Reference-based analysis of lung single-cell sequencing reveals a transitional profibrotic macrophage

Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in fibrosis, but the role of specific subgroups in supporting fibrogenesis has not been investigated in vivo. Here, we used single-cell RNA sequencing...

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Published in	Nature immunology Vol. 20; no. 2; pp. 163 - 172
Main Authors	Aran, Dvir, Looney, Agnieszka P., Liu, Leqian, Wu, Esther, Fong, Valerie, Hsu, Austin, Chak, Suzanna, Naikawadi, Ram P., Wolters, Paul J., Abate, Adam R., Butte, Atul J., Bhattacharya, Mallar
Format	Journal Article
Language	English
Published	New York Nature Publishing Group US 01.02.2019 Nature Publishing Group
Subjects	631/1647/2017 631/1647/767/1424 631/250/2504/342/1927 692/699 Alveoli Analysis Animals Antigens, Differentiation, Myelomonocytic - genetics Antigens, Differentiation, Myelomonocytic - immunology Antigens, Differentiation, Myelomonocytic - metabolism Biochemistry Biomedical and Life Sciences Biomedicine Bleomycin Bleomycin - immunology Cells, Cultured Computer applications CX3C Chemokine Receptor 1 - genetics CX3C Chemokine Receptor 1 - immunology CX3C Chemokine Receptor 1 - metabolism CX3CR1 protein Disease Models, Animal Female Fibrosis Gene expression Gene Expression Profiling - methods Genes Genomes Health aspects Heterogeneity Humans Idiopathic Pulmonary Fibrosis - immunology Idiopathic Pulmonary Fibrosis - pathology Immunology Infectious Diseases Lung - cytology Lung - immunology Lung - pathology Lung diseases Macrophage Activation Macrophages Macrophages, Alveolar - immunology Macrophages, Alveolar - metabolism Male Mesenchyme Mice Monocytes Mortality Proteins Pulmonary fibrosis Respiratory tract diseases Ribonucleic acid RNA RNA sequencing Sequence Analysis, RNA - methods Single-Cell Analysis - methods Up-Regulation
Online Access	Get full text
ISSN	1529-2908 1529-2916 1529-2916
DOI	10.1038/s41590-018-0276-y

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Abstract	Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in fibrosis, but the role of specific subgroups in supporting fibrogenesis has not been investigated in vivo. Here, we used single-cell RNA sequencing (scRNA-seq) to characterize the heterogeneity of macrophages in bleomycin-induced lung fibrosis in mice. A novel computational framework for the annotation of scRNA-seq by reference to bulk transcriptomes (SingleR) enabled the subclustering of macrophages and revealed a disease-associated subgroup with a transitional gene expression profile intermediate between monocyte-derived and alveolar macrophages. These CX3CR1 + SiglecF + transitional macrophages localized to the fibrotic niche and had a profibrotic effect in vivo. Human orthologs of genes expressed by the transitional macrophages were upregulated in samples from patients with idiopathic pulmonary fibrosis. Thus, we have identified a pathological subgroup of transitional macrophages that are required for the fibrotic response to injury. Using scRNA-seq analysis, Bhattacharya and colleagues identify a subset of profibrotic lung macrophages that have a gene expression signature intermediate between those of monocytes and alveolar macrophages.
