Longitudinal Multi-omics Analyses Identify Responses of Megakaryocytes, Erythroid Cells, and Plasmablasts as Hallmarks of Severe COVID-19

HCA Lung Biological Network; the Deutsche COVID-19 Omics Initiative (DeCOI)

doi:10.1016/j.immuni.2020.11.017

Longitudinal Multi-omics Analyses Identify Responses of Megakaryocytes, Erythroid Cells, and Plasmablasts as Hallmarks of Severe COVID-19

HCA Lung Biological Network, the Deutsche COVID-19 Omics Initiative (DeCOI)

Medicine, Pulmonary Division

Research output: Contribution to journal › Article › peer-review

251 Scopus citations

Abstract

Bernardes et al. explore COVID-19 disease trajectories by performing longitudinal multi-omics analyses in peripheral blood samples from hospitalized patients. The analyses identify increased numbers of plasmablasts, interferon-activated megakaryocytes, and erythroid cells as hallmarks of severe disease and define molecular signatures linked to a fatal COVID-19 disease outcome.

Original language	English (US)
Pages (from-to)	1296-1314.e9
Journal	Immunity
Volume	53
Issue number	6
DOIs	https://doi.org/10.1016/j.immuni.2020.11.017
State	Published - Dec 15 2020

Funding

We thank K. Greve, M. Rohm, M. Hansen, S. Kock, D. Oelsner, S. Baumgarten, M. Reffelmann, M. Schlapkohl, N. Braun, T. Wesse, M. Basso, Y. Dolschanskaya, X. Yi, C. Lancken, and M. Vollstedt for perfect technical assistance. This work was supported by the German Research Foundation (DFG) CCGA Nr. 07495230, a COVID-response grant of the state SH, ExC 2167 Precision Medicine in Chronic Inflammation (RTF-VI), the research group miTARGET and the CRC1182 C2 project to P.R.; the IMI2 Project 3TR to P.R. and S.S.; INST 37/1049-1, INST 216/981-1, INST 257/605-1, INST 269/768-1, INST 217/988-1, INST 217/577-1, and EXC2151/1 (390873048) to J.L.S.; SFB TR57 and SPP1937 to J.N.; Helmholtz-Gemeinschaft Deutscher Forschungszentren, Germany (sparse2big) to J.L.S.; EU projects SYSCID (733100) to P.R. and J.L.S.; the DZIF, Germany (TTU 04.816 and 04.817) to J.N.; and the Hector Foundation) (M89) to J.N. A.D. acknowledges support by the DFG (EXC 2124-390838134 Controlling Microbes to Fight Infections) and the German Center for Infection Research (DZIF grant N\u00B0 8020708703). C.K. acknowledges support by the DFG through EXC 2167, RTF-VIII, and the CRC 1182. This publication is part of the Human Cell Atlas (www.humancellatlas.org/publications). We are indebted to the patients, their families, and the hospital staff for support, without whom this study would not have been possible. S.S. J.L.S. and P.R. conceived study concept and design. J.P.B. N.M. F.T. T. Bahmer, U.G. P.K. P.B. G.E. A.F. N.F. R.J. K.F.R. J. Rupp, A.S. H.B. B.F.H. C.K. J. Heyckendorf, M.K. and J. Rybniker contributed to study concept. J.P.B. N.M. F.T. L.B. U.G. A.K, E.R. J.J.S, H.B. B.F.H. C.K. J.L.S. and P.R. contributed to literature search, data interpretation, and writing the initial manuscript. All authors contributed to reviewing and editing of the manuscript. F.T. T. Bahmer, J.I.B. J.F. U.G. P.K. E.R. J.D. G.E. J. Franzenburg, S.F. N.F. J. Fu\u00DF, A.G. J. Hamm, F.H. S.I. S.K. C.L. G.L. M.L. R.M. J.N. P.P. C.R. J. Rupp, A.S. D. Skowasch, J. Heyckendorf, M.K. and P.R. conducted sample collection and processing. J.P.B. N.M. F.T. L.B. U.G. J.J.S. A.K. E.R. A.C.A, N.B. T. Boysen, B.B. A.D. D.E. M.F. M.P.H. Y.H.K. R.K. C.L. G.M. A.R. J.S.S, T.U. K.P.W. M.W. J.Z. H.B. and C.K. conducted data analysis. J.P.B. N.M. F.T. L.B. D.B. U.G. J.J.S. A.K. C.R. E.R. H.B. and P.R. made figures and tables. The authors declare no conflicting interests. We thank K. Greve, M. Rohm, M. Hansen, S. Kock, D. Oelsner, S. Baumgarten, M. Reffelmann, M. Schlapkohl, N. Braun, T. Wesse, M. Basso, Y. Dolschanskaya, X. Yi, C. Lancken, and M. Vollstedt for perfect technical assistance. This work was supported by the German Research Foundation (DFG) CCGA Nr. 07495230 , a COVID-response grant of the state SH , ExC 2167 Precision Medicine in Chronic Inflammation ( RTF-VI ), the research group miTARGET and the CRC1182 C2 project to P.R.; the IMI2 Project 3TR to P.R. and S.S.; INST 37/1049-1 , INST 216/981-1 , INST 257/605-1 , INST 269/768-1 , INST 217/988-1 , INST 217/577-1 , and EXC2151/1 ( 390873048 ) to J.L.S.; SFB TR57 and SPP1937 to J.N.; Helmholtz-Gemeinschaft Deutscher Forschungszentren, Germany ( sparse2big ) to J.L.S.; EU projects SYSCID ( 733100 ) to P.R. and J.L.S.; the DZIF, Germany ( TTU 04.816 and 04.817 ) to J.N.; and the Hector Foundation ) ( M89 ) to J.N. A.D. acknowledges support by the DFG ( EXC 2124-390838134 Controlling Microbes to Fight Infections) and the German Center for Infection Research (DZIF grant N\u00B0 8020708703). C.K. acknowledges support by the DFG through EXC 2167 , RTF-VIII , and the CRC 1182 . This publication is part of the Human Cell Atlas ( www.humancellatlas.org/publications ). We are indebted to the patients, their families, and the hospital staff for support, without whom this study would not have been possible.

