Single-Cell Analyses of Colon and Blood Reveal Distinct Immune Cell Signatures of Ulcerative Colitis and Crohn’s Disease
Studies are needed to determine the mechanisms of mucosal dysregulation in patients with inflammatory bowel diseases (IBDs) and differences in inflammatory responses of patients with ulcerative colitis (UC) vs Crohn’s disease (CD). We used mass cytometry (CyTOF) to characterize and compare immune ce...
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| Published in | Gastroenterology (New York, N.Y. 1943) Vol. 159; no. 2; pp. 591 - 608.e10 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.08.2020
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Studies are needed to determine the mechanisms of mucosal dysregulation in patients with inflammatory bowel diseases (IBDs) and differences in inflammatory responses of patients with ulcerative colitis (UC) vs Crohn’s disease (CD). We used mass cytometry (CyTOF) to characterize and compare immune cell populations in the mucosa and blood from patients with IBD and without IBD (controls) at single-cell resolution.
We performed CyTOF analysis of colonic mucosa samples (n = 87) and peripheral blood mononuclear cells (n = 85) from patients with active or inactive UC or CD and controls. We also performed single-cell RNA sequencing, flow cytometry, and RNA in situ hybridization analyses to validate key findings. We used random forest modeling to identify differences in signatures across subject groups.
Compared with controls, colonic mucosa samples from patients with IBD had increased abundances of HLA-DR+CD38+ T cells, including T-regulatory cells that produce inflammatory cytokines; CXCR3+ plasmablasts; and IL1B+ macrophages and monocytes. Colonic mucosa samples from patients with UC were characterized by expansion of IL17A+ CD161+ effector memory T cells and IL17A+ T-regulatory cells; expansion of HLA-DR+CD56+ granulocytes; and reductions in type 3 innate lymphoid cells. Mucosal samples from patients with active CD were characterized by IL1B+HLA-DR+CD38+ T cells, IL1B+TNF+IFNG+ naïve B cells, IL1B+ dendritic cells (DCs), and IL1B+ plasmacytoid DCs. Peripheral blood mononuclear cells from patients with active CD differed from those of active UC in that the peripheral blood mononuclear cells from patients with CD had increased IL1B+ T-regulatory cells, IL1B+ DCs and IL1B+ plasmacytoid DCs, IL1B+ monocytes, and fewer group 1 innate lymphoid cells. Random forest modeling differentiated active UC from active CD in colonic mucosa and blood samples; top discriminating features included many of the cellular populations identified above.
We used single-cell technologies to identify immune cell populations specific to mucosa and blood samples from patients with active or inactive CD and UC and controls. This information might be used to develop therapies that target specific cell populations in patients with different types of IBD.
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| AbstractList | Studies are needed to determine the mechanisms of mucosal dysregulation in patients with inflammatory bowel diseases (IBDs) and differences in inflammatory responses of patients with ulcerative colitis (UC) vs Crohn’s disease (CD). We used mass cytometry (CyTOF) to characterize and compare immune cell populations in the mucosa and blood from patients with IBD and without IBD (controls) at single-cell resolution.
We performed CyTOF analysis of colonic mucosa samples (n = 87) and peripheral blood mononuclear cells (n = 85) from patients with active or inactive UC or CD and controls. We also performed single-cell RNA sequencing, flow cytometry, and RNA in situ hybridization analyses to validate key findings. We used random forest modeling to identify differences in signatures across subject groups.
Compared with controls, colonic mucosa samples from patients with IBD had increased abundances of HLA-DR+CD38+ T cells, including T-regulatory cells that produce inflammatory cytokines; CXCR3+ plasmablasts; and IL1B+ macrophages and monocytes. Colonic mucosa samples from patients with UC were characterized by expansion of IL17A+ CD161+ effector memory T cells and IL17A+ T-regulatory cells; expansion of HLA-DR+CD56+ granulocytes; and reductions in type 3 innate lymphoid cells. Mucosal samples from patients with active CD were characterized by IL1B+HLA-DR+CD38+ T cells, IL1B+TNF+IFNG+ naïve B cells, IL1B+ dendritic cells (DCs), and IL1B+ plasmacytoid DCs. Peripheral blood mononuclear cells from patients with active CD differed from those of active UC in that the peripheral blood mononuclear cells from patients with CD had increased IL1B+ T-regulatory cells, IL1B+ DCs and IL1B+ plasmacytoid DCs, IL1B+ monocytes, and fewer group 1 innate lymphoid cells. Random forest modeling differentiated active UC from active CD in colonic mucosa and blood samples; top discriminating features included many of the cellular populations identified above.
