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12 15, 2020;53 (6): 1296-1314.e9.

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

Joana P Bernardes, Neha Mishra, Florian Tran, Thomas Bahmer, Lena Best, Johanna I Blase, Dora Bordoni, Jeanette Franzenburg, Ulf Geisen, Jonathan Josephs-Spaulding, Philipp Köhler, Axel Künstner, Elisa Rosati, Anna C Aschenbrenner, Petra Bacher, Nathan Baran, Teide Boysen, Burkhard Brandt, Niklas Bruse, Jonathan Dörr, Andreas Dräger, Gunnar Elke, David Ellinghaus, Julia Fischer, Michael Forster, Andre Franke, Sören Franzenburg, Norbert Frey, Anette Friedrichs, Janina Fuß, Andreas Glück, Jacob Hamm, Finn Hinrichsen, Marc P Hoeppner, Simon Imm, Ralf Junker, Sina Kaiser, Ying H Kan, Rainer Knoll, Christoph Lange, Georg Laue, Clemens Lier, Matthias Lindner, Georgios Marinos, Robert Markewitz, Jacob Nattermann, Rainer Noth, Peter Pickkers, Klaus F Rabe, Alina Renz, Christoph Röcken, Jan Rupp, Annika Schaffarzyk, Alexander Scheffold, Jonas Schulte-Schrepping, Domagoj Schunk, Dirk Skowasch, Thomas Ulas, Klaus-Peter Wandinger, Michael Wittig, Johannes Zimmermann, Hauke Busch, Bimba F Hoyer, Christoph Kaleta, Jan Heyckendorf, Matthijs Kox, Jan Rybniker, Stefan Schreiber, Joachim L Schultze, Philip Rosenstiel, HCA Lung Biological Network, Deutsche COVID-19 Omics Initiative (DeCOI)
Author Information
  1. Joana P Bernardes: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  2. Neha Mishra: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  3. Florian Tran: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany; Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  4. Thomas Bahmer: Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  5. Lena Best: Institute for Experimental Medicine, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  6. Johanna I Blase: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  7. Dora Bordoni: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  8. Jeanette Franzenburg: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany; Institute of Clinical Chemistry, University Medical Center Schleswig-Holstein, 24105 Kiel and 23562 Lübeck, Germany.
  9. Ulf Geisen: Section for Rheumatology, Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  10. Jonathan Josephs-Spaulding: Institute for Experimental Medicine, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  11. Philipp Köhler: Department I of Internal Medicine, University of Cologne and University Hospital Cologne; German Center for Infection Research, Partner Site Bonn-Cologne and Center for Molecular Medicine Cologne, University of Cologne, 50931 Cologne, Germany; Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), 50937 Cologne, Germany.
  12. Axel Künstner: Center for Molecular Medicine Cologne (CMMC), University of Cologne, 50931, Germany.
  13. Elisa Rosati: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  14. Anna C Aschenbrenner: Genomics & Immunoregulation, Life & Medical Sciences (LIMES) Institute, University of Bonn, 53115 Bonn, Germany; Departments of Intensive Care Medicine and Radboud Center for Infectious Diseases (RCI), Radboud University Medical Center, 6500 HB Nijmegen, the Netherlands; Systems Medicine, German Center for Neurodegenerative Diseases (DZNE), 53127 Bonn, Germany; German Center for Neurodegenerative Diseases (DZNE), PRECISE Platform for Genomics and Epigenomics at DZNE, and University of Bonn, 53127 Bonn, Germany.
  15. Petra Bacher: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany; Institute of Immunology, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  16. Nathan Baran: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  17. Teide Boysen: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  18. Burkhard Brandt: Institute of Clinical Chemistry, University Medical Center Schleswig-Holstein, 24105 Kiel and 23562 Lübeck, Germany.
  19. Niklas Bruse: Departments of Intensive Care Medicine and Radboud Center for Infectious Diseases (RCI), Radboud University Medical Center, 6500 HB Nijmegen, the Netherlands.
  20. Jonathan Dörr: Section for Rheumatology, Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  21. Andreas Dräger: Department of Computer Science, Institute for Bioinformatics and Medical Informatics (IBMI), University of Tübingen and German Center for Infection Research (DZIF), Partner site Tübingen, 72076 Tübingen, Germany.
  22. Gunnar Elke: Department of Anaesthesiology and Intensive Care Medicine, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  23. David Ellinghaus: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  24. Julia Fischer: Department I of Internal Medicine, University of Cologne and University Hospital Cologne; German Center for Infection Research, Partner Site Bonn-Cologne and Center for Molecular Medicine Cologne, University of Cologne, 50931 Cologne, Germany; Center for Molecular Medicine Cologne (CMMC), University of Cologne, 50931, Germany.
  25. Michael Forster: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  26. Andre Franke: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  27. Sören Franzenburg: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  28. Norbert Frey: Department of Internal Medicine III, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  29. Anette Friedrichs: Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  30. Janina Fuß: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  31. Andreas Glück: Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  32. Jacob Hamm: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  33. Finn Hinrichsen: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  34. Marc P Hoeppner: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  35. Simon Imm: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  36. Ralf Junker: Institute of Clinical Chemistry, University Medical Center Schleswig-Holstein, 24105 Kiel and 23562 Lübeck, Germany.
