Single-Cell Transcriptomic Analysis of Human Lung Provides Insights into the Pathobiology of Pulmonary Fibrosis
The contributions of diverse cell populations in the human lung to pulmonary fibrosis pathogenesis are poorly understood. Single-cell RNA sequencing can reveal changes within individual cell populations during pulmonary fibrosis that are important for disease pathogenesis. To determine whether singl...
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| Published in | American journal of respiratory and critical care medicine Vol. 199; no. 12; pp. 1517 - 1536 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Thoracic Society
15.06.2019
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| Subjects | |
| Online Access | Get full text |
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| Abstract | The contributions of diverse cell populations in the human lung to pulmonary fibrosis pathogenesis are poorly understood. Single-cell RNA sequencing can reveal changes within individual cell populations during pulmonary fibrosis that are important for disease pathogenesis.
To determine whether single-cell RNA sequencing can reveal disease-related heterogeneity within alveolar macrophages, epithelial cells, or other cell types in lung tissue from subjects with pulmonary fibrosis compared with control subjects.
We performed single-cell RNA sequencing on lung tissue obtained from eight transplant donors and eight recipients with pulmonary fibrosis and on one bronchoscopic cryobiospy sample from a patient with idiopathic pulmonary fibrosis. We validated these data using
RNA hybridization, immunohistochemistry, and bulk RNA-sequencing on flow-sorted cells from 22 additional subjects.
We identified a distinct, novel population of profibrotic alveolar macrophages exclusively in patients with fibrosis. Within epithelial cells, the expression of genes involved in Wnt secretion and response was restricted to nonoverlapping cells. We identified rare cell populations including airway stem cells and senescent cells emerging during pulmonary fibrosis. We developed a web-based tool to explore these data.
We generated a single-cell atlas of pulmonary fibrosis. Using this atlas, we demonstrated heterogeneity within alveolar macrophages and epithelial cells from subjects with pulmonary fibrosis. These results support the feasibility of discovery-based approaches using next-generation sequencing technologies to identify signaling pathways for targeting in the development of personalized therapies for patients with pulmonary fibrosis. |
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| AbstractList | The contributions of diverse cell populations in the human lung to pulmonary fibrosis pathogenesis are poorly understood. Single-cell RNA sequencing can reveal changes within individual cell populations during pulmonary fibrosis that are important for disease pathogenesis.
To determine whether single-cell RNA sequencing can reveal disease-related heterogeneity within alveolar macrophages, epithelial cells, or other cell types in lung tissue from subjects with pulmonary fibrosis compared with control subjects.
We performed single-cell RNA sequencing on lung tissue obtained from eight transplant donors and eight recipients with pulmonary fibrosis and on one bronchoscopic cryobiospy sample from a patient with idiopathic pulmonary fibrosis. We validated these data using
RNA hybridization, immunohistochemistry, and bulk RNA-sequencing on flow-sorted cells from 22 additional subjects.
We identified a distinct, novel population of profibrotic alveolar macrophages exclusively in patients with fibrosis. Within epithelial cells, the expression of genes involved in Wnt secretion and response was restricted to nonoverlapping cells. We identified rare cell populations including airway stem cells and senescent cells emerging during pulmonary fibrosis. We developed a web-based tool to explore these data.
We generated a single-cell atlas of pulmonary fibrosis. Using this atlas, we demonstrated heterogeneity within alveolar macrophages and epithelial cells from subjects with pulmonary fibrosis. These results support the feasibility of discovery-based approaches using next-generation sequencing technologies to identify signaling pathways for targeting in the development of personalized therapies for patients with pulmonary fibrosis. Rationale: The contributions of diverse cell populations in the human lung to pulmonary fibrosis pathogenesis are poorly understood. Single-cell RNA sequencing can reveal changes within individual cell populations during pulmonary fibrosis that are important for disease pathogenesis. Objectives: To determine whether single-cell RNA sequencing can reveal disease-related heterogeneity within alveolar macrophages, epithelial cells, or other cell types in lung tissue from subjects with pulmonary fibrosis compared with control subjects. Methods: We performed single-cell RNA sequencing on lung tissue obtained from eight transplant donors and eight recipients with pulmonary fibrosis and on one bronchoscopic cryobiospy sample from a patient with idiopathic pulmonary fibrosis. We validated these data using in situ RNA hybridization, immunohistochemistry, and bulk RNA-sequencing on flow-sorted cells from 22 additional subjects. Measurements and Main Results: We identified a distinct, novel population of profibrotic alveolar macrophages exclusively in patients with fibrosis. Within epithelial cells, the expression of genes involved in Wnt secretion and response