Tubular cell and keratinocyte single-cell transcriptomics applied to lupus nephritis reveal type I IFN and fibrosis relevant pathways
The molecular and cellular processes that lead to renal damage and to the heterogeneity of lupus nephritis (LN) are not well understood. We applied single-cell RNA sequencing (scRNA-seq) to renal biopsies from patients with LN and evaluated skin biopsies as a potential source of diagnostic and progn...
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| Published in | Nature immunology Vol. 20; no. 7; pp. 915 - 927 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.07.2019
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The molecular and cellular processes that lead to renal damage and to the heterogeneity of lupus nephritis (LN) are not well understood. We applied single-cell RNA sequencing (scRNA-seq) to renal biopsies from patients with LN and evaluated skin biopsies as a potential source of diagnostic and prognostic markers of renal disease. Type I interferon (IFN)-response signatures in tubular cells and keratinocytes distinguished patients with LN from healthy control subjects. Moreover, a high IFN-response signature and fibrotic signature in tubular cells were each associated with failure to respond to treatment. Analysis of tubular cells from patients with proliferative, membranous and mixed LN indicated pathways relevant to inflammation and fibrosis, which offer insight into their histologic differences. In summary, we applied scRNA-seq to LN to deconstruct its heterogeneity and identify novel targets for personalized approaches to therapy.
Nephritis is a major cause of lupus morbidity. Putterman and colleagues use single-cell RNA sequencing on human renal and skin biopsies to describe the expression landscape associated with lupus nephritis. |
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| AbstractList | The molecular and cellular processes that lead to renal damage and to the heterogeneity of lupus nephritis (LN) are not well understood. We applied single-cell RNA sequencing (scRNA-seq) to renal biopsies from patients with LN and evaluated skin biopsies as a potential source of diagnostic and prognostic markers of renal disease. Type I interferon (IFN)-response signatures in tubular cells and keratinocytes distinguished patients with LN from healthy control subjects. Moreover, a high IFN-response signature and fibrotic signature in tubular cells were each associated with failure to respond to treatment. Analysis of tubular cells from patients with proliferative, membranous and mixed LN indicated pathways relevant to inflammation and fibrosis, which offer insight into their histologic differences. In summary, we applied scRNA-seq to LN to deconstruct its heterogeneity and identify novel targets for personalized approaches to therapy.Nephritis is a major cause of lupus morbidity. Putterman and colleagues use single-cell RNA sequencing on human renal and skin biopsies to describe the expression landscape associated with lupus nephritis. The molecular and cellular processes that lead to renal damage and to the heterogeneity of lupus nephritis (LN) are not well understood. We applied single-cell RNA sequencing (scRNA-seq) to renal biopsies from patients with LN and evaluated skin biopsies as a potential source of diagnostic and prognostic markers of renal disease. Type I interferon (IFN)-response signatures in tubular cells and keratinocytes distinguished patients with LN from healthy control subjects. Moreover, a high IFN-response signature and fibrotic signature in tubular cells were each associated with failure to respond to treatment. Analysis of tubular cells from patients with proliferative, membranous and mixed LN indicated pathways relevant to inflammation and fibrosis, which offer insight into their histologic differences. In summary, we applied scRNA-seq to LN to deconstruct its heterogeneity and identify novel targets for personalized approaches to therapy.The molecular and cellular processes that lead to renal damage and to the heterogeneity of lupus nephritis (LN) are not well understood. We applied single-cell RNA sequencing (scRNA-seq) to renal biopsies from patients with LN and evaluated skin biopsies as a potential source of diagnostic and prognostic markers of renal disease. Type I interferon (IFN)-response signatures in tubular cells and keratinocytes distinguished patients with LN from healthy control subjects. Moreover, a high IFN-response signature and fibrotic signature in tubular cells were each associated with failure to respond to treatment. Analysis of tubular cells from patients with proliferative, membranous and mixed LN indicated pathways relevant to inflammation and fibrosis, which offer