We used single-cell technologies to identify immune cell populations specific to mucosa and blood samples from patients with active or inactive CD and UC and controls. This information might be used to develop therapies that target specific cell populations in patients with different types of IBD.
[Display omitted] Studies are needed to determine the mechanisms of mucosal dysregulation in patients with inflammatory bowel diseases (IBDs) and differences in inflammatory responses of patients with ulcerative colitis (UC) vs Crohn's disease (CD). We used mass cytometry (CyTOF) to characterize and compare immune cell populations in the mucosa and blood from patients with IBD and without IBD (controls) at single-cell resolution.BACKGROUND & AIMSStudies are needed to determine the mechanisms of mucosal dysregulation in patients with inflammatory bowel diseases (IBDs) and differences in inflammatory responses of patients with ulcerative colitis (UC) vs Crohn's disease (CD). We used mass cytometry (CyTOF) to characterize and compare immune cell populations in the mucosa and blood from patients with IBD and without IBD (controls) at single-cell resolution.We performed CyTOF analysis of colonic mucosa samples (n = 87) and peripheral blood mononuclear cells (n = 85) from patients with active or inactive UC or CD and controls. We also performed single-cell RNA sequencing, flow cytometry, and RNA in situ hybridization analyses to validate key findings. We used random forest modeling to identify differences in signatures across subject groups.METHODSWe performed CyTOF analysis of colonic mucosa samples (n = 87) and peripheral blood mononuclear cells (n = 85) from patients with active or inactive UC or CD and controls. We also performed single-cell RNA sequencing, flow cytometry, and RNA in situ hybridization analyses to validate key findings. We used random forest modeling to identify differences in signatures across subject groups.Compared with controls, colonic mucosa samples from patients with IBD had increased abundances of HLA-DR+CD38+ T cells, including T-regulatory cells that produce inflammatory cytokines; CXCR3+ plasmablasts; and IL1B+ macrophages and monocytes. Colonic mucosa samples from patients with UC were characterized by expansion of IL17A+ CD161+ effector memory T cells and IL17A+ T-regulatory cells; expansion of HLA-DR+CD56+ granulocytes; and reductions in type 3 innate lymphoid cells. Mucosal samples from patients with active CD were characterized by IL1B+HLA-DR+CD38+ T cells, IL1B+TNF+IFNG+ naïve B cells, IL1B+ dendritic cells (DCs), and IL1B+ plasmacytoid DCs. Peripheral blood mononuclear cells from patients with active CD differed from those of active UC in that the peripheral blood mononuclear cells from patients with CD had increased IL1B+ T-regulatory cells, IL1B+ DCs and IL1B+ plasmacytoid DCs, IL1B+ monocytes, and fewer group 1 innate lymphoid cells. Random forest modeling differentiated active UC from active CD in colonic mucosa and blood samples; top discriminating features included many of the cellular populations identified above.RESULTSCompared with controls, colonic mucosa samples from patients with IBD had increased abundances of HLA-DR+CD38+ T cells, including T-regulatory cells that produce inflammatory cytokines; CXCR3+ plasmablasts; and IL1B+ macrophages and monocytes. Colonic mucosa samples from patients with UC were characterized by expansion of IL17A+ CD161+ effector memory T cells and IL17A+ T-regulatory cells; expansion of HLA-DR+CD56+ granulocytes; and reductions in type 3 innate lymphoid cells. Mucosal samples from patients with active CD were characterized by IL1B+HLA-DR+CD38+ T cells, IL1B+TNF+IFNG+ naïve B cells, IL1B+ dendritic cells (DCs), and IL1B+ plasmacytoid DCs. Peripheral blood mononuclear cells from