CD127 imprints functional heterogeneity to diversify monocyte responses in inflammatory diseases

Inflammatory monocytes are key mediators of acute and chronic inflammation; yet, their functional diversity remains obscure. Single-cell transcriptome analyses of human inflammatory monocytes from COVID-19 and rheumatoid arthritis patients revealed a subset of cells positive for CD127, an IL-7 recep...

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Published inThe Journal of experimental medicine Vol. 219; no. 2
Main Authors Zhang, Bin, Zhang, Yuan, Xiong, Lei, Li, Yuzhe, Zhang, Yunliang, Zhao, Jiuliang, Jiang, Hui, Li, Can, Liu, Yunqi, Liu, Xindong, Liu, Haofei, Ping, Yi-Fang, Zhang, Qiangfeng Cliff, Zhang, Zheng, Bian, Xiu-Wu, Zhao, Yan, Hu, Xiaoyu
Format Journal Article
LanguageEnglish
Published United States Rockefeller University Press 07.02.2022
Subjects
Arthritis, Rheumatoid - immunology
COVID-19 - immunology
Epigenesis, Genetic - immunology
Female
Humans
Inflammation - immunology
Innate Immunity and Inflammation
Interleukin-7 - immunology
Interleukin-7 Receptor alpha Subunit - immunology
Male
Monocytes - immunology
SARS-CoV-2 - immunology
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Abstract Inflammatory monocytes are key mediators of acute and chronic inflammation; yet, their functional diversity remains obscure. Single-cell transcriptome analyses of human inflammatory monocytes from COVID-19 and rheumatoid arthritis patients revealed a subset of cells positive for CD127, an IL-7 receptor subunit, and such positivity rendered otherwise inert monocytes responsive to IL-7. Active IL-7 signaling engaged epigenetically coupled, STAT5-coordinated transcriptional programs to restrain inflammatory gene expression, resulting in inverse correlation between CD127 expression and inflammatory phenotypes in a seemingly homogeneous monocyte population. In COVID-19 and rheumatoid arthritis, CD127 marked a subset of monocytes/macrophages that retained hypoinflammatory phenotypes within the highly inflammatory tissue environments. Furthermore, generation of an integrated expression atlas revealed unified features of human inflammatory monocytes across different diseases and different tissues, exemplified by those of the CD127high subset. Overall, we phenotypically and molecularly characterized CD127-imprinted functional heterogeneity of human inflammatory monocytes with direct relevance for inflammatory diseases.
AbstractList Inflammatory monocytes are key mediators of acute and chronic inflammation; yet, their functional diversity remains obscure. Single-cell transcriptome analyses of human inflammatory monocytes from COVID-19 and rheumatoid arthritis patients revealed a subset of cells positive for CD127, an IL-7 receptor subunit, and such positivity rendered otherwise inert monocytes responsive to IL-7. Active IL-7 signaling engaged epigenetically coupled, STAT5-coordinated transcriptional programs to restrain inflammatory gene expression, resulting in inverse correlation between CD127 expression and inflammatory phenotypes in a seemingly homogeneous monocyte population. In COVID-19 and rheumatoid arthritis, CD127 marked a subset of monocytes/macrophages that retained hypoinflammatory phenotypes within the highly inflammatory tissue environments. Furthermore, generation of an integrated expression atlas revealed unified features of human inflammatory monocytes across different diseases and different tissues, exemplified by those of the CD127high subset. Overall, we phenotypically and molecularly characterized CD127-imprinted functional heterogeneity of human inflammatory monocytes with direct relevance for inflammatory diseases.
Inflammatory monocytes are key mediators of acute and chronic inflammation; yet, their functional diversity remains obscure. Single-cell transcriptome analyses of human inflammatory monocytes from COVID-19 and rheumatoid arthritis patients revealed a subset of cells positive for CD127, an IL-7 receptor subunit, and such positivity rendered otherwise inert monocytes responsive to IL-7. Active IL-7 signaling engaged epigenetically coupled, STAT5-coordinated transcriptional programs to restrain inflammatory gene expression, resulting in inverse correlation between CD127 expression and inflammatory phenotypes in a seemingly homogeneous monocyte population. In COVID-19 and rheumatoid arthritis, CD127 marked a subset of monocytes/macrophages that retained hypoinflammatory phenotypes within the highly inflammatory tissue environments. Furthermore, generation of an integrated expression atlas revealed unified features of human inflammatory monocytes across different diseases and different tissues, exemplified by those of the CD127high subset. Overall, we phenotypically and molecularly characterized CD127-imprinted functional heterogeneity of human inflammatory monocytes with direct relevance for inflammatory diseases.Inflammatory monocytes are key mediators of acute and chronic inflammation; yet, their functional diversity remains obscure. Single-cell transcriptome analyses of human inflammatory monocytes from COVID-19 and rheumatoid arthritis patients revealed a subset of cells positive for CD127, an IL-7 receptor subunit, and such positivity rendered otherwise inert monocytes responsive to IL-7. Active IL-7 signaling engaged epigenetically coupled, STAT5-coordinated transcriptional programs to restrain inflammatory gene expression, resulting in inverse correlation between CD127 expression and inflammatory phenotypes in a seemingly homogeneous monocyte population. In COVID-19 and rheumatoid arthritis, CD127 marked a subset of monocytes/macrophages that retained hypoinflammatory phenotypes within the highly inflammatory tissue environments. Furthermore, generation of an integrated expression atlas revealed unified features of human inflammatory monocytes across different diseases and different tissues, exemplified by those of the CD127high subset. Overall, we phenotypically and molecularly characterized CD127-imprinted functional heterogeneity of human inflammatory monocytes with direct relevance for inflammatory diseases.