AbstractList	Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in fibrosis, but the role of specific subgroups in supporting fibrogenesis has not been investigated in vivo. Here, we used single-cell RNA sequencing (scRNA-seq) to characterize the heterogeneity of macrophages in bleomycin-induced lung fibrosis in mice. A novel computational framework for the annotation of scRNA-seq by reference to bulk transcriptomes (SingleR) enabled the subclustering of macrophages and revealed a disease-associated subgroup with a transitional gene expression profile intermediate between monocyte-derived and alveolar macrophages. These CX3CR1 SiglecF transitional macrophages localized to the fibrotic niche and had a profibrotic effect in vivo. Human orthologs of genes expressed by the transitional macrophages were upregulated in samples from patients with idiopathic pulmonary fibrosis. Thus, we have identified a pathological subgroup of transitional macrophages that are required for the fibrotic response to injury. Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in fibrosis, but the role of specific subgroups in supporting fibrogenesis has not been investigated in vivo. Here, we used single-cell RNA sequencing (scRNA-seq) to characterize the heterogeneity of macrophages in bleomycin-induced lung fibrosis in mice. A novel computational framework for the annotation of scRNA-seq by reference to bulk transcriptomes (SingleR) enabled the subclustering of macrophages and revealed a disease-associated subgroup with a transitional gene expression profile intermediate between monocyte-derived and alveolar macrophages. These CX3CR1+SiglecF+ transitional macrophages localized to the fibrotic niche and had a profibrotic effect in vivo. Human orthologs of genes expressed by the transitional macrophages were upregulated in samples from patients with idiopathic pulmonary fibrosis. Thus, we have identified a pathological subgroup of transitional macrophages that are required for the fibrotic response to injury.Using scRNA-seq analysis, Bhattacharya and colleagues identify a subset of profibrotic lung macrophages that have a gene expression signature intermediate between those of monocytes and alveolar macrophages. Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in fibrosis, but the role of specific subgroups in supporting fibrogenesis has not been investigated in vivo. Here, we used single-cell RNA sequencing (scRNA-seq) to characterize the heterogeneity of macrophages in bleomycin-induced lung fibrosis in mice. A novel computational framework for the annotation of scRNA-seq by reference to bulk transcriptomes (SingleR) enabled the subclustering of macrophages and revealed a disease-associated subgroup with a transitional gene expression profile intermediate between monocyte-derived and alveolar macrophages. These CX3CR1.sup.+SiglecF.sup.+ transitional macrophages localized to the fibrotic niche and had a profibrotic effect in vivo. Human orthologs of genes expressed by the transitional macrophages were upregulated in samples from patients with idiopathic pulmonary fibrosis. Thus, we have identified a pathological subgroup of transitional macrophages that are required for the fibrotic response to injury. Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in fibrosis, but the role of specific subgroups in supporting fibrogenesis has not been investigated in vivo. Here, we used single-cell RNA sequencing (scRNA-seq) to characterize the heterogeneity of macrophages in bleomycin-induced lung fibrosis in mice. A novel computational framework for the annotation of scRNA-seq by reference to bulk transcriptomes (SingleR) enabled the subclustering of macrophages and revealed a disease-associated subgroup with a transitional gene expression profile intermediate between monocyte-derived and alveolar macrophages. These CX3CR1+SiglecF+ transitional macrophages localized to the fibrotic niche and had a profibrotic effect in vivo. Human orthologs of genes expressed by the transitional macrophages were upregulated in samples from patients with idiopathic pulmonary fibrosis. Thus, we have identified a pathological subgroup of transitional macrophages that are required for the fibrotic response to injury.Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in fibrosis, but the role of specific subgroups in supporting fibrogenesis has not been investigated in vivo. Here, we used single-cell RNA sequencing (scRNA-seq) to characterize the heterogeneity of macrophages in bleomycin-induced lung fibrosis in mice. A novel computational framework for the annotation of scRNA-seq by reference to bulk transcriptomes (SingleR) enabled the subclustering of macrophages and revealed a disease-associated subgroup with a transitional gene expression profile intermediate between monocyte-derived and alveolar macrophages. These CX3CR1+SiglecF+ transitional macrophages localized to the fibrotic niche and had a profibrotic effect in vivo. Human orthologs of genes expressed by the transitional macrophages were upregulated in samples from patients with idiopathic pulmonary fibrosis. Thus, we have identified a pathological subgroup of transitional macrophages that are required for the fibrotic response to injury. Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in fibrosis, but the role of specific subgroups in supporting fibrogenesis has not been investigated in vivo. Here we used single-cell RNA sequencing (scRNA-seq) to characterize the heterogeneity of macrophages in bleomycin-induced lung fibrosis in mice. A novel computational framework for the annotation of scRNA-seq by reference to bulk transcriptomes (SingleR) enabled the subclustering of macrophages and revealed a disease-associated subgroup with a transitional gene expression profile intermediate between monocyte-derived and alveolar macrophages. These CX3CR1 + SiglecF + transitional macrophages localized to the fibrotic niche and had a profibrotic effect in vivo . Human orthologues of genes expressed by the transitional macrophages were upregulated in samples from patients with idiopathic pulmonary fibrosis. Thus, we have identified a pathological subgroup of transitional macrophages that are required for the fibrotic response to injury. Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in fibrosis, but the role of specific subgroups in supporting fibrogenesis has not been investigated in vivo. Here, we used single-cell RNA sequencing (scRNA-seq) to characterize the heterogeneity of macrophages in bleomycin-induced lung fibrosis in mice. A novel computational framework for the annotation of scRNA-seq by reference to bulk transcriptomes (SingleR) enabled the subclustering of macrophages and revealed a disease-associated subgroup with a transitional gene expression profile intermediate between monocyte-derived and alveolar macrophages. These CX3CR1 + SiglecF + transitional macrophages localized to the fibrotic niche and had a profibrotic effect in vivo. Human orthologs of genes expressed by the transitional macrophages were upregulated in samples from patients with idiopathic pulmonary fibrosis. Thus, we have identified a pathological subgroup of transitional macrophages that are required for the fibrotic response to injury. Using scRNA-seq analysis, Bhattacharya and colleagues identify a subset of profibrotic lung macrophages that have a gene expression signature intermediate between those of monocytes and alveolar macrophages. Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in fibrosis, but the role of specific subgroups in supporting fibrogenesis has not been investigated in vivo. Here, we used single-cell RNA sequencing (scRNA-seq) to characterize the heterogeneity of macrophages in bleomycin-induced lung fibrosis in mice. A novel computational framework for the annotation of scRNA-seq by reference to bulk transcriptomes (SingleR) enabled the subclustering of macrophages and revealed a disease-associated subgroup with a transitional gene expression profile intermediate between monocyte-derived and alveolar macrophages. These CX3CR1.sup.+SiglecF.sup.+ transitional macrophages localized to the fibrotic niche and had a profibrotic effect in vivo. Human orthologs of genes expressed by the transitional macrophages were upregulated in samples from patients with idiopathic pulmonary fibrosis. Thus, we have identified a pathological subgroup of transitional macrophages that are required for the fibrotic response to injury. Using scRNA-seq analysis, Bhattacharya and colleagues identify a subset of profibrotic lung macrophages that have a gene expression signature intermediate between those of monocytes and alveolar macrophages.
Audience	Academic
Author	Liu, Leqian Fong, Valerie Wu, Esther Naikawadi, Ram P. Wolters, Paul J. Abate, Adam R. Aran, Dvir Looney, Agnieszka P. Hsu, Austin Chak, Suzanna Bhattacharya, Mallar Butte, Atul J.
AuthorAffiliation	1 Institute for Computational Health Sciences, University of California, San Francisco, CA 94158, USA 6 Chan Zuckerberg Biohub, San Francisco, CA 94158, USA 5 California Institute for Quantitative Biosciences, University of California, San Francisco, CA 94158, USA 2 Division of Pulmonary, Critical Care, Allergy, and Sleep Medicine, Department of Medicine, University of California, San Francisco, CA 94143, USA 3 Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, CA 94158, USA 4 Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158, USA
AuthorAffiliation_xml	– name: 2 Division of Pulmonary, Critical Care, Allergy, and Sleep Medicine, Department of Medicine, University of California, San Francisco, CA 94143, USA – name: 4 Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158, USA – name: 1 Institute for Computational Health Sciences, University of California, San Francisco, CA 94158, USA – name: 6 Chan Zuckerberg Biohub, San Francisco, CA 94158, USA – name: 5 California Institute for Quantitative Biosciences, University of California, San Francisco, CA 94158, USA – name: 3 Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, CA 94158, USA
