Single-cell RNA sequencing reveals profibrotic roles of distinct epithelial and mesenchymal lineages in pulmonary fibrosis
Single-cell RNA sequencing provides new insights into pathologic epithelial and mesenchymal remodeling in the human lung. Pulmonary fibrosis (PF) is a form of chronic lung disease characterized by pathologic epithelial remodeling and accumulation of extracellular matrix (ECM). To comprehensively def...
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| Published in | Science advances Vol. 6; no. 28; p. eaba1972 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Association for the Advancement of Science
01.07.2020
|
| Subjects | |
| Online Access | Get full text |
| ISSN | 2375-2548 2375-2548 |
| DOI | 10.1126/sciadv.aba1972 |
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| Abstract | Single-cell RNA sequencing provides new insights into pathologic epithelial and mesenchymal remodeling in the human lung.
Pulmonary fibrosis (PF) is a form of chronic lung disease characterized by pathologic epithelial remodeling and accumulation of extracellular matrix (ECM). To comprehensively define the cell types, mechanisms, and mediators driving fibrotic remodeling in lungs with PF, we performed single-cell RNA sequencing of single-cell suspensions from 10 nonfibrotic control and 20 PF lungs. Analysis of 114,396 cells identified 31 distinct cell subsets/states. We report that a remarkable shift in epithelial cell phenotypes occurs in the peripheral lung in PF and identify several previously unrecognized epithelial cell phenotypes, including a
KRT5
−
/
KRT17
+
pathologic, ECM-producing epithelial cell population that was highly enriched in PF lungs. Multiple fibroblast subtypes were observed to contribute to ECM expansion in a spatially discrete manner. Together, these data provide high-resolution insights into the complexity and plasticity of the distal lung epithelium in human disease and indicate a diversity of epithelial and mesenchymal cells contribute to pathologic lung fibrosis. |
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| AbstractList | Pulmonary fibrosis (PF) is a form of chronic lung disease characterized by pathologic epithelial remodeling and accumulation of extracellular matrix (ECM). To comprehensively define the cell types, mechanisms, and mediators driving fibrotic remodeling in lungs with PF, we performed single-cell RNA sequencing of single-cell suspensions from 10 nonfibrotic control and 20 PF lungs. Analysis of 114,396 cells identified 31 distinct cell subsets/states. We report that a remarkable shift in epithelial cell phenotypes occurs in the peripheral lung in PF and identify several previously unrecognized epithelial cell phenotypes, including a KRT5- /KRT17 + pathologic, ECM-producing epithelial cell population that was highly enriched in PF lungs. Multiple fibroblast subtypes were observed to contribute to ECM expansion in a spatially discrete manner. Together, these data provide high-resolution insights into the complexity and plasticity of the distal lung epithelium in human disease and indicate a diversity of epithelial and mesenchymal cells contribute to pathologic lung fibrosis.Pulmonary fibrosis (PF) is a form of chronic lung disease characterized by pathologic epithelial remodeling and accumulation of extracellular matrix (ECM). To comprehensively define the cell types, mechanisms, and mediators driving fibrotic remodeling in lungs with PF, we performed single-cell RNA sequencing of single-cell suspensions from 10 nonfibrotic control and 20 PF lungs. Analysis of 114,396 cells identified 31 distinct cell subsets/states. We report that a remarkable shift in epithelial cell phenotypes occurs in the peripheral lung in PF and identify several previously unrecognized epithelial cell phenotypes, including a KRT5- /KRT17 + pathologic, ECM-producing epithelial cell population that was highly enriched in PF lungs. Multiple fibroblast subtypes were observed to contribute to ECM expansion in a spatially discrete manner. Together, these data provide high-resolution insights into the complexity and plasticity of the distal lung epithelium in human disease and indicate a diversity of epithelial and mesenchymal cells contribute to pathologic lung fibrosis. Single-cell RNA sequencing provides new insights into pathologic epithelial and mesenchymal remodeling in the human lung. Pulmonary fibrosis (PF) is a form of chronic lung