Severe COVID-19 Is Marked by a Dysregulated Myeloid Cell Compartment
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Abstract
Coronavirus disease 2019 (COVID-19) is a mild to moderate respiratory tract infection, however, a subset of patients progress to severe disease and respiratory failure. The mechanism of protective immunity in mild forms and the pathogenesis of severe COVID-19 associated with increased neutrophil counts and dysregulated immune responses remain unclear. In a dual-center, two-cohort study, we combined single-cell RNA-sequencing and single-cell proteomics of whole-blood and peripheral-blood mononuclear cells to determine changes in immune cell composition and activation in mild versus severe COVID-19 (242 samples from 109 individuals) over time. HLA-DR hi CD11c hi inflammatory monocytes with an interferon-stimulated gene signature were elevated in mild COVID-19. Severe COVID-19 was marked by occurrence of neutrophil precursors, as evidence of emergency myelopoiesis, dysfunctional mature neutrophils, and HLA-DR lo monocytes. Our study provides detailed insights into the systemic immune response to SARS-CoV-2 infection and reveals profound alterations in the myeloid cell compartment associated with severe COVID-19.
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An early transient wave of ISG expression in cells of the innate immune system, particularly monocytes, was determined by scRNA-seq.
“An early transient wave of ISG expression in cells of the innate immune system, particularly monocytes, was also determined by scRNA-seq (Schulte-Schrepping et al., 2020).”
From COVID-19 and the human innate immune system (2021) · cites this paper as Schulte-Schrepping et al., 2020
Mild COVID-19 features circulating HLA-DRhi CD11chi inflammatory monocytes with an interferon-stimulated gene signature, while severe cases show neutrophil precursors and dysfunctional PD-L1-expressing mature neutrophils.
“Mild COVID-19 patients were marked by circulating HLA-DR hi CD11c hi inflammatory monocytes with an interferon-stimulated gene signature”
From COVID-19 and the human innate immune system (2021) · cites this paper as Schulte-Schrepping et al., 2020
Single-cell transcriptomics of circulating innate immune cells supports a general IFN response in all COVID-19 patients with a strong temporal component.
“Single-cell transcriptomics of circulating innate immune cells strongly support a general IFN response in all COVID-19 patients with a strong temporal component”
From COVID-19 and the human innate immune system (2021) · cites this paper as Schulte-Schrepping et al., 2020
Peripheral blood from mild COVID-19 patients contained more classical monocytes with an early and transient type I interferon signature.
“Peripheral blood of mild COVID-19 patients contained more classical monocytes (CD14+CD16−) exhibiting an early and transient type I IFN signature109,110.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [110]
HLA-DR expression on monocytes from severe COVID-19 patients is lower than on monocytes from mild patients.
“HLA-DR expression on monocytes from severe COVID-19 patients is also reduced relative to those from mild patients109,110,112,122.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [110]
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Complement activation induces excessive T cell cytotoxicity in severe COVID-19
Georg, P., Astaburuaga-García, R., Bonaguro, L., Brumhard, S., Michalick, L., Lippert, L. J., Kostevc, T., Gäbel, C., Schneider, M., Streitz, M., et al. (2022) · Cell · doi:10.1016/j.cell.2021.12.040 · Cited by 218 · see citing works