Zhang et al. analyzed human monocytes in acute and chronic inflammatory disease conditions with multiomics approaches and identified a subset of CD127 + hypoinflammatory monocytes within the inflammatory environment, uncovering functional heterogeneity of human inflammatory monocytes imprinted by CD127. Inflammatory monocytes are key mediators of acute and chronic inflammation; yet, their functional diversity remains obscure. Single-cell transcriptome analyses of human inflammatory monocytes from COVID-19 and rheumatoid arthritis patients revealed a subset of cells positive for CD127, an IL-7 receptor subunit, and such positivity rendered otherwise inert monocytes responsive to IL-7. Active IL-7 signaling engaged epigenetically coupled, STAT5-coordinated transcriptional programs to restrain inflammatory gene expression, resulting in inverse correlation between CD127 expression and inflammatory phenotypes in a seemingly homogeneous monocyte population. In COVID-19 and rheumatoid arthritis, CD127 marked a subset of monocytes/macrophages that retained hypoinflammatory phenotypes within the highly inflammatory tissue environments. Furthermore, generation of an integrated expression atlas revealed unified features of human inflammatory monocytes across different diseases and different tissues, exemplified by those of the CD127 high subset. Overall, we phenotypically and molecularly characterized CD127-imprinted functional heterogeneity of human inflammatory monocytes with direct relevance for inflammatory diseases.
Author Jiang, Hui
Liu, Xindong
Zhang, Yunliang
Liu, Yunqi
Zhang, Qiangfeng Cliff
Liu, Haofei
Ping, Yi-Fang
Zhang, Zheng
Hu, Xiaoyu
Bian, Xiu-Wu
Zhang, Yuan
Zhang, Bin
Xiong, Lei
Li, Yuzhe
Li, Can
Zhao, Yan
Zhao, Jiuliang
AuthorAffiliation 5 Department of Rheumatology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, National Clinical Research Center for Dermatologic and Immunological Diseases, Beijing, China
10 Center for Human Disease Immuno-monitoring, Beijing Friendship Hospital, Beijing, China
9 The Second Affiliated Hospital, School of Medicine, Southern University of Science and Technology, Shenzhen, China
2 Beijing Key Laboratory for Immunological Research on Chronic Diseases, Beijing, China
4 Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, China
6 Institute of Pathology, Southwest Hospital, Third Military Medical University (Army Medical University), Chongqing, China
8 Institute for Hepatology, National Clinical Research Center for Infectious Disease, Shenzhen Third People’s Hospital, Shenzhen, China
1 Institute for Immunology and School of Medicine, Tsinghua University, Beijing, China
7 Tsinghua-Peking Center for Life Sciences, Beij
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DocumentTitleAlternate CD127 imprints hypoinflammatory human monocytes
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content type line 23
B. Zhang and Yuan Zhang contributed equally to this paper.
Yuan Zhang’s present address is Department of Pathology, Immunology and Laboratory Medicine, University of Florida, Gainesville, FL.
Yunliang Zhang’s present address is Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD.
Disclosures: The authors declare no competing interests exist.
Can Li’s present address is Department of Cardiology, National Center for Cardiovascular Diseases, Fuwai Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China.
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Snippet Inflammatory monocytes are key mediators of acute and chronic inflammation; yet, their functional diversity remains obscure. Single-cell transcriptome analyses...
Zhang et al. analyzed human monocytes in acute and chronic inflammatory disease conditions with multiomics approaches and identified a subset of CD127 +...
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SubjectTerms Arthritis, Rheumatoid - immunology
COVID-19 - immunology
Epigenesis, Genetic - immunology
Female
Humans
Inflammation - immunology
Innate Immunity and Inflammation
Interleukin-7 - immunology
Interleukin-7 Receptor alpha Subunit - immunology
Male
Monocytes - immunology
SARS-CoV-2 - immunology
Title CD127 imprints functional heterogeneity to diversify monocyte responses in inflammatory diseases
URI https://www.ncbi.nlm.nih.gov/pubmed/35015026
https://www.proquest.com/docview/2618915865
https://pubmed.ncbi.nlm.nih.gov/PMC8757045
Volume 219
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