Keywords

COVID-19
RNA-seq
acute respiratory distress
blood
disease trajectory
immune response
infectious disease
methylation
scRNA-seq
virus

ASJC Scopus subject areas

Immunology and Allergy
Immunology
Infectious Diseases

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.immuni.2020.11.017

Cite this

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title = "Longitudinal Multi-omics Analyses Identify Responses of Megakaryocytes, Erythroid Cells, and Plasmablasts as Hallmarks of Severe COVID-19",

abstract = "Bernardes et al. explore COVID-19 disease trajectories by performing longitudinal multi-omics analyses in peripheral blood samples from hospitalized patients. The analyses identify increased numbers of plasmablasts, interferon-activated megakaryocytes, and erythroid cells as hallmarks of severe disease and define molecular signatures linked to a fatal COVID-19 disease outcome.",

keywords = "COVID-19, RNA-seq, acute respiratory distress, blood, disease trajectory, immune response, infectious disease, methylation, scRNA-seq, virus",

author = "{HCA Lung Biological Network} and {the Deutsche COVID-19 Omics Initiative (DeCOI)} and Bernardes, {Joana P.} and Neha Mishra and Florian Tran and Thomas Bahmer and Lena Best and Blase, {Johanna I.} and Dora Bordoni and Jeanette Franzenburg and Ulf Geisen and Jonathan Josephs-Spaulding and Philipp K{\"o}hler and Axel K{\"u}nstner and Elisa Rosati and Aschenbrenner, {Anna C.} and Petra Bacher and Nathan Baran and Teide Boysen and Burkhard Brandt and Niklas Bruse and Jonathan D{\"o}rr and Andreas Dr{\"a}ger and Gunnar Elke and David Ellinghaus and Julia Fischer and Michael Forster and Andre Franke and S{\"o}ren Franzenburg and Norbert Frey and Anette Friedrichs and Janina Fu{\ss} and Andreas Gl{\"u}ck and Jacob Hamm and Finn Hinrichsen and Hoeppner, {Marc P.} and Simon Imm and Ralf Junker and Sina Kaiser and Kan, {Ying H.} and Rainer Knoll and Christoph Lange and Georg Laue and Clemens Lier and Matthias Lindner and Georgios Marinos and Robert Markewitz and Jacob Nattermann and Rainer Noth and Peter Pickkers and Rabe, {Klaus F.} and Paul Reyfman",

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doi = "10.1016/j.immuni.2020.11.017",

language = "English (US)",

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AU - the Deutsche COVID-19 Omics Initiative (DeCOI)

AU - Bernardes, Joana P.

AU - Mishra, Neha

AU - Tran, Florian

AU - Bahmer, Thomas

AU - Best, Lena

AU - Blase, Johanna I.

AU - Bordoni, Dora

AU - Franzenburg, Jeanette

AU - Geisen, Ulf

AU - Josephs-Spaulding, Jonathan

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AU - Künstner, Axel

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AU - Aschenbrenner, Anna C.

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AU - Baran, Nathan

AU - Boysen, Teide

AU - Brandt, Burkhard

AU - Bruse, Niklas

AU - Dörr, Jonathan

AU - Dräger, Andreas

AU - Elke, Gunnar

AU - Ellinghaus, David

AU - Fischer, Julia

AU - Forster, Michael

AU - Franke, Andre

AU - Franzenburg, Sören

AU - Frey, Norbert

AU - Friedrichs, Anette

AU - Fuß, Janina

AU - Glück, Andreas

AU - Hamm, Jacob

AU - Hinrichsen, Finn

AU - Hoeppner, Marc P.

AU - Imm, Simon

AU - Junker, Ralf

AU - Kaiser, Sina

AU - Kan, Ying H.

AU - Knoll, Rainer

AU - Lange, Christoph

AU - Laue, Georg

AU - Lier, Clemens

AU - Lindner, Matthias

AU - Marinos, Georgios

AU - Markewitz, Robert

AU - Nattermann, Jacob

AU - Noth, Rainer

AU - Pickkers, Peter

AU - Rabe, Klaus F.

AU - Reyfman, Paul

PY - 2020/12/15

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AB - Bernardes et al. explore COVID-19 disease trajectories by performing longitudinal multi-omics analyses in peripheral blood samples from hospitalized patients. The analyses identify increased numbers of plasmablasts, interferon-activated megakaryocytes, and erythroid cells as hallmarks of severe disease and define molecular signatures linked to a fatal COVID-19 disease outcome.

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KW - RNA-seq

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KW - disease trajectory

KW - immune response

KW - infectious disease

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KW - scRNA-seq

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Longitudinal Multi-omics Analyses Identify Responses of Megakaryocytes, Erythroid Cells, and Plasmablasts as Hallmarks of Severe COVID-19

Abstract

Funding

Keywords

ASJC Scopus subject areas

UN SDGs

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