An immune-cell signature of bacterial sepsis

Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene-expression studies have defined sepsis-associated molecular signatures, but have not resolved changes in transcriptional states of specific cell types. Here, we...

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Published inNature medicine Vol. 26; no. 3; pp. 333 - 340
Main Authors Reyes, Miguel, Filbin, Michael R., Bhattacharyya, Roby P., Billman, Kianna, Eisenhaure, Thomas, Hung, Deborah T., Levy, Bruce D., Baron, Rebecca M., Blainey, Paul C., Goldberg, Marcia B., Hacohen, Nir
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.03.2020
Nature Publishing Group
Subjects
631/1647/514/1949
631/250/2504/342
692/308/53/2421
692/420/256/1980
692/699/255/1318
Bacteria
Bacteria - immunology
Bacterial diseases
Bacterial infections
Biomarkers - blood
Biomedical and Life Sciences
Biomedicine
Blood
Bone marrow
Bone Marrow Cells - metabolism
Cancer Research
CD14 antigen
Clustering
Cohort Studies
Dendritic cells
Disease control
Epigenesis, Genetic
Etiology
Gene expression
Gene Expression Profiling
Gene sequencing
Genetic aspects
Genomics
Geographical locations
Humans
Immune response
Immune system
Infectious Diseases
Letter
Leukocytes (mononuclear)
Metabolic Diseases
Molecular Medicine
Monocytes
Monocytes - metabolism
Neurosciences
Patient outcomes
Peripheral blood mononuclear cells
Phenotypes
Reproducibility of Results
Ribonucleic acid
RNA
ROC Curve
Sepsis
Sepsis - blood
Sepsis - genetics
Sepsis - immunology
Sepsis - microbiology
Sequence Analysis, RNA
Signatures
Surface markers
Transcription
Transcription, Genetic
Transcriptomics
United States
Online AccessGet full text

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Abstract Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene-expression studies have defined sepsis-associated molecular signatures, but have not resolved changes in transcriptional states of specific cell types. Here, we used single-cell RNA-sequencing to profile the blood of people with sepsis ( n  = 29) across three clinical cohorts with corresponding controls ( n   =  36). We profiled total peripheral blood mononuclear cells (PBMCs, 106,545 cells) and dendritic cells (19,806 cells) across all subjects and, on the basis of clustering of their gene-expression profiles, defined 16 immune-cell states. We identified a unique CD14 + monocyte state that is expanded in people with sepsis and validated its power in distinguishing these individuals from controls using public transcriptomic data from subjects with different disease etiologies and from multiple geographic locations (18 cohorts, n   =  1,467 subjects). We identified a panel of surface markers for isolation and quantification of the monocyte state and characterized its epigenomic and functional phenotypes, and propose a model for its induction from human bone marrow. This study demonstrates the utility of single-cell genomics in discovering disease-associated cytologic signatures and provides insight into the cellular basis of immune dysregulation in bacterial sepsis. Single-cell transcriptomic analysis identifies a distinct gene signature associated with peripheral monocyte populations that distinguishes people with sepsis from those with sterile inflammation and uninfected controls.
AbstractList Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene-expression studies have defined sepsis-associated molecular signatures, but have not resolved changes in transcriptional states of specific cell types. Here, we used single-cell RNA-sequencing to profile the blood of people with sepsis (n = 29) across three clinical cohorts with corresponding controls (n = 36). We profiled total peripheral blood mononuclear cells (PBMCs, 106,545 cells) and dendritic cells (19,806 cells) across all subjects and, on the basis of clustering of their gene-expression profiles, defined 16 immune-cell states. We identified a unique CD14+ monocyte state that is expanded in people with sepsis and validated its power in distinguishing these individuals from controls using public transcriptomic data from subjects with different disease etiologies and from multiple geographic locations (18 cohorts, n = 1,467 subjects). We identified a panel of surface markers for isolation and quantification of the monocyte state and characterized its epigenomic and functional phenotypes, and propose a model for its induction from human bone marrow. This study demonstrates the utility of single-cell genomics in discovering disease-associated cytologic signatures and provides insight into the cellular basis of immune dysregulation in bacterial sepsis.Single-cell transcriptomic analysis identifies a distinct gene signature associated with peripheral monocyte populations that distinguishes people with sepsis from those with sterile inflammation and uninfected controls.
Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene-expression studies have defined sepsis-associated molecular signatures, but have not resolved changes in transcriptional states of specific cell types. Here, we used single-cell RNA-sequencing to profile the blood of people with sepsis (n = 29) across three clinical cohorts with corresponding controls (n = 36). We profiled total peripheral blood mononuclear cells (PBMCs, 106,545 cells) and dendritic cells (19,806 cells) across all subjects and, on the basis of clustering of their gene-expression profiles, defined 16 immune-cell states. We identified a unique CD14.sup.+ monocyte state that is expanded in people with sepsis and validated its power in distinguishing these individuals from controls using public transcriptomic data from subjects with different disease etiologies and from multiple geographic locations (18 cohorts, n = 1,467 subjects). We identified a panel of surface markers for isolation and quantification of the monocyte state and characterized its epigenomic and functional phenotypes, and propose a model for its induction from human bone marrow. This study demonstrates the utility of single-cell genomics in discovering disease-associated cytologic signatures and provides insight into the cellular basis of immune dysregulation in bacterial sepsis.
Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene-expression studies have defined sepsis-associated molecular signatures, but have not resolved changes in transcriptional states of specific cell types. Here, we used single-cell RNA-sequencing to profile the blood of people with sepsis (n = 29) across three clinical cohorts with corresponding controls (n = 36). We profiled total peripheral blood mononuclear cells (PBMCs, 106,545 cells) and dendritic cells (19,806 cells) across all subjects and, on the basis of clustering of their gene-expression profiles, defined 16 immune-cell states. We identified a unique CD14 monocyte state that is expanded in people with sepsis and validated its power in distinguishing these individuals from controls using public transcriptomic data from subjects with different disease etiologies and from multiple geographic locations (18 cohorts, n = 1,467 subjects). We identified a panel of surface markers for isolation and quantification of the monocyte state and characterized its epigenomic and functional phenotypes, and propose a model for its induction from human bone marrow. This study demonstrates the utility of single-cell genomics in discovering disease-associated cytologic signatures and provides insight into the cellular basis of immune dysregulation in bacterial sepsis.
Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene-expression studies have defined sepsis-associated molecular signatures, but have not resolved changes in transcriptional states of specific cell types. Here, we used single-cell RNA-sequencing to profile the blood of people with sepsis (n = 29) across three clinical cohorts with corresponding controls (n = 36). We profiled total peripheral blood mononuclear cells (PBMCs, 106,545 cells) and dendritic cells (19,806 cells) across all subjects and, on the basis of clustering of their gene-expression profiles, defined 16 immune-cell states. We identified a unique CD14.sup.+ monocyte state that is expanded in people with sepsis and validated its power in distinguishing these individuals from controls using public transcriptomic data from subjects with different disease etiologies and from multiple geographic locations (18 cohorts, n = 1,467 subjects). We identified a panel of surface markers for isolation and quantification of the monocyte state and characterized its epigenomic and functional phenotypes, and propose a model for its induction from human bone marrow. This study demonstrates the utility of single-cell genomics in discovering disease-associated cytologic signatures and provides insight into the cellular basis of immune dysregulation in bacterial sepsis. Single-cell transcriptomic analysis identifies a distinct gene signature associated with peripheral monocyte populations that distinguishes people with sepsis from those with sterile inflammation and uninfected controls.
Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene-expression studies have defined sepsis-associated molecular signatures, but have not resolved changes in transcriptional states of specific cell types. Here, we used single-cell RNA-sequencing to profile the blood of people with sepsis ( n  = 29) across three clinical cohorts with corresponding controls ( n   =  36). We profiled total peripheral blood mononuclear cells (PBMCs, 106,545 cells) and dendritic cells (19,806 cells) across all subjects and, on the basis of clustering of their gene-expression profiles, defined 16 immune-cell states. We identified a unique CD14 + monocyte state that is expanded in people with sepsis and validated its power in distinguishing these individuals from controls using public transcriptomic data from subjects with different disease etiologies and from multiple geographic locations (18 cohorts, n   =  1,467 subjects). We identified a panel of surface markers for isolation and quantification of the monocyte state and characterized its epigenomic and functional phenotypes, and propose a model for its induction from human bone marrow. This study demonstrates the utility of single-cell genomics in discovering disease-associated cytologic signatures and provides insight into the cellular basis of immune dysregulation in bacterial sepsis. Single-cell transcriptomic analysis identifies a distinct gene signature associated with peripheral monocyte populations that distinguishes people with sepsis from those with sterile inflammation and uninfected controls.
Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene expression studies have defined sepsis-associated molecular signatures but did not resolve changes in transcriptional states of specific cell types. Here, we used single-cell RNA sequencing to profile the blood of patients with sepsis ( n = 29) across three clinical cohorts with corresponding controls ( n =36). We profiled total peripheral blood mononuclear cells (PBMCs, 106,545 cells) and dendritic cells (19,806 cells) across all patients and, based on clustering of their gene expression profiles, defined 16 immune cell states. We identified a unique CD14+ monocyte state that is expanded in septic patients and validated its power in discriminating septic patients from controls using public transcriptomic data from patients of different disease etiologies and multiple geographic locations (18 cohorts, n = 1,213 patients). We identified a panel of surface markers for isolation and quantification of the monocyte state, characterized its epigenomic and functional phenotypes, and propose a model for its induction from human bone marrow. This study demonstrates the utility of single cell genomics in discovering disease-associated cytologic signatures and provides insight into the cellular basis of immune dysregulation in bacterial sepsis.
Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene-expression studies have defined sepsis-associated molecular signatures, but have not resolved changes in transcriptional states of specific cell types. Here, we used single-cell RNA-sequencing to profile the blood of people with sepsis (n = 29) across three clinical cohorts with corresponding controls (n = 36). We profiled total peripheral blood mononuclear cells (PBMCs, 106,545 cells) and dendritic cells (19,806 cells) across all subjects and, on the basis of clustering of their gene-expression profiles, defined 16 immune-cell states. We identified a unique CD14+ monocyte state that is expanded in people with sepsis and validated its power in distinguishing these individuals from controls using public transcriptomic data from subjects with different disease etiologies and from multiple geographic locations (18 cohorts, n = 1,467 subjects). We identified a panel of surface markers for isolation and quantification of the monocyte state and characterized its epigenomic and functional phenotypes, and propose a model for its induction from human bone marrow. This study demonstrates the utility of single-cell genomics in discovering disease-associated cytologic signatures and provides insight into the cellular basis of immune dysregulation in bacterial sepsis.
Audience Academic
Author Filbin, Michael R.
Hung, Deborah T.
Blainey, Paul C.
Baron, Rebecca M.
Goldberg, Marcia B.
Hacohen, Nir
Eisenhaure, Thomas
Bhattacharyya, Roby P.
Billman, Kianna
Levy, Bruce D.
Reyes, Miguel
AuthorAffiliation 6 Center for Cancer Research, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA
2 Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA
4 Center for Bacterial Pathogenesis, Division of Infectious Diseases, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA
3 Department of Emergency Medicine, Massachusetts General Hospital and Harvard Medical School, Boston,MA, USA
5 Division of Pulmonary and Critical Care Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA
1 Broad Institute of MIT and Harvard, Cambridge, MA, USA
AuthorAffiliation_xml – name: 1 Broad Institute of MIT and Harvard, Cambridge, MA, USA
– name: 4 Center for Bacterial Pathogenesis, Division of Infectious Diseases, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA
– name: 2 Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA
– name: 6 Center for Cancer Research, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA
– name: 3 Department of Emergency Medicine, Massachusetts General Hospital and Harvard Medical School, Boston,MA, USA
– name: 5 Division of Pulmonary and Critical Care Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA
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  organization: Broad Institute of MIT and Harvard, Department of Biological Engineering, Massachusetts Institute of Technology
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  fullname: Filbin, Michael R.
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  email: pblainey@broadinstitute.org
  organization: Broad Institute of MIT and Harvard, Department of Biological Engineering, Massachusetts Institute of Technology
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  givenname: Marcia B.
  orcidid: 0000-0003-4266-9733
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/32066974$$D View this record in MEDLINE/PubMed
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AUTHOR CONTRIBUTIONS
These authors contributed equally to this work.
M.R. designed and performed experiments, and analyzed the data with clinical input from M.R.F., R.P.B., R.M.B., and M.B.G.. K.B. and T.E. assisted in sorting and sample processing for single-cell RNA sequencing. M.R.F., R.P.B., M.B.G. designed the MGH clinical cohorts and supervised patient enrollment, specimen collection, and performed clinical adjudications. D.T.H., B.D.L., and R.M.B. supervised patient enrollment and specimen collection at the BWH. M.B.G., M.R.F., N.H., P.C.B., D.T.H., and R.P.B. conceived the study. M.B.G., N.H., and P.C.B. supervised the study. M.R., P.C.B, and N.H. prepared the manuscript; all authors reviewed and edited the final manuscript.
ORCID 0000-0002-4889-8783
0000-0001-6955-5088
0000-0002-2349-2656
0000-0003-4266-9733
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Snippet Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene-expression studies...
Dysregulation of the immune response to bacterial infection can lead to sepsis, a condition with high mortality. Multiple whole-blood gene expression studies...
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SubjectTerms 631/1647/514/1949
631/250/2504/342
692/308/53/2421
692/420/256/1980
692/699/255/1318
Bacteria
Bacteria - immunology
Bacterial diseases
Bacterial infections
Biomarkers - blood
Biomedical and Life Sciences
Biomedicine
Blood
Bone marrow
Bone Marrow Cells - metabolism
Cancer Research
CD14 antigen
Clustering
Cohort Studies
Dendritic cells
Disease control
Epigenesis, Genetic
Etiology
Gene expression
Gene Expression Profiling
Gene sequencing
Genetic aspects
Genomics
Geographical locations
Humans
Immune response
Immune system
Infectious Diseases
Letter
Leukocytes (mononuclear)
Metabolic Diseases
Molecular Medicine
Monocytes
Monocytes - metabolism
Neurosciences
Patient outcomes
Peripheral blood mononuclear cells
Phenotypes
Reproducibility of Results
Ribonucleic acid
RNA
ROC Curve
Sepsis
Sepsis - blood
Sepsis - genetics
Sepsis - immunology
Sepsis - microbiology
Sequence Analysis, RNA
Signatures
Surface markers
Transcription
Transcription, Genetic
Transcriptomics
Title An immune-cell signature of bacterial sepsis
URI https://link.springer.com/article/10.1038/s41591-020-0752-4
https://www.ncbi.nlm.nih.gov/pubmed/32066974
https://www.proquest.com/docview/2376207291
https://www.proquest.com/docview/2357459067
https://pubmed.ncbi.nlm.nih.gov/PMC7235950
Volume 26
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