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A single-cell atlas of the peripheral immune response in patients with severe COVID-19

There is an urgent need to better understand the pathophysiology of Coronavirus disease 2019 (COVID-19), the global pandemic caused by SARS-CoV-2, which has infected more than three million people worldwide . Approximately 20% of patients with COVID-19 develop severe disease and 5% of patients requi... Full description

Journal Title: Nature medicine 2020-07, Vol.26 (7), p.1070-1076
Main Author: Wilk, Aaron J
Other Authors: Rustagi, Arjun , Zhao, Nancy Q , Roque, Jonasel , Martínez-Colón, Giovanny J , McKechnie, Julia L , Ivison, Geoffrey T , Ranganath, Thanmayi , Vergara, Rosemary , Hollis, Taylor , Simpson, Laura J , Grant, Philip , Subramanian, Aruna , Rogers, Angela J , Blish, Catherine A
Format: Electronic Article Electronic Article
Language: English
Subjects:
RNA
Publisher: United States: Nature Publishing Group
ID: ISSN: 1078-8956
Link: https://www.ncbi.nlm.nih.gov/pubmed/32514174
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recordid: cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7382903
title: A single-cell atlas of the peripheral immune response in patients with severe COVID-19
format: Article
creator:
  • Wilk, Aaron J
  • Rustagi, Arjun
  • Zhao, Nancy Q
  • Roque, Jonasel
  • Martínez-Colón, Giovanny J
  • McKechnie, Julia L
  • Ivison, Geoffrey T
  • Ranganath, Thanmayi
  • Vergara, Rosemary
  • Hollis, Taylor
  • Simpson, Laura J
  • Grant, Philip
  • Subramanian, Aruna
  • Rogers, Angela J
  • Blish, Catherine A
subjects:
  • Acute respiratory distress syndrome
  • Adult
  • Aged
  • Aged, 80 and over
  • Analysis
  • B cells
  • Betacoronavirus - immunology
  • Biological response modifiers
  • Care and treatment
  • Case-Control Studies
  • Coronavirus Infections - genetics
  • Coronavirus Infections - immunology
  • Coronavirus Infections - pathology
  • Coronaviruses
  • COVID-19
  • Cytokines
  • Cytokines - genetics
  • Cytokines - metabolism
  • Development and progression
  • Female
  • Gene expression
  • Gene Expression Profiling - methods
  • Gene sequencing
  • Genes
  • Genetic aspects
  • Health aspects
  • Histocompatibility antigen HLA
  • Humans
  • Immune response
  • Immune system
  • Immunity, Cellular
  • Immunotherapy
  • Inflammation
  • Interferon
  • Killer Cells, Natural - immunology
  • Killer Cells, Natural - metabolism
  • Leukocytes (mononuclear)
  • Leukocytes, Mononuclear - immunology
  • Leukocytes, Mononuclear - metabolism
  • Leukocytes, Mononuclear - virology
  • Lymphocytes
  • Lymphocytes T
  • Male
  • Middle Aged
  • Monocytes
  • Pandemics
  • Peripheral blood mononuclear cells
  • Phenotypes
  • Physiological aspects
  • Pneumonia, Viral - genetics
  • Pneumonia, Viral - immunology
  • Pneumonia, Viral - pathology
  • Reconfiguration
  • Respiratory distress syndrome
  • Respiratory therapy
  • Ribonucleic acid
  • RNA
  • RNA sequencing
  • RNA-Seq - methods
  • SARS-CoV-2
  • Sequence Analysis, RNA - methods
  • Severe acute respiratory syndrome coronavirus 2
  • Severity of Illness Index
  • Single-Cell Analysis - methods
  • T cells
  • T-Lymphocytes - immunology
  • T-Lymphocytes - metabolism
  • Transcriptomics
  • Ventilation
  • Viral diseases
  • Young Adult
ispartof: Nature medicine, 2020-07, Vol.26 (7), p.1070-1076
description: There is an urgent need to better understand the pathophysiology of Coronavirus disease 2019 (COVID-19), the global pandemic caused by SARS-CoV-2, which has infected more than three million people worldwide . Approximately 20% of patients with COVID-19 develop severe disease and 5% of patients require intensive care . Severe disease has been associated with changes in peripheral immune activity, including increased levels of pro-inflammatory cytokines that may be produced by a subset of inflammatory monocytes , lymphopenia and T cell exhaustion . To elucidate pathways in peripheral immune cells that might lead to immunopathology or protective immunity in severe COVID-19, we applied single-cell RNA sequencing (scRNA-seq) to profile peripheral blood mononuclear cells (PBMCs) from seven patients hospitalized for COVID-19, four of whom had acute respiratory distress syndrome, and six healthy controls. We identify reconfiguration of peripheral immune cell phenotype in COVID-19, including a heterogeneous interferon-stimulated gene signature, HLA class II downregulation and a developing neutrophil population that appears closely related to plasmablasts appearing in patients with acute respiratory failure requiring mechanical ventilation. Importantly, we found that peripheral monocytes and lymphocytes do not express substantial amounts of pro-inflammatory cytokines. Collectively, we provide a cell atlas of the peripheral immune response to severe COVID-19.