was restricted to nonoverlapping cells. We identified rare cell populations including airway stem cells and senescent cells emerging during pulmonary fibrosis. We developed a web-based tool to explore these data. Conclusions: We generated a single-cell atlas of pulmonary fibrosis. Using this atlas, we demonstrated heterogeneity within alveolar macrophages and epithelial cells from subjects with pulmonary fibrosis. These results support the feasibility of discovery-based approaches using next-generation sequencing technologies to identify signaling pathways for targeting in the development of personalized therapies for patients with pulmonary fibrosis.Rationale: The contributions of diverse cell populations in the human lung to pulmonary fibrosis pathogenesis are poorly understood. Single-cell RNA sequencing can reveal changes within individual cell populations during pulmonary fibrosis that are important for disease pathogenesis. Objectives: To determine whether single-cell RNA sequencing can reveal disease-related heterogeneity within alveolar macrophages, epithelial cells, or other cell types in lung tissue from subjects with pulmonary fibrosis compared with control subjects. Methods: We performed single-cell RNA sequencing on lung tissue obtained from eight transplant donors and eight recipients with pulmonary fibrosis and on one bronchoscopic cryobiospy sample from a patient with idiopathic pulmonary fibrosis. We validated these data using in situ RNA hybridization, immunohistochemistry, and bulk RNA-sequencing on flow-sorted cells from 22 additional subjects. Measurements and Main Results: We identified a distinct, novel population of profibrotic alveolar macrophages exclusively in patients with fibrosis. Within epithelial cells, the expression of genes involved in Wnt secretion and response was restricted to nonoverlapping cells. We identified rare cell populations including airway stem cells and senescent cells emerging during pulmonary fibrosis. We developed a web-based tool to explore these data. Conclusions: We generated a single-cell atlas of pulmonary fibrosis. Using this atlas, we demonstrated heterogeneity within alveolar macrophages and epithelial cells from subjects with pulmonary fibrosis. These results support the feasibility of discovery-based approaches using next-generation sequencing technologies to identify signaling pathways for targeting in the development of personalized therapies for patients with pulmonary fibrosis. Rationale: The contributions of diverse cell populations in the human lung to pulmonary fibrosis pathogenesis are poorly understood. Single-cell RNA sequencing can reveal changes within individual cell populations during pulmonary fibrosis that are important for disease pathogenesis. Objectives: To determine whether single-cell RNA sequencing can reveal disease-related heterogeneity within alveolar macrophages, epithelial cells, or other cell types in lung tissue from subjects with pulmonary fibrosis compared with control subjects. Methods: We performed single-cell RNA sequencing on lung tissue obtained from eight transplant donors and eight recipients with pulmonary fibrosis and on one bronchoscopic cryobiospy sample from a patient with idiopathic pulmonary fibrosis. We validated these data using in situ RNA hybridization, immunohistochemistry, and bulk RNA-sequencing on flow-sorted cells from 22 additional subjects. Measurements and Main Results: We identified a distinct, novel population of profibrotic alveolar macrophages exclusively in patients with fibrosis. Within epithelial cells, the expression of genes involved in Wnt secretion and response was restricted to nonoverlapping cells. We identified rare cell populations including airway stem cells and senescent cells emerging during pulmonary fibrosis. We developed a web-based tool to explore these data. Conclusions: We generated a single-cell atlas of pulmonary fibrosis. Using this atlas, we demonstrated heterogeneity within alveolar macrophages and epithelial cells from subjects with pulmonary fibrosis. These results support the feasibility of discovery-based approaches using next-generation sequencing technologies to identify signaling pathways for targeting in the development of personalized therapies for patients with pulmonary fibrosis. Rationale: The contributions of diverse cell populations in the human lung to pulmonary fibrosis pathogenesis are poorly understood. Single-cell RNA sequencing can reveal changes within individual cell populations during pulmonary fibrosis that are important for disease pathogenesis. Objectives: To determine whether single-cell RNA sequencing can reveal disease-related heterogeneity within alveolar macrophages, epithelial cells, or other cell types in lung tissue from subjects with pulmonary fibrosis compared with control subjects. Methods: We performed single-cell RNA sequencing on lung tissue obtained from eight transplant donors and eight recipients with pulmonary fibrosis and on one bronchoscopic cryobiospy sample from a patient with idiopathic pulmonary fibrosis. We validated these data using in situ RNA hybridization, immunohistochemistry, and bulk RNA-sequencing on flow-sorted cells from 22 additional subjects. Measurements and Main Results: We identified a distinct, novel population of profibrotic alveolar macrophages exclusively in patients with fibrosis. Within epithelial cells, the expression of genes involved in Wnt secretion and response was restricted to nonoverlapping cells. We identified rare cell populations including airway stem cells and senescent cells emerging during pulmonary fibrosis. We developed a web-based tool to explore these data. Conclusions: We generated a single-cell atlas of pulmonary fibrosis. Using this atlas, we demonstrated heterogeneity within alveolar macrophages and epithelial cells from subjects with pulmonary fibrosis. These results support the feasibility of discovery-based approaches using next-generation sequencing technologies to identify signaling pathways for targeting in the development of personalized therapies for patients with pulmonary fibrosis. |