patients with active CD differed from those of active UC in that the peripheral blood mononuclear cells from patients with CD had increased IL1B+ T-regulatory cells, IL1B+ DCs and IL1B+ plasmacytoid DCs, IL1B+ monocytes, and fewer group 1 innate lymphoid cells. Random forest modeling differentiated active UC from active CD in colonic mucosa and blood samples; top discriminating features included many of the cellular populations identified above.We used single-cell technologies to identify immune cell populations specific to mucosa and blood samples from patients with active or inactive CD and UC and controls. This information might be used to develop therapies that target specific cell populations in patients with different types of IBD.CONCLUSIONSWe used single-cell technologies to identify immune cell populations specific to mucosa and blood samples from patients with active or inactive CD and UC and controls. This information might be used to develop therapies that target specific cell populations in patients with different types of IBD. The authors analyzed immune cells in colon tissues and blood samples from patients with IBD and found that samples from patients with CD vs UC contain different types of immune cells. Studies are needed to determine the mechanisms of mucosal dysregulation in patients with inflammatory bowel diseases (IBDs) and differences in inflammatory responses of patients with ulcerative colitis (UC) vs Crohn's disease (CD). We used mass cytometry (CyTOF) to characterize and compare immune cell populations in the mucosa and blood from patients with IBD and without IBD (controls) at single-cell resolution. We performed CyTOF analysis of colonic mucosa samples (n = 87) and peripheral blood mononuclear cells (n = 85) from patients with active or inactive UC or CD and controls. We also performed single-cell RNA sequencing, flow cytometry, and RNA in situ hybridization analyses to validate key findings. We used random forest modeling to identify differences in signatures across subject groups. Compared with controls, colonic mucosa samples from patients with IBD had increased abundances of HLA-DR+CD38+ T cells, including T-regulatory cells that produce inflammatory cytokines; CXCR3+ plasmablasts; and IL1B+ macrophages and monocytes. Colonic mucosa samples from patients with UC were characterized by expansion of IL17A+ CD161+ effector memory T cells and IL17A+ T-regulatory cells; expansion of HLA-DR+CD56+ granulocytes; and reductions in type 3 innate lymphoid cells. Mucosal samples from patients with active CD were characterized by IL1B+HLA-DR+CD38+ T cells, IL1B+TNF+IFNG naïve B cells, IL1B+ dendritic cells (DCs), and IL1B+ plasmacytoid DCs. Peripheral blood mononuclear cells from patients with active CD differed from those of active UC in that the peripheral blood mononuclear cells from patients with CD had increased IL1B+ T-regulatory cells, IL1B+ DCs and IL1B+ plasmacytoid DCs, IL1B+ monocytes, and fewer group 1 innate lymphoid cells. Random forest modeling differentiated active UC from active CD in colonic mucosa and blood samples; top discriminating features included many of the cellular populations identified above. We used single-cell technologies to identify immune cell populations specific to mucosa and blood samples from patients with active or inactive CD and UC and controls. This information might be used to develop therapies that target specific cell populations in patients with different types of IBD. |
