Multi-omic profiling reveals widespread dysregulation of innate immunity and hematopoiesis in COVID-19
Our understanding of protective versus pathological immune responses to SARS-CoV-2, the virus that causes coronavirus disease 2019 (COVID-19), is limited by inadequate profiling of patients at the extremes of the disease severity spectrum. Here, we performed multi-omic single-cell immune profiling o...
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| Published in | The Journal of experimental medicine Vol. 218; no. 8 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Rockefeller University Press
02.08.2021
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Our understanding of protective versus pathological immune responses to SARS-CoV-2, the virus that causes coronavirus disease 2019 (COVID-19), is limited by inadequate profiling of patients at the extremes of the disease severity spectrum. Here, we performed multi-omic single-cell immune profiling of 64 COVID-19 patients across the full range of disease severity, from outpatients with mild disease to fatal cases. Our transcriptomic, epigenomic, and proteomic analyses revealed widespread dysfunction of peripheral innate immunity in severe and fatal COVID-19, including prominent hyperactivation signatures in neutrophils and NK cells. We also identified chromatin accessibility changes at NF-κB binding sites within cytokine gene loci as a potential mechanism for the striking lack of pro-inflammatory cytokine production observed in monocytes in severe and fatal COVID-19. We further demonstrated that emergency myelopoiesis is a prominent feature of fatal COVID-19. Collectively, our results reveal disease severity–associated immune phenotypes in COVID-19 and identify pathogenesis-associated pathways that are potential targets for therapeutic intervention. |
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| AbstractList | Single-cell profiling demonstrates multifarious dysregulation of innate immune phenotype associated with COVID-19 severity. Severe COVID-19 is associated with hyperactivation of neutrophils and NK cells, while monocytes take on tolerogenic phenotypes. Meanwhile, mild COVID-19 is associated with limited, or rapidly resolved, immune perturbation.
Our understanding of protective versus pathological immune responses to SARS-CoV-2, the virus that causes coronavirus disease 2019 (COVID-19), is limited by inadequate profiling of patients at the extremes of the disease severity spectrum. Here, we performed multi-omic single-cell immune profiling of 64 COVID-19 patients across the full range of disease severity, from outpatients with mild disease to fatal cases. Our transcriptomic, epigenomic, and proteomic analyses revealed widespread dysfunction of peripheral innate immunity in severe and fatal COVID-19, including prominent hyperactivation signatures in neutrophils and NK cells. We also identified chromatin accessibility changes at NF-κB binding sites within cytokine gene loci as a potential mechanism for the striking lack of pro-inflammatory cytokine production observed in monocytes in severe and fatal COVID-19. We further demonstrated that emergency myelopoiesis is a prominent feature of fatal COVID-19. Collectively, our results reveal disease severity–associated immune phenotypes in COVID-19 and identify pathogenesis-associated pathways that are potential targets for therapeutic intervention. Our understanding of protective versus pathological immune responses to SARS-CoV-2, the virus that causes coronavirus disease 2019 (COVID-19), is limited by inadequate profiling of patients at the extremes of the disease severity spectrum. Here, we performed multi-omic single-cell immune profiling of 64 COVID-19 patients across the full range of disease severity, from outpatients with mild disease to fatal cases. Our transcriptomic, epigenomic, and proteomic analyses revealed widespread dysfunction of peripheral innate immunity in severe and fatal COVID-19, including prominent hyperactivation signatures in neutrophils and NK cells. We also identified chromatin accessibility changes at NF-κB binding sites within cytokine gene loci as a potential mechanism for the striking lack of pro-inflammatory cytokine production observed in monocytes in severe and fatal COVID-19. We further demonstrated that emergency myelopoiesis is a prominent feature of fatal COVID-19. Collectively, our results reveal disease severity-associated immune phenotypes in COVID-19 and identify pathogenesis-associated pathways that are potential targets for therapeutic intervention. Our understanding of protective versus pathological immune responses to SARS-CoV-2, the virus that causes coronavirus disease 2019 (COVID-19), is limited by inadequate profiling of patients at the extremes of the disease severity spectrum. Here, we performed multi-omic single-cell immune