The immune cell landscape in kidneys of patients with lupus nephritis

Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of disease, we analyzed kidney samples from patients with lupus nephritis and from healthy control subjects using single-cell RNA sequencing. Ou...

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Published in	Nature immunology Vol. 20; no. 7; pp. 902 - 914
Main Authors	Arazi, Arnon, Rao, Deepak A., Berthier, Celine C., Davidson, Anne, Liu, Yanyan, Hoover, Paul J., Chicoine, Adam, Eisenhaure, Thomas M., Jonsson, A. Helena, Li, Shuqiang, Lieb, David J., Zhang, Fan, Slowikowski, Kamil, Browne, Edward P., Noma, Akiko, Sutherby, Danielle, Steelman, Scott, Smilek, Dawn E., Tosta, Patti, Apruzzese, William, Massarotti, Elena, Dall’Era, Maria, Park, Meyeon, Kamen, Diane L., Furie, Richard A., Payan-Schober, Fernanda, Pendergraft, William F., McInnis, Elizabeth A., Buyon, Jill P., Petri, Michelle A., Putterman, Chaim, Kalunian, Kenneth C., Woodle, E. Steve, Lederer, James A., Hildeman, David A., Nusbaum, Chad, Raychaudhuri, Soumya, Kretzler, Matthias, Anolik, Jennifer H., Brenner, Michael B., Wofsy, David, Hacohen, Nir, Diamond, Betty
Format	Journal Article
Language	English
Published	New York Nature Publishing Group US 01.07.2019 Nature Publishing Group
Subjects	631/1647/514/1949 631/250/256 631/250/38 692/699/249/1313 Age Analysis Autoimmune diseases Biomarkers Biomedical and Life Sciences Biomedicine Biopsy Care and treatment Cell activation Chemokine receptors Cluster Analysis Complications and side effects Computational Biology - methods CX3CR1 protein CXCR4 protein Epithelial Cells - metabolism Flow Cytometry Gene expression Gene Expression Profiling Gene Expression Regulation Health aspects Humans Immunohistochemistry Immunology Immunophenotyping Infectious Diseases Inflammation Interferon Interferons - metabolism Kidney - immunology Kidney - metabolism Kidney - pathology Kidneys Leukocytes Leukocytes - immunology Leukocytes - metabolism Lupus Lupus nephritis Lupus Nephritis - genetics Lupus Nephritis - immunology Lupus Nephritis - metabolism Lupus Nephritis - pathology Lymphocytes - immunology Lymphocytes - metabolism Lymphocytes B Lymphocytes T Molecular Sequence Annotation Monocytes Myeloid cells Myeloid Cells - immunology Myeloid Cells - metabolism Natural killer cells Nephritis Resource Ribonucleic acid Risk factors RNA Single-Cell Analysis Systemic lupus erythematosus Transcription Transcriptome Urine
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Abstract	Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of disease, we analyzed kidney samples from patients with lupus nephritis and from healthy control subjects using single-cell RNA sequencing. Our analysis revealed 21 subsets of leukocytes active in disease, including multiple populations of myeloid cells, T cells, natural killer cells and B cells that demonstrated both pro-inflammatory responses and inflammation-resolving responses. We found evidence of local activation of B cells correlated with an age-associated B-cell signature and evidence of progressive stages of monocyte differentiation within the kidney. A clear interferon response was observed in most cells. Two chemokine receptors, CXCR4 and CX3CR1 , were broadly expressed, implying a potentially central role in cell trafficking. Gene expression of immune cells in urine and kidney was highly correlated, which would suggest that urine might serve as a surrogate for kidney biopsies. Much about the kidney-resident immune populations is a black box. Hacohen and colleagues use single cell RNA sequencing of kidney, skin and urine from lupus nephritis patients to describe the transcriptional state of the immune cells present in each compartment.