Author_xml	– sequence: 1 givenname: Dvir orcidid: 0000-0001-6334-5039 surname: Aran fullname: Aran, Dvir organization: Bakar Computational Health Sciences Institute, University of California, San Francisco – sequence: 2 givenname: Agnieszka P. surname: Looney fullname: Looney, Agnieszka P. organization: Division of Pulmonary, Critical Care, Allergy, and Sleep Medicine, Department of Medicine, University of California, San Francisco – sequence: 3 givenname: Leqian surname: Liu fullname: Liu, Leqian organization: Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco – sequence: 4 givenname: Esther surname: Wu fullname: Wu, Esther organization: Division of Pulmonary, Critical Care, Allergy, and Sleep Medicine, Department of Medicine, University of California, San Francisco – sequence: 5 givenname: Valerie surname: Fong fullname: Fong, Valerie organization: Division of Pulmonary, Critical Care, Allergy, and Sleep Medicine, Department of Medicine, University of California, San Francisco – sequence: 6 givenname: Austin surname: Hsu fullname: Hsu, Austin organization: Gladstone Institute of Cardiovascular Disease – sequence: 7 givenname: Suzanna surname: Chak fullname: Chak, Suzanna organization: Division of Pulmonary, Critical Care, Allergy, and Sleep Medicine, Department of Medicine, University of California, San Francisco – sequence: 8 givenname: Ram P. surname: Naikawadi fullname: Naikawadi, Ram P. organization: Division of Pulmonary, Critical Care, Allergy, and Sleep Medicine, Department of Medicine, University of California, San Francisco – sequence: 9 givenname: Paul J. surname: Wolters fullname: Wolters, Paul J. organization: Division of Pulmonary, Critical Care, Allergy, and Sleep Medicine, Department of Medicine, University of California, San Francisco – sequence: 10 givenname: Adam R. surname: Abate fullname: Abate, Adam R. organization: Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, California Institute for Quantitative Biosciences, University of California, San Francisco, Chan Zuckerberg Biohub – sequence: 11 givenname: Atul J. orcidid: 0000-0002-7433-2740 surname: Butte fullname: Butte, Atul J. organization: Bakar Computational Health Sciences Institute, University of California, San Francisco – sequence: 12 givenname: Mallar orcidid: 0000-0002-5439-547X surname: Bhattacharya fullname: Bhattacharya, Mallar email: mallar.bhattacharya@ucsf.edu organization: Division of Pulmonary, Critical Care, Allergy, and Sleep Medicine, Department of Medicine, University of California, San Francisco
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/30643263$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 D.A. developed SingleR and performed computational analysis of single cell data under the guidance of A.J.B.; A.P.L. performed in vivo and in vitro experiments under the guidance of M.B. and with the assistance of E.W. and S.C.; L.L. performed microfluidic capture of single cell transcriptomes, library preparation, and sequencing under the guidance of A.R.A.; V.F., A.H, and E.W. prepared breeding and experimental stocks of genetically modified mice and performed lung injury models under the guidance of M.B.; P.J.W. contributed acquisition, storage, and processing of human samples and, with R.P.N., acquired lung microarray data from mice with telomere dysfunction; D.A. prepared the figures. M.B. conceived of the work, supervised experimental planning and execution, and wrote the manuscript with input D.A., A.P.L, and L.L. Author contributions
ORCID	0000-0001-6334-5039 0000-0002-7433-2740 0000-0002-5439-547X
OpenAccessLink	https://pubmed.ncbi.nlm.nih.gov/PMC6340744
PMID	30643263
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PublicationDate	2019-02-01
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PublicationDate_xml	– month: 02 year: 2019 text: 2019-02-01 day: 01
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PublicationPlace_xml	– name: New York – name: United States
PublicationTitle	Nature immunology
PublicationTitleAbbrev	Nat Immunol
PublicationTitleAlternate	Nat Immunol
PublicationYear	2019
Publisher	Nature Publishing Group US Nature Publishing Group
Publisher_xml	– name: Nature Publishing Group US – name: Nature Publishing Group
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Snippet	Tissue fibrosis is a major cause of mortality that results from the deposition of matrix proteins by an activated mesenchyme. Macrophages accumulate in...
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SubjectTerms	631/1647/2017 631/1647/767/1424 631/250/2504/342/1927 692/699 Alveoli Analysis Animals Antigens, Differentiation, Myelomonocytic - genetics Antigens, Differentiation, Myelomonocytic - immunology Antigens, Differentiation, Myelomonocytic - metabolism Biochemistry Biomedical and Life Sciences Biomedicine Bleomycin Bleomycin - immunology Cells, Cultured Computer applications CX3C Chemokine Receptor 1 - genetics CX3C Chemokine Receptor 1 - immunology CX3C Chemokine Receptor 1 - metabolism CX3CR1 protein Disease Models, Animal Female Fibrosis Gene expression Gene Expression Profiling - methods Genes Genomes Health aspects Heterogeneity Humans Idiopathic Pulmonary Fibrosis - immunology Idiopathic Pulmonary Fibrosis - pathology Immunology Infectious Diseases Lung - cytology Lung - immunology Lung - pathology Lung diseases Macrophage Activation Macrophages Macrophages, Alveolar - immunology Macrophages, Alveolar - metabolism Male Mesenchyme Mice Monocytes Mortality Proteins Pulmonary fibrosis Respiratory tract diseases Ribonucleic acid RNA RNA sequencing Sequence Analysis, RNA - methods Single-Cell Analysis - methods Up-Regulation
Title	Reference-based analysis of lung single-cell sequencing reveals a transitional profibrotic macrophage
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