  37. Sina Kaiser: Section for Rheumatology, Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  38. Ying H Kan: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  39. Rainer Knoll: Systems Medicine, German Center for Neurodegenerative Diseases (DZNE), 53127 Bonn, Germany; German Center for Neurodegenerative Diseases (DZNE), PRECISE Platform for Genomics and Epigenomics at DZNE, and University of Bonn, 53127 Bonn, Germany.
  40. Christoph Lange: Division of Clinical Infectious Diseases, Research Center Borstel and German Center for Infection Research (DZIF), TTU-TB, 23845 Borstel, Germany.
  41. Georg Laue: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  42. Clemens Lier: Institute of Clinical Chemistry, University Medical Center Schleswig-Holstein, 24105 Kiel and 23562 Lübeck, Germany.
  43. Matthias Lindner: Department of Anaesthesiology and Intensive Care Medicine, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  44. Georgios Marinos: Institute for Experimental Medicine, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  45. Robert Markewitz: Institute of Clinical Chemistry, University Medical Center Schleswig-Holstein, 24105 Kiel and 23562 Lübeck, Germany.
  46. Jacob Nattermann: Department of Internal Medicine I and German Center for Infection Research (DZIF), University of Bonn, 53217 Bonn, Germany.
  47. Rainer Noth: Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  48. Peter Pickkers: Departments of Intensive Care Medicine and Radboud Center for Infectious Diseases (RCI), Radboud University Medical Center, 6500 HB Nijmegen, the Netherlands.
  49. Klaus F Rabe: Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany;  LungenClinic Grosshansdorf, Airway Research Centre North, German Centre for Lung Research, 22927 Grosshansdorf, Germany.
  50. Alina Renz: Department of Computer Science, Institute for Bioinformatics and Medical Informatics (IBMI), University of Tübingen and German Center for Infection Research (DZIF), Partner site Tübingen, 72076 Tübingen, Germany.
  51. Christoph Röcken: Department of Pathology, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  52. Jan Rupp: Department of Infectious Diseases and Microbiology, University of Lübeck, 23562 Lübeck, Germany.
  53. Annika Schaffarzyk: Section for Rheumatology, Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  54. Alexander Scheffold: Institute of Immunology, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  55. Jonas Schulte-Schrepping: Genomics & Immunoregulation, Life & Medical Sciences (LIMES) Institute, University of Bonn, 53115 Bonn, Germany; Systems Medicine, German Center for Neurodegenerative Diseases (DZNE), 53127 Bonn, Germany.
  56. Domagoj Schunk: Department for Emergency Medicine, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  57. Dirk Skowasch: Section of Pneumology, Department of Internal Medicine II, University Hospital Bonn, , 53127 Bonn, Germany.
  58. Thomas Ulas: Genomics & Immunoregulation, Life & Medical Sciences (LIMES) Institute, University of Bonn, 53115 Bonn, Germany; Systems Medicine, German Center for Neurodegenerative Diseases (DZNE), 53127 Bonn, Germany; German Center for Neurodegenerative Diseases (DZNE), PRECISE Platform for Genomics and Epigenomics at DZNE, and University of Bonn, 53127 Bonn, Germany.
  59. Klaus-Peter Wandinger: Institute of Clinical Chemistry, University Medical Center Schleswig-Holstein, 24105 Kiel and 23562 Lübeck, Germany.
  60. Michael Wittig: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  61. Johannes Zimmermann: Institute for Experimental Medicine, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  62. Hauke Busch: Lübeck Institute of Experimental Dermatology, University of Lübeck, 23562 Lübeck, Germany.
  63. Bimba F Hoyer: Section for Rheumatology, Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  64. Christoph Kaleta: Institute for Experimental Medicine, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  65. Jan Heyckendorf: Department of Internal Medicine III, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  66. Matthijs Kox: Genomics & Immunoregulation, Life & Medical Sciences (LIMES) Institute, University of Bonn, 53115 Bonn, Germany.
  67. Jan Rybniker: Department I of Internal Medicine, University of Cologne and University Hospital Cologne; German Center for Infection Research, Partner Site Bonn-Cologne and Center for Molecular Medicine Cologne, University of Cologne, 50931 Cologne, Germany; Center for Molecular Medicine Cologne (CMMC), University of Cologne, 50931, Germany.
  68. Stefan Schreiber: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany; Department of Internal Medicine I, University Medical Center Schleswig-Holstein, 24105 Kiel, Germany.
  69. Joachim L Schultze: Genomics & Immunoregulation, Life & Medical Sciences (LIMES) Institute, University of Bonn, 53115 Bonn, Germany; Systems Medicine, German Center for Neurodegenerative Diseases (DZNE), 53127 Bonn, Germany; German Center for Neurodegenerative Diseases (DZNE), PRECISE Platform for Genomics and Epigenomics at DZNE, and University of Bonn, 53127 Bonn, Germany.
  70. Philip Rosenstiel: Institute of Clinical Molecular Biology, Kiel University and University Medical Center Schleswig-Holstein, 24105 Kiel, Germany. Electronic address: p.rosenstiel@mucosa.de.
PMID: 33296687 DOI: 10.1016/j.immuni.2020.11.017