profiling of 64 COVID-19 patients across the full range of disease severity, from outpatients with mild disease to fatal cases. Our transcriptomic, epigenomic, and proteomic analyses revealed widespread dysfunction of peripheral innate immunity in severe and fatal COVID-19, including prominent hyperactivation signatures in neutrophils and NK cells. We also identified chromatin accessibility changes at NF-κB binding sites within cytokine gene loci as a potential mechanism for the striking lack of pro-inflammatory cytokine production observed in monocytes in severe and fatal COVID-19. We further demonstrated that emergency myelopoiesis is a prominent feature of fatal COVID-19. Collectively, our results reveal disease severity-associated immune phenotypes in COVID-19 and identify pathogenesis-associated pathways that are potential targets for therapeutic intervention.Our understanding of protective versus pathological immune responses to SARS-CoV-2, the virus that causes coronavirus disease 2019 (COVID-19), is limited by inadequate profiling of patients at the extremes of the disease severity spectrum. Here, we performed multi-omic single-cell immune profiling of 64 COVID-19 patients across the full range of disease severity, from outpatients with mild disease to fatal cases. Our transcriptomic, epigenomic, and proteomic analyses revealed widespread dysfunction of peripheral innate immunity in severe and fatal COVID-19, including prominent hyperactivation signatures in neutrophils and NK cells. We also identified chromatin accessibility changes at NF-κB binding sites within cytokine gene loci as a potential mechanism for the striking lack of pro-inflammatory cytokine production observed in monocytes in severe and fatal COVID-19. We further demonstrated that emergency myelopoiesis is a prominent feature of fatal COVID-19. Collectively, our results reveal disease severity-associated immune phenotypes in COVID-19 and identify pathogenesis-associated pathways that are potential targets for therapeutic intervention. |
| Author | Do, Evan Thi Tran, Kim Quyen Whittle Dantzler, Kathleen Quinn, James V. Lyu, Shu-Chen Simpson, Laura Blomkalns, Andra L. Wei, Bei Brewer, Rachel Pi, Ruoxi Roque, Jonasel Fernandes, Andrea Ivison, Geoff Wilk, Aaron J. O’Hara, Ruth Rabinovitch, Marlene Zhao, Nancy Q. Martínez-Colón, Giovanny J. Bogusch, Drina Parks, Benjamin Rustagi, Arjun Ranganath, Thanmayi Blish, Catherine A. Yang, Samuel Jee, Kathryn McKechnie, Julia L. Kathale, Nimish Kumar, Komal de la Parte, Lauren Zhang, Wenming Visweswaran, Anita Lee, Madeline J. Jimenez-Morales, David Ashley, Euan A. Vergara, Rosemary Becker, Winston Hollis, Taylor Ugur, Michele Zudock, Elizabeth J. Haider, Kazim Nadeau, Kari C. Mann, Rosen Din, Hena Chang, Iris Martinez-Colon, Giovanny J. Greenleaf, William J. Newberry, Jennifer A. Holmes, Susan Manohar, Monali Tal, Michal Taylor, Shalina Baird, Andrea Krempski, James Ty, Maureen Nahass, Georgie Rogers, Angela J. Schreiber, Donald |
| AuthorAffiliation | 5 Graduate Program in Computer Science, Stanford University School of Medicine, Stanford, CA 2 Stanford Immunology Program, Stanford University School of Medicine, Stanford, CA 11 Sean N. Parker Center for Allergy and Asthma Research, Stanford University School of Medicine, Stanford, CA 9 Department of Emergency Medicine, Stanford University School of Medicine, Stanford, CA 3 Department of Medicine, Stanford University School of Medicine, Stanford, CA 4 Department of Genetics, Stanford University School of Medicine, Stanford, CA 6 Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 13 Department of Applied Physics, Stanford University, Stanford, CA 8 Vera Moulton Wall Center for Pulmonary Vascular Disease, Stanford University School of Medicine, Stanford, CA 12 Department of Statistics, Stanford University, Stanford, CA 10 Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA 1 Stanford Medical Scientist Training Program, |
| AuthorAffiliation_xml | – name: 5 Graduate Program in Computer Science, Stanford University School of Medicine, Stanford, CA – name: 13 Department of Applied Physics, Stanford University, Stanford, CA – name: 1 Stanford Medical Scientist Training Program, Stanford University School of Medicine, Stanford, CA – name: 12 Department of Statistics, Stanford University, Stanford, CA – name: 11 Sean N. Parker Center for Allergy and Asthma Research, Stanford University School of Medicine, Stanford, CA – name: 14 Chan Zuckerberg Biohub, San Francisco, CA – name: 3 Department of Medicine, Stanford University School of Medicine, Stanford, CA – name: 6 Department of Pediatrics, Stanford University School of Medicine, Stanford, CA – name: 4 Department of Genetics, Stanford University School of Medicine, Stanford, CA – name: 2 Stanford Immunology Program, Stanford University School of Medicine, Stanford, CA – name: 7 Cardiovascular Institute, Stanford University School of Medicine, Stanford, CA – name: 8 Vera Moulton Wall Center for Pulmonary Vascular Disease, Stanford University School of Medicine, Stanford, CA – name: 9 Department of Emergency Medicine, Stanford University School of Medicine, Stanford, CA – name: 10 Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34128959$$D View this record in MEDLINE/PubMed |