| Author | Horwitz, Bruce Ordovas-Montanes, Jose Parmet, Tamar Vukovic, Marko Bousvaros, Athos De Silva, Punyanganie Rufo, Paul A. Mobassaleh, Munir Grover, Amit S. Silverstein, Jared Friedman, Sonia Kahn, Stacy Tseng, George Regan, Brian Norton, Beth-Ann Allegretti, Jessica R. Liu, Peng Wall, Sarah Zimmerman, Lori Shalek, Alex K. Kean, Leslie Mitsialis, Vanessa Toothaker, Jessica Fawaz, Rima Ballal, Sonia Hamilton, Matthew Goldsmith, Jeffrey Field, Michael Zitomersky, Naamah Fishman, Laurie N. Flores, Alejandro Higuchi, Leslie Makrauer, Frederick McCourt, Collin Bonilla, Silvana Huh, Susanna Sabharwal, Sabina Fox, Victor Korzenik, Joshua Konnikova, Liza Snapper, Scott B. Spencer, Dennis Wolf, Anne Pleskow, Randi G. Ouahed, Jodie Winter, Rachel W. Lee, Christine Verhave, Menno |
| AuthorAffiliation | 12 Ragon Institute of MGH, MIT and Harvard, Cambridge, MA, 02139 USA 5 Division of Hematology Oncology Boston Children’s Hospital, Boston, MA 02115, USA 2 Division of Gastroenterology, Hepatology and Nutrition, Boston, MA 02115, USA 16 Department of Biostatistics University of Pittsburgh, Pittsburgh, PA 15224, USA 13 Department of Pediatrics, UPMC Children’s Hospital, Pittsburgh, PA 15224, USA 15 Department of Developmental Biology, Pittsburgh, PA 15224, USA 7 BWH Crohn’s and Colitis Center: Jessica R. Allegretti, MD, MPH, Punyanganie De Silva, MD, MPH, Sonia Friedman, MD, Matthew Hamilton, MD, Joshua Korzenik, MD, Frederick Makrauer, MD, Beth-Ann Norton, MS, RN, ANP-BC, Rachel W. Winter, MD, MPH 14 Department of Immunology, Pittsburgh, PA 15224, USA 1 Division of Gastroenterology, Brigham and Women’s Hospital, Boston, MA 02115, USA 11 Koch Institute for Integrative Cancer Research, MIT, Cambridge, MA, 02139 USA 9 Broad Institute of MIT and Harvard, Cambridge, MA, USA 02139 USA 3 Department of Pa |
| AuthorAffiliation_xml | – name: 6 BCH IBD Center: Sonia Ballal, MD, Silvana Bonilla, MD, MS, Rima Fawaz, MD, Laurie N. Fishman, MD, Alejandro Flores, MD, Victor Fox, MD, Amit S. Grover, MB, BCh BAO, Leslie Higuchi, MD, Susanna Huh, MD, Stacy Kahn, MD, Christine Lee, MD, Munir Mobassaleh, MD, Jodie Ouahed, MD, Randi G. Pleskow, MD, Brian Regan, DO, Paul A. Rufo, MD, MMSc, Sabina Sabharwal, MD, Jared Silverstein, MD, Menno Verhave, MD, Anne Wolf, MD, Lori Zimmerman, MD, Naamah Zitomersky, MD – name: 10 Harvard Stem Cell Institute, Cambridge, MA, USA 02138 USA – name: 15 Department of Developmental Biology, Pittsburgh, PA 15224, USA – name: 11 Koch Institute for Integrative Cancer Research, MIT, Cambridge, MA, 02139 USA – name: 5 Division of Hematology Oncology Boston Children’s Hospital, Boston, MA 02115, USA – name: 2 Division of Gastroenterology, Hepatology and Nutrition, Boston, MA 02115, USA – name: 3 Department of Pathology, Boston, MA 02115, USA – name: 13 Department of Pediatrics, UPMC Children’s Hospital, Pittsburgh, PA 15224, USA – name: 8 Institute for Medical Engineering and Science (IMES), MIT, Cambridge, MA, 02139 USA – name: 4 Division of Newborn Medicine, Boston, MA 02115, USA – name: 16 Department of Biostatistics University of Pittsburgh, Pittsburgh, PA 15224, USA – name: 1 Division of Gastroenterology, Brigham and Women’s Hospital, Boston, MA 02115, USA – name: 14 Department of Immunology, Pittsburgh, PA 15224, USA – name: 12 Ragon Institute of MGH, MIT and Harvard, Cambridge, MA, 02139 USA – name: 9 Broad Institute of MIT and Harvard, Cambridge, MA, USA 02139 USA – name: 7 BWH Crohn’s and Colitis Center: Jessica R. Allegretti, MD, MPH, Punyanganie De Silva, MD, MPH, Sonia Friedman, MD, Matthew Hamilton, MD, Joshua Korzenik, MD, Frederick Makrauer, MD, Beth-Ann Norton, MS, RN, ANP-BC, Rachel W. Winter, MD, MPH |