Self-citationA time-resolved proteomic and prognostic map of COVID-19
Demichev, V., Tober-Lau, P., Lemke, O., Nazarenko, T., Thibeault, C., Whitwell, H., Röhl, A., Freiwald, A., Szyrwiel, L., Ludwig, D., et al. (2021) · Cell Systems · doi:10.1016/j.cels.2021.05.005 · Cited by 200 · see citing works
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Li, X., Zhang, Z., Wang, Z., Gutiérrez-Castrellón, P., & Shi, H. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01043-6 · Cited by 67 · see citing works
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Cui, A., Li, B., Wallace, M. S., Gonye, A. L. K., Oetheimer, C., Patel, H., Tonnerre, P., Holmes, J. A., Lieb, D., Yao, B. S., et al. (2024) · Journal of Hepatology · doi:10.1016/j.jhep.2023.02.040 · Cited by 46 · see citing works
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- Authors
- Schulte-Schrepping, J., Reusch, N., Paclik, D., Baßler, K., Schlickeiser, S., Zhang, B., Krämer, B., Krammer, T., Brumhard, S., Bonaguro, L., De Domenico, E., Wendisch, D., Grasshoff, M., Kapellos, T. S., Beckstette, M., Pecht, T., Saglam, A., Dietrich, O., Mei, H. E., Schulz, A. R., Conrad, C., Kunkel, D., Vafadarnejad, E., Xu, C.-J., Horne, A., Herbert, M., Drews, A., Thibeault, C., Pfeiffer, M., Hippenstiel, S., Hocke, A., Müller-Redetzky, H., Heim, K.-M., Machleidt, F., Uhrig, A., Bosquillon de Jarcy, L., Jürgens, L., Stegemann, M., Glösenkamp, C. R., Volk, H.-D., Goffinet, C., Landthaler, M., Wyler, E., Georg, P., Schneider, M., Dang-Heine, C., Neuwinger, N., Kappert, K., Tauber, R., Corman, V., Raabe, J., Kaiser, K. M., Vinh, M. T., Rieke, G., Meisel, C., Ulas, T., Becker, M., Geffers, R., Witzenrath, M., Drosten, C., Suttorp, N., von Kalle, C., Kurth, F., Händler, K., Schultze, J. L., Aschenbrenner, A. C., Li, Y., Nattermann, J., Sawitzki, B., Saliba, A.-E., Sander, L. E., Angelov, A., Bals, R., Bartholomäus, A., Becker, A., Bezdan, D., Bonifacio, E., Bork, P., Clavel, T., Colome-Tatche, M., Diefenbach, A., Dilthey, A., Fischer, N., Förstner, K., Frick, J.-S., Gagneur, J., Goesmann, A., Hain, T., Hummel, M., Janssen, S., Kalinowski, J., Kallies, R., Kehr, B., Keller, A., Kim-Hellmuth, S., Klein, C., Kohlbacher, O., Korbel, J. O., Kurth, I., Landthaler, M., Li, Y., Ludwig, K., Makarewicz, O., Marz, M., McHardy, A., Mertes, C., Nöthen, M., Nürnberg, P., Ohler, U., Ossowski, S., Overmann, J., Peter, S., Pfeffer, K., Poetsch, A. R., Pühler, A., Rajewsky, N., Ralser, M., Rieß, O., Ripke, S., Nunes da Rocha, U., Rosenstiel, P., Saliba, A.-E., Sander, L. E., Sawitzki, B., Schiffer, P., Schulte, E.-C., Schultze, J. L., Sczyrba, A., Stegle, O., Stoye, J., Theis, F., Vehreschild, J., Vogel, J., von Kleist, M., Walker, A., Walter, J., Wieczorek, D., & Ziebuhr, J.
- Affiliations
- University of Bonn (DE)
- Charité – Universitätsmedizin Berlin (DE)
- Berlin Institute of Health at Charité - Universitätsmedizin Berlin (DE)
- Medizinische Hochschule Hannover (DE)
- University Hospital Bonn (DE)
- Helmholtz Institute for RNA-based Infection Research (DE)
- German Rheumatism Research Centre (DE)
- Radboud University Nijmegen (NL)
- German Center for Lung Research (DE)
- Max Delbrück Center (DE)
- Helmholtz Centre for Infection Research (DE)
- German Center for Infection Research (DE)
- University Medical Center Hamburg-Eppendorf (DE)
- ORCID
- Schulte-Schrepping, Jonas
- Reusch, Nico
- Paclik, Daniela
- Baßler, Kevin
- Schlickeiser, Stephan
- Zhang, Bowen
- Krämer, Benjamin
- Krammer, Tobias
- Brumhard, Sophia
- Bonaguro, Lorenzo
- De Domenico, Elena
- Wendisch, Daniel
- Grasshoff, Martin
- Kapellos, Theodore S.
- Beckstette, Michael
- Pecht, Tal
- Dietrich, Oliver
- Mei, Henrik E.
- Schulz, Axel R.