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| Contributor | Kumar, Komal Do, Evan de la Parte, Lauren Zhang, Wenming Visweswaran, Anita Thi Tran, Kim Quyen Lee, Madeline J. Whittle Dantzler, Kathleen Quinn, James V. Lyu, Shu-Chen Simpson, Laura Ashley, Euan A. Vergara, Rosemary Blomkalns, Andra L. Brewer, Rachel Hollis, Taylor Ugur, Michele Pi, Ruoxi Roque, Jonasel Fernandes, Andrea Zudock, Elizabeth J. Ivison, Geoff Haider, Kazim Nadeau, Kari C. Mann, Rosen Din, Hena Chang, Iris Martinez-Colon, Giovanny J. Newberry, Jennifer A. Wilk, Aaron J. O’Hara, Ruth Manohar, Monali Tal, Michal Zhao, Nancy Q. Baird, Andrea Krempski, James Ty, Maureen Bogusch, Drina Nahass, Georgie Rustagi, Arjun Ranganath, Thanmayi Blish, Catherine A. Rogers, Angela J. Yang, Samuel Jee, Kathryn McKechnie, Julia L. Kathale, Nimish Schreiber, Donald |
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| Copyright | 2021 Wilk et al. 2021 Wilk et al. 2021 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Disclosures: A.J. Wilk reported grants from Stanford University Interdisciplinary Graduate Fellowship and NIH during the conduct of the study. M.J. Lee reported grants from NIH during the conduct of the study. B. Wei reported "Stanford University." E.A. Ashley reported "other" from Personalis, Inc., DeepCell, Inc., SVEXA Inc., Astra Zeneca, Gilead, MyoKardia, Amgen, Takeda, Novartis, Genome Medical, Avive, Samsung, Apple Inc., Google, Verily, Disney Inc., Illumina Inc., PacBio, Nanopore, Foresite Capital, and Sequence Bio outside the submitted work. K.C. Nadeau reported grants from National Institute of Allergy and Infectious Diseases, National Heart, Lung, and Blood Institute, Food Allergy Research and Education, and World Allergy Organization; "other" from Cour Pharma, Before Brands, Alladapt, Latitude, IgGenix, Immune Tolerance Network, and National Institutes of Health clinical research centers outside the submitted work; in addition, K.C. Nadeau had a patent to "mixed allergen composition and methods for using the same with royalties paid (Alladapt and Before Brands), a patent to "granulocyte-based methods for detecting and monitoring immune system disorders" issued, and a patent to "methods and assays for detecting and quantifying pure subpopulations of white blood cells in immune system disorders" issued. A.J. Rogers reported personal fees from Merck outside the submitted work. W.J. Greenleaf reported personal fees from 10x Genomics during the conduct of the study, and personal fees from Guardant Health and Protillion Biosciences outside the submitted work; in addition, W.J. Greenleaf had a patent to US20160060691A1 with royalties paid (10x Genomics). C.A. Blish reported personal fees from Catamaran Bio outside the submitted work. No other disclosures were reported. A.J. Wilk, M.J. Lee, B. Wei, and B. Parks contributed equally to this paper. Stanford COVID-19 Biobank members: Thanmayi Ranganath, Nancy Q. Zhao, Aaron J. Wilk, Rosemary Vergara, Julia L. McKechnie, Lauren de la Parte, Kathleen Whittle Dantzler, Maureen Ty, Nimish Kathale, Giovanny J. Martínez-Colón, Arjun Rustagi, Geoff Ivison, Ruoxi Pi, Madeline J. Lee, Rachel Brewer, Taylor Hollis, Andrea Baird, Michele Ugur, Michal Tal, Drina Bogusch, Georgie Nahass, Kazim Haider, Kim Quyen Thi Tran, Laura Simpson, Hena Din, Jonasel Roque, Rosen Mann, Iris Chang, Evan Do, Andrea Fernandes, Shu-Chen Lyu, Wenming Zhang, Monali Manohar, James Krempski, Anita Visweswaran, Elizabeth J. Zudock, Kathryn Jee, Komal Kumar, Jennifer A. Newberry, James V. Quinn, Donald Schreiber, Euan A. Ashley, Catherine A. Blish, Andra L. Blomkalns, Kari C. Nadeau, Ruth O’Hara, Angela J. Rogers, Samuel Yang. |
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| SubjectTerms | Adult Aged Case-Control Studies Covid-19 COVID-19 - blood COVID-19 - genetics COVID-19 - immunology COVID-19 - mortality Cytokines - genetics Epigenesis, Genetic Female Hematopoiesis Humans Immunity, Innate - physiology Infectious Disease and Host Defense Innate Immunity and Inflammation Killer Cells, Natural - pathology Killer Cells, Natural - virology Male Middle Aged Monocytes - pathology Monocytes - virology Neutrophils - pathology Neutrophils - virology NF-kappa B - metabolism Proteomics Severity of Illness Index Single-Cell Analysis |
| Title | Multi-omic profiling reveals widespread dysregulation of innate immunity and hematopoiesis in COVID-19 |
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