insight into their histologic differences. In summary, we applied scRNA-seq to LN to deconstruct its heterogeneity and identify novel targets for personalized approaches to therapy. The molecular and cellular processes that lead to renal damage and to the heterogeneity of lupus nephritis (LN) are not well understood. We applied single-cell RNA sequencing (scRNA-seq) to renal biopsies from patients with LN and evaluated skin biopsies as a potential source of diagnostic and prognostic markers of renal disease. Type I interferon (IFN)-response signatures in tubular cells and keratinocytes distinguished patients with LN from healthy control subjects. Moreover, a high IFN-response signature and fibrotic signature in tubular cells were each associated with failure to respond to treatment. Analysis of tubular cells from patients with proliferative, membranous and mixed LN indicated pathways relevant to inflammation and fibrosis, which offer insight into their histologic differences. In summary, we applied scRNA-seq to LN to deconstruct its heterogeneity and identify novel targets for personalized approaches to therapy. The molecular and cellular processes that lead to renal damage and to the heterogeneity of lupus nephritis (LN) are not well understood. We applied single-cell RNA sequencing (scRNA-seq) to renal biopsies from patients with LN and evaluated skin biopsies as a potential source of diagnostic and prognostic markers of renal disease. Type I interferon (IFN)-response signatures in tubular cells and keratinocytes distinguished patients with LN from healthy control subjects. Moreover, a high IFN-response signature and fibrotic signature in tubular cells were each associated with failure to respond to treatment. Analysis of tubular cells from patients with proliferative, membranous and mixed LN indicated pathways relevant to inflammation and fibrosis, which offer insight into their histologic differences. In summary, we applied scRNA-seq to LN to deconstruct its heterogeneity and identify novel targets for personalized approaches to therapy. Nephritis is a major cause of lupus morbidity. Putterman and colleagues use single-cell RNA sequencing on human renal and skin biopsies to describe the expression landscape associated with lupus nephritis. The molecular and cellular processes that lead to renal damage and to the heterogeneity of lupus nephritis (LN) are not well understood. We applied single-cell RNA sequencing (scRNA-seq) to renal biopsies from patients with LN and evaluated skin biopsies as a potential source of diagnostic and prognostic markers of renal disease. Type I interferon (IFN) response signatures in tubular cells and in keratinocytes distinguished patients with LN from healthy control subjects. Moreover, a high IFN response signature and fibrotic signature in tubular cells were each associated with failure to respond to treatment. Analysis of tubular cells from patients with proliferative, membranous, and mixed LN indicated pathways relevant to inflammation and fibrosis, which offer insight into their histological differences. In summary, we applied scRNA-seq to LN to deconstruct its heterogeneity and identify novel targets for personalized approaches to therapy. |
| Audience | Academic |
| Author | Ranabothu, Saritha Belmont, H. Michael Suryawanshi, Hemant Kustagi, Manjunath Mokrzycki, Michele Schulte, Emma Putterman, Chaim Koenigsberg, Mordecai Slowikowski, Kamil James, Judith Rocca, Juan P. Tuschl, Thomas Raychaudhuri, Soumya Rominieki, Helen Clancy, Robert Wu, Ming Jordan, Nicole Der, Evan Izmirly, Peter Bornkamp, Nicole Graham, Jay A. Buyon, Jill Morozov, Pavel Guthridge, Joel Pullman, James Goilav, Beatrice |
| AuthorAffiliation | 8 Montefiore Einstein Center for Transplantation, Montefiore Medical Center, Bronx, New York, USA 7 Division of Nephrology, Department of Medicine, Albert Einstein College of Medicine, Montefiore Medical Center, Bronx, New York, USA 12 Lupus investigators in the Accelerating Medicines Partnership in RA/SLE network include the following individuals: Jennifer Anolik, William Apruzzese, Arnon Arazi, Celine Berthier, Michael Brenner, Jill Buyon, Robert Clancy, Sean Connery, Melissa Cunningham, Maria Dall’Era, Anne Davidson, Evan Der, Andrea Fava, Chamith Fonseka, Richard Furie, Dan Goldman, Rohit Gupta, Joel Guthridge, Nir Hacohen, David Hildeman, Paul Hoover, Raymond Hsu, Judith James, Ruba Kado, Ken Kalunian, Diane Kamen, Mattias Kretzler, Holden Maecker, Elena Massarotti, William McCune, Maureen McMahon, Meyeon Park, Fernanda Payan-Schober, William Pendergraft, Michelle Petri, Mina Pichavant, Chaim Putterman, Deepak Rao, Soumya Raychaudhuri, Kamil Slowikowski, Hemant Suryawanshi, Thomas T |