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givenname: Athos surname: Bousvaros fullname: Bousvaros, Athos organization: Division of Gastroenterology, Hepatology and Nutrition, Boston Children’s Hospital, Boston, Massachusetts – sequence: 12 givenname: Sonia surname: Ballal fullname: Ballal, Sonia – sequence: 13 givenname: Silvana surname: Bonilla fullname: Bonilla, Silvana – sequence: 14 givenname: Rima surname: Fawaz fullname: Fawaz, Rima – sequence: 15 givenname: Laurie N. surname: Fishman fullname: Fishman, Laurie N. – sequence: 16 givenname: Alejandro surname: Flores fullname: Flores, Alejandro – sequence: 17 givenname: Victor surname: Fox fullname: Fox, Victor – sequence: 18 givenname: Amit S. surname: Grover fullname: Grover, Amit S. – sequence: 19 givenname: Leslie surname: Higuchi fullname: Higuchi, Leslie – sequence: 20 givenname: Susanna surname: Huh fullname: Huh, Susanna – sequence: 21 givenname: Stacy surname: Kahn fullname: Kahn, Stacy – sequence: 22 givenname: Christine surname: Lee fullname: Lee, Christine – 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Division of Gastroenterology, Hepatology and Nutrition, Boston Children’s Hospital, Boston, Massachusetts – sequence: 45 givenname: Jeffrey surname: Goldsmith fullname: Goldsmith, Jeffrey organization: Department of Pathology, Boston Children’s Hospital, Boston, Massachusetts – sequence: 46 givenname: George orcidid: 0000-0002-5447-1014 surname: Tseng fullname: Tseng, George organization: Department of Biostatistics University of Pittsburgh, Pittsburgh, Pennsylvania – sequence: 47 givenname: Scott B. surname: Snapper fullname: Snapper, Scott B. email: scott.snapper@childrens.harvard.edu organization: Division of Gastroenterology, Brigham and Women’s Hospital, Boston, Massachusetts – sequence: 48 givenname: Liza orcidid: 0000-0003-4804-5497 surname: Konnikova fullname: Konnikova, Liza email: liza.konnikova@yale.edu organization: Division of Newborn Medicine, Boston Children’s Hospital, Boston, Massachusetts |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32428507$$D View this record in MEDLINE/PubMed |
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| Copyright | 2020 AGA Institute Copyright © 2020 AGA Institute. Published by Elsevier Inc. All rights reserved. |
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| Keywords | a CD ILC TCR MAIT Cells Treg EM i t-SNE IBD TNF pDC UC AUC ILC3 scRNA-Seq RF MAIT CyTOF DC |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 ObjectType-Undefined-3 Authors equally supervised the work Contributions to manuscript: V.M., S.B.S. and L.K. conceived of the experiments. V.M., S.W., T.P., M.F. and L.K. performed the CyTOF experiments. V.M. and L.K. analyzed the CyTOF data. J.G. assisted with histological analysis. C.M. and J.T. performed and analyzed RNA in situ hybridization data. V.M., S.W., J.O., M.V., D.S., A.K.S. and L.K.5 were involved in scRNA-seq acquisition and analysis. P.L. and G.T. designed and developed the predictive modeling of the cohort. V.M., S.B.S. and L.K. wrote the manuscript. All authors have read and approve of the manuscript. |
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| Snippet | Studies are needed to determine the mechanisms of mucosal dysregulation in patients with inflammatory bowel diseases (IBDs) and differences in inflammatory... The authors analyzed immune cells in colon tissues and blood samples from patients with IBD and found that samples from patients with CD vs UC contain... |
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| SubjectTerms | Adolescent Adult Case-Control Studies Child Colitis, Ulcerative - blood Colitis, Ulcerative - immunology Colitis, Ulcerative - pathology Colon - immunology Colon - pathology Crohn Disease - blood Crohn Disease - immunology Crohn Disease - pathology Female Flow Cytometry Humans ILC3 Immunity, Cellular Immunophenotyping - methods Intestinal Mucosa - immunology Intestinal Mucosa - pathology MAIT Cells Male RNA-Seq scRNA-Seq Single-Cell Analysis Treg Young Adult |
| Title | Single-Cell Analyses of Colon and Blood Reveal Distinct Immune Cell Signatures of Ulcerative Colitis and Crohn’s Disease |
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