AbstractList	Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of disease, we analyzed kidney samples from patients with lupus nephritis and from healthy control subjects using single-cell RNA sequencing. Our analysis revealed 21 subsets of leukocytes active in disease, including multiple populations of myeloid cells, T cells, natural killer cells and B cells that demonstrated both pro-inflammatory responses and inflammation-resolving responses. We found evidence of local activation of B cells correlated with an age-associated B-cell signature and evidence of progressive stages of monocyte differentiation within the kidney. A clear interferon response was observed in most cells. Two chemokine receptors, CXCR4 and CX3CR1, were broadly expressed, implying a potentially central role in cell trafficking. Gene expression of immune cells in urine and kidney was highly correlated, which would suggest that urine might serve as a surrogate for kidney biopsies.Much about the kidney-resident immune populations is a black box. Hacohen and colleagues use single cell RNA sequencing of kidney, skin and urine from lupus nephritis patients to describe the transcriptional state of the immune cells present in each compartment. Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of disease, we analyzed kidney samples from patients with lupus nephritis and from healthy control subjects using single-cell RNA sequencing. Our analysis revealed 21 subsets of leukocytes active in disease, including multiple populations of myeloid cells, T cells, natural killer cells and B cells that demonstrated both pro-inflammatory responses and inflammation-resolving responses. We found evidence of local activation of B cells correlated with an age-associated B-cell signature and evidence of progressive stages of monocyte differentiation within the kidney. A clear interferon response was observed in most cells. Two chemokine receptors, CXCR4 and CX3CR1, were broadly expressed, implying a potentially central role in cell trafficking. Gene expression of immune cells in urine and kidney was highly correlated, which would suggest that urine might serve as a surrogate for kidney biopsies. Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of disease, we analyzed kidney samples from patients with lupus nephritis and from healthy control subjects using single-cell RNA sequencing. Our analysis revealed 21 subsets of leukocytes active in disease, including multiple populations of myeloid cells, T cells, natural killer cells and B cells that demonstrated both pro-inflammatory responses and inflammation-resolving responses. We found evidence of local activation of B cells correlated with an age-associated B-cell signature and evidence of progressive stages of monocyte differentiation within the kidney. A clear interferon response was observed in most cells. Two chemokine receptors, CXCR4 and CX3CR1, were broadly expressed, implying a potentially central role in cell trafficking. Gene expression of immune cells in urine and kidney was highly correlated, which would suggest that urine might serve as a surrogate for kidney biopsies.Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of disease, we analyzed kidney samples from patients with lupus nephritis and from healthy control subjects using single-cell RNA sequencing. Our analysis revealed 21 subsets of leukocytes active in disease, including multiple populations of myeloid cells, T cells, natural killer cells and B cells that demonstrated both pro-inflammatory responses and inflammation-resolving responses. We found evidence of local activation of B cells correlated with an age-associated B-cell signature and evidence of progressive stages of monocyte differentiation within the kidney. A clear interferon response was observed in most cells. Two chemokine receptors, CXCR4 and CX3CR1, were broadly expressed, implying a potentially central role in cell trafficking. Gene expression of immune cells in urine and kidney was highly correlated, which would suggest that urine might serve as a surrogate for kidney biopsies. Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of disease, we analyzed kidney samples from patients with lupus nephritis and from healthy control subjects using single-cell RNA sequencing. Our analysis revealed 21 subsets of leukocytes active in disease, including multiple populations of myeloid cells, T cells, natural killer cells and B cells that demonstrated both pro-inflammatory responses and inflammation-resolving responses. We found evidence of local activation of B cells correlated with an age-associated B-cell signature and evidence of progressive stages of monocyte differentiation within the kidney. A clear interferon response was observed in most cells. Two chemokine receptors, CXCR4 and CX3CR1 , were broadly expressed, implying a potentially central role in cell trafficking. Gene expression of immune cells in urine and kidney was highly correlated, which would suggest that urine might serve as a surrogate for kidney biopsies. Much about the kidney-resident immune populations is a black box. Hacohen and colleagues use single cell RNA sequencing of kidney, skin and urine from lupus nephritis patients to describe the transcriptional state of the immune cells present in each compartment. Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of disease, we analyzed kidney samples from patients with lupus nephritis and from healthy control subjects using single-cell RNA sequencing. Our analysis revealed 21 subsets of leukocytes active in disease, including multiple populations of myeloid cells, T cells, natural killer cells and B cells that demonstrated both pro-inflammatory responses and inflammation-resolving responses. We found evidence of local activation of B cells correlated with an age-associated B-cell signature and evidence of progressive stages of monocyte differentiation within the kidney. A clear interferon response was observed in most cells. Two chemokine receptors, CXCR4 and CX3CR1, were broadly expressed, implying a potentially central role in cell trafficking. Gene expression of immune cells in urine and kidney was highly correlated, which would suggest that urine might serve as a surrogate for kidney biopsies. The immune cell landscape in kidneys of patients with lupus nephritis. Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of disease, we analyzed kidney samples from patients with lupus nephritis and from healthy control subjects using single-cell RNA sequencing. Our analysis revealed 21 subsets of leukocytes active in disease, including multiple populations of myeloid cells, T cells, natural killer cells and B cells that demonstrated both pro-inflammatory responses and inflammation-resolving responses. We found evidence of local activation of B cells correlated with an age-associated B-cell signature and evidence of progressive stages of monocyte differentiation within the kidney. A clear interferon response was observed in most cells. Two chemokine receptors, CXCR4 and CX3CR1 , were broadly expressed, implying a potentially central role in cell trafficking. Gene expression of immune cells in urine and kidney was highly correlated, which would suggest that urine might serve as a surrogate for kidney biopsies.