| AuthorAffiliation_xml | – name: 9 Clinical Pathology, Montefiore Medical Center, Bronx, New York, USA – name: 3 Pediatric Nephrology, The Children’s Hospital at Montefiore, Albert Einstein College of Medicine, Bronx, New York, USA – name: 2 Laboratory for RNA Molecular Biology, The Rockefeller University, New York, New York, USA – name: 8 Montefiore Einstein Center for Transplantation, Montefiore Medical Center, Bronx, New York, USA – name: 10 Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA – name: 7 Division of Nephrology, Department of Medicine, Albert Einstein College of Medicine, Montefiore Medical Center, Bronx, New York, USA – name: 4 Pediatric Nephrology, Arkansas Children’s Hospital, University of Arkansas Medical Sciences, Little Rock, Arkansas, USA – name: 1 Albert Einstein College of Medicine, Bronx, New York, USA – name: 12 Lupus investigators in the Accelerating Medicines Partnership in RA/SLE network include the following individuals: Jennifer Anolik, William Apruzzese, Arnon Arazi, Celine Berthier, Michael Brenner, Jill Buyon, Robert Clancy, Sean Connery, Melissa Cunningham, Maria Dall’Era, Anne Davidson, Evan Der, Andrea Fava, Chamith Fonseka, Richard Furie, Dan Goldman, Rohit Gupta, Joel Guthridge, Nir Hacohen, David Hildeman, Paul Hoover, Raymond Hsu, Judith James, Ruba Kado, Ken Kalunian, Diane Kamen, Mattias Kretzler, Holden Maecker, Elena Massarotti, William McCune, Maureen McMahon, Meyeon Park, Fernanda Payan-Schober, William Pendergraft, Michelle Petri, Mina Pichavant, Chaim Putterman, Deepak Rao, Soumya Raychaudhuri, Kamil Slowikowski, Hemant Suryawanshi, Thomas Tuschl, PJ Utz, Dia Waguespack, David Wofsy, Fan Zhang – name: 6 Department of Radiology, Montefiore Medical Center, Bronx, New York, USA – name: 11 Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma, USA – name: 5 New York University School of Medicine, New York, New York, USA |
| Author_xml | – sequence: 1 givenname: Evan surname: Der fullname: Der, Evan organization: Division of Rheumatology and Department of Microbiology and Immunology, Albert Einstein College of Medicine – sequence: 2 givenname: Hemant surname: Suryawanshi fullname: Suryawanshi, Hemant organization: Laboratory for RNA Molecular Biology, The Rockefeller University – sequence: 3 givenname: Pavel surname: Morozov fullname: Morozov, Pavel organization: Laboratory for RNA Molecular Biology, The Rockefeller University – sequence: 4 givenname: Manjunath surname: Kustagi fullname: Kustagi, Manjunath organization: Laboratory for RNA Molecular Biology, The Rockefeller University – sequence: 5 givenname: Beatrice surname: Goilav fullname: Goilav, Beatrice organization: Pediatric Nephrology, The Children’s Hospital at Montefiore, Albert Einstein College of Medicine – sequence: 6 givenname: Saritha surname: Ranabothu fullname: Ranabothu, Saritha organization: Pediatric Nephrology, Arkansas Children’s Hospital, University of Arkansas Medical Sciences – sequence: 7 givenname: Peter surname: Izmirly fullname: Izmirly, Peter organization: New York University School of Medicine – sequence: 8 givenname: Robert surname: Clancy fullname: Clancy, Robert organization: New York University School of Medicine – sequence: 9 givenname: H. Michael surname: Belmont fullname: Belmont, H. Michael organization: New York University School of Medicine – sequence: 10 givenname: Mordecai surname: Koenigsberg fullname: Koenigsberg, Mordecai organization: Department of Radiology, Montefiore Medical Center – sequence: 11 givenname: Michele surname: Mokrzycki fullname: Mokrzycki, Michele organization: Division of Nephrology, Department of Medicine, Albert Einstein College of Medicine, Montefiore Medical Center – sequence: 12 givenname: Helen surname: Rominieki fullname: Rominieki, Helen organization: Montefiore Einstein Center for Transplantation, Montefiore Medical Center – sequence: 13 givenname: Jay A. orcidid: 0000-0003-2054-1253 surname: Graham fullname: Graham, Jay A. organization: Montefiore Einstein Center for Transplantation, Montefiore Medical Center – sequence: 14 givenname: Juan P. surname: Rocca fullname: Rocca, Juan P. organization: Montefiore Einstein Center for Transplantation, Montefiore Medical Center – sequence: 15 givenname: Nicole surname: Bornkamp fullname: Bornkamp, Nicole organization: New York University School of Medicine – sequence: 16 givenname: Nicole surname: Jordan fullname: Jordan, Nicole organization: Division of Rheumatology and Department of Microbiology and Immunology, Albert Einstein College of Medicine – sequence: 17 givenname: Emma surname: Schulte fullname: Schulte, Emma organization: Division of Rheumatology and Department of Microbiology and Immunology, Albert Einstein College of Medicine – sequence: 18 givenname: Ming surname: Wu fullname: Wu, Ming organization: New York University School of Medicine – sequence: 19 givenname: James orcidid: 0000-0002-2677-945X surname: Pullman fullname: Pullman, James organization: Clinical Pathology, Montefiore Medical Center – sequence: 20 givenname: Kamil orcidid: 0000-0002-2843-6370 surname: Slowikowski fullname: Slowikowski, Kamil organization: Broad Institute of MIT and Harvard – sequence: 21 givenname: Soumya orcidid: 0000-0002-1901-8265 surname: Raychaudhuri fullname: Raychaudhuri, Soumya organization: Broad Institute of MIT and Harvard – sequence: 22 givenname: Joel orcidid: 0000-0002-9308-237X surname: Guthridge fullname: Guthridge, Joel organization: Oklahoma Medical Research Foundation – sequence: 23 givenname: Judith surname: James fullname: James, Judith organization: Oklahoma Medical Research Foundation – sequence: 24 givenname: Jill orcidid: 0000-0002-3852-7129 surname: Buyon fullname: Buyon, Jill email: jill.buyon@nyumc.org organization: New York University School of Medicine – sequence: 25 givenname: Thomas orcidid: 0000-0002-6483-5678 surname: Tuschl fullname: Tuschl, Thomas email: ttuschl@mail.rockefeller.edu organization: Laboratory for RNA Molecular Biology, The Rockefeller University – sequence: 26 givenname: Chaim orcidid: 0000-0002-3204-6068 surname: Putterman fullname: Putterman, Chaim email: chaim.putterman@einstein.yu.edu organization: Division of Rheumatology and Department of Microbiology and Immunology, Albert Einstein College of Medicine |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31110316$$D View this record in MEDLINE/PubMed |
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| Contributor | Utz, Paul Park, Meyeon Payan-Schober, Fernanda Davidson, Anne Suryawanshi, Hemant Dall'Era, Maria Hoover, Paul Hsu, Raymond Connery, Sean Putterman, Chaim Goldman, Dan Hildeman, David James, Judith Slowikowski, Kamil Apruzzese, William Gupta, Rohit Tuschl, Thomas Fava, Andrea Pichavant, Mina Raychaudhuri, Soumya Pendergraft, William Clancy, Robert Cunningham, Melissa Arazi, Arnon Kretzler, Mattias Wofsy, David Maecker, Holden Der, Evan McMahon, Maureen Petri, Michelle McCune, William Anolik, Jennifer Furie, Richard Hacohen, Nir Kamen, Diane Brenner, Michael Kalunian, Kenneth Kado, Ruba Rao, Deepak Zhang, Fan Fonseka, Chamith Berthier, Celine Waguespack, Dia Buyon, Jill Massarotti, Elena Guthridge, Joel |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Authors contributed equally JB, TT, and CP conceived the study with help from S. Ranabothu, JJ, J. Guthridge and S. Raychaudhuri. Input regarding the skin came from RC and HMB. ED, HS, and S. Ranabothu performed all biopsy dissociations and single-cell experiments. BG, PI, HMB, M. Koenigsberg, M. Mokrzycki, NJ, NB, and ES assisted with patient consent and sample acquisition of LN biopsies. HR, JR, J. Graham assisted with patient consent and sample acquisition of live kidney donor tissue. Renal biopsy histology was evaluated by MW and JP. HMB and PI performed all skin biopsies. Analysis was performed by ED, HS, PM, KS, and M. Kustagi. ED, JB, TT and CP prepared and wrote the manuscript. Author contributions |
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| Snippet | The molecular and cellular processes that lead to renal damage and to the heterogeneity of lupus nephritis (LN) are not well understood. We applied single-cell... |
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| SubjectTerms | 631/250/2520 631/250/38 692/420 Autoimmune diseases Biomedical and Life Sciences Biomedicine Biopsy Care and treatment Cell Lineage - genetics Cell proliferation Computational Biology - methods Extracellular Matrix Proteins - genetics Extracellular Matrix Proteins - metabolism Fibrosis Gene Expression Profiling - methods Heterogeneity Humans Immunology Infectious Diseases Interferon Interferon Type I - metabolism Keratinocytes Keratinocytes - metabolism Kidney Tubules - cytology Kidney Tubules - metabolism Lupus Lupus nephritis Lupus Nephritis - genetics Lupus Nephritis - metabolism Lupus Nephritis - pathology Morbidity Nephritis Protein Binding Resource Ribonucleic acid RNA Signal Transduction Single-Cell Analysis Skin Skin - immunology Skin - metabolism Skin - pathology Systemic lupus erythematosus Transcriptome |
| Title | Tubular cell and keratinocyte single-cell transcriptomics applied to lupus nephritis reveal type I IFN and fibrosis relevant pathways |
| URI | https://link.springer.com/article/10.1038/s41590-019-0386-1 https://www.ncbi.nlm.nih.gov/pubmed/31110316 https://www.proquest.com/docview/2242771788 https://www.proquest.com/docview/2475007427 https://www.proquest.com/docview/2232086976 https://pubmed.ncbi.nlm.nih.gov/PMC6584054 |
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