunology Discovery Unit, MRC Weatherall Institute of Molecular Medicine, University of Oxford

Nature Communications, 2023, vol. 14, issue 1, 1-20

Abstract: Abstract Single cell spatial interrogation of the immune-structural interactions in COVID −19 lungs is challenging, mainly because of the marked cellular infiltrate and architecturally distorted microstructure. To address this, we develop a suite of mathematical tools to search for statistically significant co-locations amongst immune and structural cells identified using 37-plex imaging mass cytometry. This unbiased method reveals a cellular map interleaved with an inflammatory network of immature neutrophils, cytotoxic CD8 T cells, megakaryocytes and monocytes co-located with regenerating alveolar progenitors and endothelium. Of note, a highly active cluster of immature neutrophils and CD8 T cells, is found spatially linked with alveolar progenitor cells, and temporally with the diffuse alveolar damage stage. These findings offer further insights into how immune cells interact in the lungs of severe COVID-19 disease. We provide our pipeline [Spatial Omics Oxford Pipeline (SpOOx)] and visual-analytical tool, Multi-Dimensional Viewer (MDV) software, as a resource for spatial analysis.

Date: 2023
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DOI: 10.1038/s41467-023-42421-0

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