disease characterized by pathologic epithelial remodeling and accumulation of extracellular matrix (ECM). To comprehensively define the cell types, mechanisms, and mediators driving fibrotic remodeling in lungs with PF, we performed single-cell RNA sequencing of single-cell suspensions from 10 nonfibrotic control and 20 PF lungs. Analysis of 114,396 cells identified 31 distinct cell subsets/states. We report that a remarkable shift in epithelial cell phenotypes occurs in the peripheral lung in PF and identify several previously unrecognized epithelial cell phenotypes, including a KRT5 − / KRT17 + pathologic, ECM-producing epithelial cell population that was highly enriched in PF lungs. Multiple fibroblast subtypes were observed to contribute to ECM expansion in a spatially discrete manner. Together, these data provide high-resolution insights into the complexity and plasticity of the distal lung epithelium in human disease and indicate a diversity of epithelial and mesenchymal cells contribute to pathologic lung fibrosis. Pulmonary fibrosis (PF) is a form of chronic lung disease characterized by pathologic epithelial remodeling and accumulation of extracellular matrix (ECM). To comprehensively define the cell types, mechanisms, and mediators driving fibrotic remodeling in lungs with PF, we performed single-cell RNA sequencing of single-cell suspensions from 10 nonfibrotic control and 20 PF lungs. Analysis of 114,396 cells identified 31 distinct cell subsets/states. We report that a remarkable shift in epithelial cell phenotypes occurs in the peripheral lung in PF and identify several previously unrecognized epithelial cell phenotypes, including a / pathologic, ECM-producing epithelial cell population that was highly enriched in PF lungs. Multiple fibroblast subtypes were observed to contribute to ECM expansion in a spatially discrete manner. Together, these data provide high-resolution insights into the complexity and plasticity of the distal lung epithelium in human disease and indicate a diversity of epithelial and mesenchymal cells contribute to pathologic lung fibrosis. |
| Author | Chung, Mei-I McDonnell, Wyatt J. Winters, Nichelle I. Sucre, Jennifer M. S. Ware, Lorraine B. Blackwell, Timothy S. Taylor, Chase J. Ding, Guixiao Bremner, Ross Gutierrez, Austin J. Mallal, Simon B. Bacchetta, Matthew J. Yahn, Stephanie L. Kropski, Jonathan A. Loyd, James E. Walia, Rajat Habermann, Arun C. Calvi, Carla L. Bui, Linh T. Serezani, Ana P. Richmond, Bradley W. Peter, Lance Shaver, Ciara M. Raju, Latha Wood, Lori Jetter, Christopher Banovich, Nicholas E. Roberson, Jamie |
| Author_xml | – sequence: 1 givenname: Arun C. orcidid: 0000-0002-7564-6370 surname: Habermann fullname: Habermann, Arun C. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 2 givenname: Austin J. surname: Gutierrez fullname: Gutierrez, Austin J. organization: Translational Genomics Research Institute, Phoenix, AZ, USA – sequence: 3 givenname: Linh T. orcidid: 0000-0003-3152-8978 surname: Bui fullname: Bui, Linh T. organization: Translational Genomics Research Institute, Phoenix, AZ, USA – sequence: 4 givenname: Stephanie L. orcidid: 0000-0003-3267-0992 surname: Yahn fullname: Yahn, Stephanie L. organization: Translational Genomics Research Institute, Phoenix, AZ, USA – sequence: 5 givenname: Nichelle I. surname: Winters fullname: Winters, Nichelle I. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 6 givenname: Carla L. surname: Calvi fullname: Calvi, Carla L. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 7 givenname: Lance surname: Peter fullname: Peter, Lance organization: Translational Genomics Research Institute, Phoenix, AZ, USA – sequence: 8 givenname: Mei-I surname: Chung fullname: Chung, Mei-I organization: Translational Genomics Research Institute, Phoenix, AZ, USA – sequence: 9 givenname: Chase J. orcidid: 0000-0002-7942-0483 surname: Taylor fullname: Taylor, Chase J. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 10 givenname: Christopher orcidid: 0000-0002-3826-5843 surname: Jetter fullname: Jetter, Christopher organization: Division of Neonatology, Department of Pediatrics, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 11 givenname: Latha orcidid: 0000-0002-1498-2469 surname: Raju fullname: Raju, Latha organization: Vanderbilt Center for Advanced Genomics, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 12 givenname: Jamie surname: Roberson fullname: Roberson, Jamie organization: Vanderbilt Center for Advanced Genomics, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 13 givenname: Guixiao surname: Ding fullname: Ding, Guixiao organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 14 givenname: Lori surname: Wood fullname: Wood, Lori organization: Department of Thoracic Disease and Transplantation, Norton Thoracic Institute, Phoenix, AZ, USA – sequence: 15 givenname: Jennifer M. S. surname: Sucre fullname: Sucre, Jennifer M. S. organization: Division of Neonatology, Department of Pediatrics, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 16 givenname: Bradley W. surname: Richmond fullname: Richmond, Bradley W. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA., Department of Veterans Affairs Medical Center, Nashville, TN, USA – sequence: 17 givenname: Ana P. surname: Serezani fullname: Serezani, Ana P. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 18 givenname: Wyatt J. orcidid: 0000-0003-3859-2067 surname: McDonnell fullname: McDonnell, Wyatt J. organization: Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 19 givenname: Simon B. surname: Mallal fullname: Mallal, Simon B. organization: Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA., Division of Infectious Diseases, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA., Institute for Immunology and Infectious Diseases, Murdoch University, Discovery Way, Murdoch, Western Australia 6150, Australia – sequence: 20 givenname: Matthew J. surname: Bacchetta fullname: Bacchetta, Matthew J. organization: Department of Thoracic Surgery, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 21 givenname: James E. surname: Loyd fullname: Loyd, James E. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 22 givenname: Ciara M. orcidid: 0000-0002-5677-0288 surname: Shaver fullname: Shaver, Ciara M. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 23 givenname: Lorraine B. surname: Ware fullname: Ware, Lorraine B. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA., Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA – sequence: 24 givenname: Ross orcidid: 0000-0003-2216-9109 surname: Bremner fullname: Bremner, Ross organization: Department of Thoracic Disease and Transplantation, Norton Thoracic Institute, Phoenix, AZ, USA – sequence: 25 givenname: Rajat orcidid: 0000-0001-5036-2921 surname: Walia fullname: Walia, Rajat organization: Department of Thoracic Disease and Transplantation, Norton Thoracic Institute, Phoenix, AZ, USA – sequence: 26 givenname: Timothy S. surname: Blackwell fullname: Blackwell, Timothy S. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA., Department of Veterans Affairs Medical Center, Nashville, TN, USA., Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN, USA – sequence: 27 givenname: Nicholas E. orcidid: 0000-0003-2604-3247 surname: Banovich fullname: Banovich, Nicholas E. organization: Translational Genomics Research Institute, Phoenix, AZ, USA – sequence: 28 givenname: Jonathan A. orcidid: 0000-0002-8923-1344 surname: Kropski fullname: Kropski, Jonathan A. organization: Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA., Department of Veterans Affairs Medical Center, Nashville, TN, USA., Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32832598$$D View this record in MEDLINE/PubMed |
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| Language | English |
| License | https://creativecommons.org/licenses/by-nc/4.0 Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally to this work. Present address: 10x Genomics Inc., 6230 Stoneridge Mall Road, Pleasanton, CA 94588, USA. |
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| Snippet | Single-cell RNA sequencing provides new insights into pathologic epithelial and mesenchymal remodeling in the human lung.
Pulmonary fibrosis (PF) is a form of... Pulmonary fibrosis (PF) is a form of chronic lung disease characterized by pathologic epithelial remodeling and accumulation of extracellular matrix (ECM). To... |
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| SubjectTerms | Diseases and Disorders Extracellular Matrix - metabolism Fibrosis Humans Lung - metabolism Pulmonary Fibrosis - genetics Pulmonary Fibrosis - metabolism SciAdv r-articles Sequence Analysis, RNA |
| Title | Single-cell RNA sequencing reveals profibrotic roles of distinct epithelial and mesenchymal lineages in pulmonary fibrosis |
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