- Kunkel, Désirée
- Vafadarnejad, Ehsan
- Xu, Cheng-Jian
- Horne, Arik
- Herbert, Miriam
- Drews, Anna
- Thibeault, Charlotte
- Hippenstiel, Stefan
- Hocke, Andreas
- Müller-Redetzky, Holger
- Machleidt, Felix
- Uhrig, Alexander
- Stegemann, Miriam
- Volk, Hans-Dieter
- Goffinet, Christine
- Wyler, Emanuel
- Georg, Philipp
- Neuwinger, Nick
- Kappert, Kai
- Tauber, Rudolf
- Corman, Victor
- Raabe, Jan
- Kaiser, Kim Melanie
- Rieke, Gereon
- Meisel, Christian
- Ulas, Thomas
- Becker, Matthias
- Geffers, Robert
- Witzenrath, Martin
- Drosten, Christian
- Suttorp, Norbert
- Kurth, Florian
- Händler, Kristian
- Aschenbrenner, Anna C.
- Nattermann, Jacob
- Angelov, Angel
- Bals, Robert
- Bartholomäus, Alexander
- Becker, Anke
- Bezdan, Daniela
- Bonifacio, Ezio
- Clavel, Thomas
- Diefenbach, Andreas
- Dilthey, Alexander
- Förstner, Konrad
- Frick, Julia-Stefanie
- Gagneur, Julien
- Goesmann, Alexander
- Hain, Torsten
- Hummel, Michael
- Kalinowski, Jörn
- Kallies, René
- Kehr, Birte
- Keller, Andreas
- Kim-Hellmuth, Sarah
- Klein, Christoph
- Kohlbacher, Oliver
- Korbel, Jan O.
- Kurth, Ingo
- Ludwig, Kerstin
- Makarewicz, Oliwia
- Marz, Manja
- McHardy, Alice
- Mertes, Christian
- Nöthen, Markus
- Nürnberg, Peter
- Ohler, Uwe
- Ossowski, Stephan
- Overmann, Jörg
- Peter, Silke
- Pfeffer, Klaus
- Poetsch, Anna R.
- Pühler, Alfred
- Rajewsky, Nikolaus
- Ralser, Markus
- Rieß, Olaf
- Ripke, Stephan
- Rosenstiel, Philip
- Sczyrba, Alexander
- Stegle, Oliver
- Stoye, Jens
- Theis, Fabian
- Vogel, Jörg
- Walker, Andreas
- Walter, Jörn
- Wieczorek, Dagmar
- Ziebuhr, John
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2020-09
- Volume
- 182
- Issue
- 6
- Pages
- 1419-1440.e23
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC7405822
- OpenAlex
- W3047402958
- Cited by
- 1,461
- References
- 146
- Citations by year
- 2026: 107 · 2025: 152 · 2024: 157 · 2023: 232 · 2022: 346 · 2021: 380 · 2020: 86
- FWCI
- 34.40
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- medRxiv (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- bonndoc (University of Bonn) (submittedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- DZNE Pub (submittedVersion)
- PUB – Publications at Bielefeld University (Bielefeld University) (submittedVersion)
- HZI (Helmholtz Centre for Infection Research) (submittedVersion, cc-by-nc-sa)
- Funders
- European Commission
- Radboud Universitair Medisch Centrum
- Helmholtz Association
- Bundesministerium für Bildung und Forschung
- Deutsche Forschungsgemeinschaft
- Deutsches Zentrum für Infektionsforschung
- Topics
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
- Keywords
- severe COVID-19, SARS-CoV-2, myeloid cells, inflammatory monocytes, neutrophils, emergency myelopoiesis, neutrophil dysfunction, HLA-DR, interferon-stimulated genes, immune dysregulation, peripheral blood mononuclear cells, single-cell RNA sequencing, single-cell proteomics, disease severity
- MeSH terms
- COVID-19, Adult, Aged, Cells, Cultured, Female, HLA-DR Antigens, Humans, Male, Middle Aged, Pneumonia, Viral, Coronavirus Infections, CD11 Antigens, Proteome, Myeloid Cells, Myelopoiesis, Proteomics, Pandemics, Single-Cell Analysis
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