Audience	Academic
Author	Browne, Edward P. Park, Meyeon Payan-Schober, Fernanda Davidson, Anne Diamond, Betty McInnis, Elizabeth A. Kamen, Diane L. Hoover, Paul J. Woodle, E. Steve Anolik, Jennifer H. Putterman, Chaim Nusbaum, Chad Slowikowski, Kamil Steelman, Scott Noma, Akiko Apruzzese, William Petri, Michelle A. Raychaudhuri, Soumya Chicoine, Adam Smilek, Dawn E. Brenner, Michael B. Kretzler, Matthias Arazi, Arnon Lieb, David J. Wofsy, David Eisenhaure, Thomas M. Furie, Richard A. Kalunian, Kenneth C. Li, Shuqiang Buyon, Jill P. Sutherby, Danielle Hacohen, Nir Hildeman, David A. Berthier, Celine C. Pendergraft, William F. Dall’Era, Maria Zhang, Fan Rao, Deepak A. Jonsson, A. Helena Massarotti, Elena Tosta, Patti Liu, Yanyan Lederer, James A.
AuthorAffiliation	17 Department of Medicine, Division of Rheumatology, New York University School of Medicine, New York, New-York, USA 3 Internal Medicine, Department of Nephrology, University of Michigan, Ann Arbor, Michigan, USA 7 Cellarity, Inc., Cambridge, Massachusetts, USA 18 Division of Rheumatology, Johns Hopkins University, Baltimore, Maryland, USA 21 Division of Transplantation, Department of Surgery, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA 2 Division of Rheumatology, Immunology, Allergy, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston Massachusetts, USA 23 Department of Pediatrics, University of Cincinnati, Cincinnati, Ohio, USA 5 UNC HIV Cure Center and Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA 9 Immune Tolerance Network, University of California San Francisco, San Francisco, California, USA 10 Rheumatology Division, University of California San Francisco, San Francisco, Califo
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors contributed equally: Arnon Arazi, Deepak A. Rao and Celine C. Berthier. AUTHORS CONTRIBUTIONS A.A., D.A.R, A.D., P.J.H., A.H.J. and D.J.L. analyzed the data; D.A.R., C.C.B., T.M.E., E.P.B., J.A.L. and D.A.H. developed the sample collection and processing protocols; D.A.R., Y.L., P.J.H., A.C., A.N., D.S. and S.S. processed the samples; S.L., D.J.L., A.N., D.S. and S.S. developed the scRNA-seq library preparation protocol; F.Z. and K.S. developed the web-based browser of the data; D.E.S., P.T., E.M., M.D.E., M.P., D.L.K., R.A.F., F.P.S., W.F.P., E.A.M., J.P.B., M.A.P., C.P., K.C.K., E.S.W., D.A.H., D.W. and J.H.A. acquired samples; A.A., D.A.R., C.C.B., A.D., W.A., J.A.L., D.A.H., C.N., D.W., M.K., J.H.A., M.B.B., N.H. and B.D. designed the study; A.D., W.A., D.A.H., C.N., S.R., D.W., M.K., J.H.A., M.B.B., N.H. and B.D. supervised the work; A.A., D.A.R., C.C.B., A.D., P.J.H., N.H. and B.D. wrote the manuscript.
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Snippet	Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of... Lupus nephritis is a potentially fatal autoimmune disease for which the current treatment is ineffective and often toxic. To develop mechanistic hypotheses of...
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SubjectTerms	631/1647/514/1949 631/250/256 631/250/38 692/699/249/1313 Age Analysis Autoimmune diseases Biomarkers Biomedical and Life Sciences Biomedicine Biopsy Care and treatment Cell activation Chemokine receptors Cluster Analysis Complications and side effects Computational Biology - methods CX3CR1 protein CXCR4 protein Epithelial Cells - metabolism Flow Cytometry Gene expression Gene Expression Profiling Gene Expression Regulation Health aspects Humans Immunohistochemistry Immunology Immunophenotyping Infectious Diseases Inflammation Interferon Interferons - metabolism Kidney - immunology Kidney - metabolism Kidney - pathology Kidneys Leukocytes Leukocytes - immunology Leukocytes - metabolism Lupus Lupus nephritis Lupus Nephritis - genetics Lupus Nephritis - immunology Lupus Nephritis - metabolism Lupus Nephritis - pathology Lymphocytes - immunology Lymphocytes - metabolism Lymphocytes B Lymphocytes T Molecular Sequence Annotation Monocytes Myeloid cells Myeloid Cells - immunology Myeloid Cells - metabolism Natural killer cells Nephritis Resource Ribonucleic acid Risk factors RNA Single-Cell Analysis Systemic lupus erythematosus Transcription Transcriptome Urine
Title	The immune cell landscape in kidneys of patients with lupus nephritis
URI	https://link.springer.com/article/10.1038/s41590-019-0398-x https://www.ncbi.nlm.nih.gov/pubmed/31209404 https://www.proquest.com/docview/2242773502 https://www.proquest.com/docview/2475009006 https://www.proquest.com/docview/2242828163 https://pubmed.ncbi.nlm.nih.gov/PMC6726437
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