language: eng
source:
identifier: ISSN: 1078-8956
fulltext: no_fulltext
issn:
  • 1078-8956
  • 1546-170X
url: Link


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titleA single-cell atlas of the peripheral immune response in patients with severe COVID-19
creatorWilk, Aaron J ; Rustagi, Arjun ; Zhao, Nancy Q ; Roque, Jonasel ; Martínez-Colón, Giovanny J ; McKechnie, Julia L ; Ivison, Geoffrey T ; Ranganath, Thanmayi ; Vergara, Rosemary ; Hollis, Taylor ; Simpson, Laura J ; Grant, Philip ; Subramanian, Aruna ; Rogers, Angela J ; Blish, Catherine A
creatorcontribWilk, Aaron J ; Rustagi, Arjun ; Zhao, Nancy Q ; Roque, Jonasel ; Martínez-Colón, Giovanny J ; McKechnie, Julia L ; Ivison, Geoffrey T ; Ranganath, Thanmayi ; Vergara, Rosemary ; Hollis, Taylor ; Simpson, Laura J ; Grant, Philip ; Subramanian, Aruna ; Rogers, Angela J ; Blish, Catherine A
descriptionThere is an urgent need to better understand the pathophysiology of Coronavirus disease 2019 (COVID-19), the global pandemic caused by SARS-CoV-2, which has infected more than three million people worldwide . Approximately 20% of patients with COVID-19 develop severe disease and 5% of patients require intensive care . Severe disease has been associated with changes in peripheral immune activity, including increased levels of pro-inflammatory cytokines that may be produced by a subset of inflammatory monocytes , lymphopenia and T cell exhaustion . To elucidate pathways in peripheral immune cells that might lead to immunopathology or protective immunity in severe COVID-19, we applied single-cell RNA sequencing (scRNA-seq) to profile peripheral blood mononuclear cells (PBMCs) from seven patients hospitalized for COVID-19, four of whom had acute respiratory distress syndrome, and six healthy controls. We identify reconfiguration of peripheral immune cell phenotype in COVID-19, including a heterogeneous interferon-stimulated gene signature, HLA class II downregulation and a developing neutrophil population that appears closely related to plasmablasts appearing in patients with acute respiratory failure requiring mechanical ventilation. Importantly, we found that peripheral monocytes and lymphocytes do not express substantial amounts of pro-inflammatory cytokines. Collectively, we provide a cell atlas of the peripheral immune response to severe COVID-19.