Abstract

Temporal resolution of cellular features associated with a severe COVID-19 disease trajectory is needed for understanding skewed immune responses and defining predictors of outcome. Here, we performed a longitudinal multi-omics study using a two-center cohort of 14 patients. We analyzed the bulk transcriptome, bulk DNA methylome, and single-cell transcriptome (>358,000 cells, including BCR profiles) of peripheral blood samples harvested from up to 5 time points. Validation was performed in two independent cohorts of COVID-19 patients. Severe COVID-19 was characterized by an increase of proliferating, metabolically hyperactive plasmablasts. Coinciding with critical illness, we also identified an expansion of interferon-activated circulating megakaryocytes and increased erythropoiesis with features of hypoxic signaling. Megakaryocyte- and erythroid-cell-derived co-expression modules were predictive of fatal disease outcome. The study demonstrates broad cellular effects of SARS-CoV-2 infection beyond adaptive immune cells and provides an entry point toward developing biomarkers and targeted treatments of patients with COVID-19.

Keywords

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

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Grants

  1. P30 DK089503/NIDDK NIH HHS

MeSH Term

Adult
Aged
Aged, 80 and over
Biomarkers
Blood Circulation
COVID-19
Cells, Cultured
Cohort Studies
Disease Progression
Erythroid Cells
Female
Gene Expression Profiling
Humans
Male
Megakaryocytes
Middle Aged
Plasma Cells
Proteomics
SARS-CoV-2
Sequence Analysis, RNA
Severity of Illness Index
Single-Cell Analysis

Chemicals

Biomarkers
Journal Article Research Support, Non-U.S. Gov't

Links to CNCB-NGDC Resources

GEN: GEND000416 (Longitudinal multi-omics identifies responses of megakaryocytes, erythroid cells and plasmablasts as hallmarks of severe COVID-19 trajectories [sequencing])

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