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subjectAcute respiratory distress syndrome ; Adult ; Aged ; Aged, 80 and over ; Analysis ; B cells ; Betacoronavirus - immunology ; Biological response modifiers ; Care and treatment ; Case-Control Studies ; Coronavirus Infections - genetics ; Coronavirus Infections - immunology ; Coronavirus Infections - pathology ; Coronaviruses ; COVID-19 ; Cytokines ; Cytokines - genetics ; Cytokines - metabolism ; Development and progression ; Female ; Gene expression ; Gene Expression Profiling - methods ; Gene sequencing ; Genes ; Genetic aspects ; Health aspects ; Histocompatibility antigen HLA ; Humans ; Immune response ; Immune system ; Immunity, Cellular ; Immunotherapy ; Inflammation ; Interferon ; Killer Cells, Natural - immunology ; Killer Cells, Natural - metabolism ; Leukocytes (mononuclear) ; Leukocytes, Mononuclear - immunology ; Leukocytes, Mononuclear - metabolism ; Leukocytes, Mononuclear - virology ; Lymphocytes ; Lymphocytes T ; Male ; Middle Aged ; Monocytes ; Pandemics ; Peripheral blood mononuclear cells ; Phenotypes ; Physiological aspects ; Pneumonia, Viral - genetics ; Pneumonia, Viral - immunology ; Pneumonia, Viral - pathology ; Reconfiguration ; Respiratory distress syndrome ; Respiratory therapy ; Ribonucleic acid ; RNA ; RNA sequencing ; RNA-Seq - methods ; SARS-CoV-2 ; Sequence Analysis, RNA - methods ; Severe acute respiratory syndrome coronavirus 2 ; Severity of Illness Index ; Single-Cell Analysis - methods ; T cells ; T-Lymphocytes - immunology ; T-Lymphocytes - metabolism ; Transcriptomics ; Ventilation ; Viral diseases ; Young Adult
ispartofNature medicine, 2020-07, Vol.26 (7), p.1070-1076
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4Martínez-Colón, Giovanny J
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6Ivison, Geoffrey T
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8Vergara, Rosemary
9Hollis, Taylor
10Simpson, Laura J
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12Subramanian, Aruna
13Rogers, Angela J
14Blish, Catherine A
title
0A single-cell atlas of the peripheral immune response in patients with severe COVID-19
1Nature medicine
addtitleNat Med
descriptionThere is an urgent need to better understand the pathophysiology of Coronavirus disease 2019 (COVID-19), the global pandemic caused by SARS-CoV-2, which has infected more than three million people worldwide . Approximately 20% of patients with COVID-19 develop severe disease and 5% of patients require intensive care . Severe disease has been associated with changes in peripheral immune activity, including increased levels of pro-inflammatory cytokines that may be produced by a subset of inflammatory monocytes , lymphopenia and T cell exhaustion . To elucidate pathways in peripheral immune cells that might lead to immunopathology or protective immunity in severe COVID-19, we applied single-cell RNA sequencing (scRNA-seq) to profile peripheral blood mononuclear cells (PBMCs) from seven patients hospitalized for COVID-19, four of whom had acute respiratory distress syndrome, and six healthy controls. We identify reconfiguration of peripheral immune cell phenotype in COVID-19, including a heterogeneous interferon-stimulated gene signature, HLA class II downregulation and a developing neutrophil population that appears closely related to plasmablasts appearing in patients with acute respiratory failure requiring mechanical ventilation. Importantly, we found that peripheral monocytes and lymphocytes do not express substantial amounts of pro-inflammatory cytokines. Collectively, we provide a cell atlas of the peripheral immune response to severe COVID-19.
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0Acute respiratory distress syndrome
1Adult
2Aged
3Aged, 80 and over
4Analysis
5B cells
6Betacoronavirus - immunology
7Biological response modifiers
8Care and treatment
9Case-Control Studies
10Coronavirus Infections - genetics
11Coronavirus Infections - immunology
12Coronavirus Infections - pathology
13Coronaviruses
14COVID-19
15Cytokines
16Cytokines - genetics
17Cytokines - metabolism
18Development and progression
19Female
20Gene expression
21Gene Expression Profiling - methods
22Gene sequencing
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24Genetic aspects
25Health aspects
26Histocompatibility antigen HLA
27Humans
28Immune response
29Immune system
30Immunity, Cellular
31Immunotherapy
32Inflammation
33Interferon
34Killer Cells, Natural - immunology
35Killer Cells, Natural - metabolism
36Leukocytes (mononuclear)
37Leukocytes, Mononuclear - immunology
38Leukocytes, Mononuclear - metabolism
39Leukocytes, Mononuclear - virology
40Lymphocytes
41Lymphocytes T
42Male
43Middle Aged
44Monocytes
45Pandemics
46Peripheral blood mononuclear cells
47Phenotypes
48Physiological aspects
49Pneumonia, Viral - genetics
50Pneumonia, Viral - immunology
51Pneumonia, Viral - pathology
52Reconfiguration
53Respiratory distress syndrome
54Respiratory therapy
55Ribonucleic acid
56RNA
57RNA sequencing
58RNA-Seq - methods
59SARS-CoV-2
60Sequence Analysis, RNA - methods
61Severe acute respiratory syndrome coronavirus 2
62Severity of Illness Index
63Single-Cell Analysis - methods
64T cells
65T-Lymphocytes - immunology
66T-Lymphocytes - metabolism
67Transcriptomics
68Ventilation
69Viral diseases
70Young Adult
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5McKechnie, Julia L
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7Ranganath, Thanmayi
8Vergara, Rosemary
9Hollis, Taylor
10Simpson, Laura J
11Grant, Philip
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titleA single-cell atlas of the peripheral immune response in patients with severe COVID-19
authorWilk, Aaron J ; Rustagi, Arjun ; Zhao, Nancy Q ; Roque, Jonasel ; Martínez-Colón, Giovanny J ; McKechnie, Julia L ; Ivison, Geoffrey T ; Ranganath, Thanmayi ; Vergara, Rosemary ; Hollis, Taylor ; Simpson, Laura J ; Grant, Philip ; Subramanian, Aruna ; Rogers, Angela J ; Blish, Catherine A
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0Acute respiratory distress syndrome
1Adult
2Aged
3Aged, 80 and over
4Analysis
5B cells
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7Biological response modifiers
8Care and treatment
9Case-Control Studies
10Coronavirus Infections - genetics
11Coronavirus Infections - immunology
12Coronavirus Infections - pathology
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14COVID-19
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16Cytokines - genetics
17Cytokines - metabolism
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51Pneumonia, Viral - pathology
52Reconfiguration
53Respiratory distress syndrome
54Respiratory therapy
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56RNA
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58RNA-Seq - methods
59SARS-CoV-2
60Sequence Analysis, RNA - methods
61Severe acute respiratory syndrome coronavirus 2
62Severity of Illness Index
63Single-Cell Analysis - methods
64T cells
65T-Lymphocytes - immunology
66T-Lymphocytes - metabolism
67Transcriptomics
68Ventilation
69Viral diseases
70Young Adult
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atitleA single-cell atlas of the peripheral immune response in patients with severe COVID-19
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notes
0C.A.B. and A.J.R. conceived the study. A.S., P.G., A.J.R., J.R. and A.R. identified eligible patients. A.J.R., A.R. and J.R. enrolled and consented patients. A.J.W., N.Q.Z., A.R., G.J.M.-C., J.L.M., G.T.I., T.R., R.V., T.H. and L.J.S. processed patient samples. A.J.W. and N.Q.Z. performed scRNA-seq and computational analysis. A.J.W., A.R., N.Q.Z. and C.A.B. interpreted data and wrote the manuscript with input from all authors.
1Author contributions
abstractThere is an urgent need to better understand the pathophysiology of Coronavirus disease 2019 (COVID-19), the global pandemic caused by SARS-CoV-2, which has infected more than three million people worldwide . Approximately 20% of patients with COVID-19 develop severe disease and 5% of patients require intensive care . Severe disease has been associated with changes in peripheral immune activity, including increased levels of pro-inflammatory cytokines that may be produced by a subset of inflammatory monocytes , lymphopenia and T cell exhaustion . To elucidate pathways in peripheral immune cells that might lead to immunopathology or protective immunity in severe COVID-19, we applied single-cell RNA sequencing (scRNA-seq) to profile peripheral blood mononuclear cells (PBMCs) from seven patients hospitalized for COVID-19, four of whom had acute respiratory distress syndrome, and six healthy controls. We identify reconfiguration of peripheral immune cell phenotype in COVID-19, including a heterogeneous interferon-stimulated gene signature, HLA class II downregulation and a developing neutrophil population that appears closely related to plasmablasts appearing in patients with acute respiratory failure requiring mechanical ventilation. Importantly, we found that peripheral monocytes and lymphocytes do not express substantial amounts of pro-inflammatory cytokines. Collectively, we provide a cell atlas of the peripheral immune response to severe COVID-19.
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