| Author | Nam, Kiwon Hinchcliff, Monique Shilatifard, Ali Walter, James M. Watanabe, Satoshi Yeldandi, Anjana V. Akbarpour, Mahzad Bharat, Ankit Ridge, Karen M. Han, SeungHye Verma, Rohan Bag, Remzi McQuattie-Pimentel, Alexandra C. Anekalla, Kishore R. Argento, A. Christine Bhorade, Sangeeta M. Lam, Anna P. Hrusch, Cara L. Sznajder, Jacob I. Gonzalez-Gonzalez, Francisco J. Hamanaka, Robert B. Fernandez, Ramiro Flozak, Annette S. Gillespie, Colin T. Ren, Ziyou Marshall, Stacy A. Perlman, Harris Misharin, Alexander V. Soberanes, Saul Jain, Manu Amaral, Luis A. N. Chen, Ching-I Bonham, Catherine A. Joshi, Nikita Singer, Benjamin D. Williams, Kinola J. N. Morgan, Vince K. Chi, Monica Dematte, Jane Winter, Deborah R. Guzy, Robert D. Gottardi, Cara J. Reyfman, Paul A. Abdala-Valencia, Hiam Budinger, G. R. Scott Mutlu, Gökhan M. Sperling, Anne I. Nicholson, Trevor T. Chiu, Stephen |
| Author_xml | – sequence: 1 givenname: Paul A. orcidid: 0000-0002-6435-6001 surname: Reyfman fullname: Reyfman, Paul A. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 2 givenname: James M. orcidid: 0000-0001-7428-3101 surname: Walter fullname: Walter, James M. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 3 givenname: Nikita orcidid: 0000-0001-8330-0663 surname: Joshi fullname: Joshi, Nikita organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 4 givenname: Kishore R. orcidid: 0000-0002-8366-5782 surname: Anekalla fullname: Anekalla, Kishore R. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 5 givenname: Alexandra C. surname: McQuattie-Pimentel fullname: McQuattie-Pimentel, Alexandra C. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 6 givenname: Stephen surname: Chiu fullname: Chiu, Stephen organization: Division of Thoracic Surgery, Department of Surgery – sequence: 7 givenname: Ramiro surname: Fernandez fullname: Fernandez, Ramiro organization: Division of Thoracic Surgery, Department of Surgery – sequence: 8 givenname: Mahzad surname: Akbarpour fullname: Akbarpour, Mahzad organization: Division of Thoracic Surgery, Department of Surgery – sequence: 9 givenname: Ching-I surname: Chen fullname: Chen, Ching-I organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 10 givenname: Ziyou surname: Ren fullname: Ren, Ziyou organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 11 givenname: Rohan surname: Verma fullname: Verma, Rohan organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 12 givenname: Hiam surname: Abdala-Valencia fullname: Abdala-Valencia, Hiam organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 13 givenname: Kiwon surname: Nam fullname: Nam, Kiwon organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 14 givenname: Monica surname: Chi fullname: Chi, Monica organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 15 givenname: SeungHye surname: Han fullname: Han, SeungHye organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 16 givenname: Francisco J. surname: Gonzalez-Gonzalez fullname: Gonzalez-Gonzalez, Francisco J. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 17 givenname: Saul surname: Soberanes fullname: Soberanes, Saul organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 18 givenname: Satoshi surname: Watanabe fullname: Watanabe, Satoshi organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 19 givenname: Kinola J. N. surname: Williams fullname: Williams, Kinola J. N. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 20 givenname: Annette S. surname: Flozak fullname: Flozak, Annette S. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 21 givenname: Trevor T. surname: Nicholson fullname: Nicholson, Trevor T. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 22 givenname: Vince K. surname: Morgan fullname: Morgan, Vince K. organization: Division of Rheumatology, Department of Medicine – sequence: 23 givenname: Deborah R. surname: Winter fullname: Winter, Deborah R. organization: Division of Rheumatology, Department of Medicine – sequence: 24 givenname: Monique surname: Hinchcliff fullname: Hinchcliff, Monique organization: Division of Rheumatology, Department of Medicine – sequence: 25 givenname: Cara L. surname: Hrusch fullname: Hrusch, Cara L. organization: Section of Pulmonary and Critical Care Medicine, University of Chicago, Chicago, Illinois; and – sequence: 26 givenname: Robert D. surname: Guzy fullname: Guzy, Robert D. organization: Section of Pulmonary and Critical Care Medicine, University of Chicago, Chicago, Illinois; and – sequence: 27 givenname: Catherine A. surname: Bonham fullname: Bonham, Catherine A. organization: Section of Pulmonary and Critical Care Medicine, University of Chicago, Chicago, Illinois; and – sequence: 28 givenname: Anne I. surname: Sperling fullname: Sperling, Anne I. organization: Section of Pulmonary and Critical Care Medicine, University of Chicago, Chicago, Illinois; and – sequence: 29 givenname: Remzi surname: Bag fullname: Bag, Remzi organization: Section of Pulmonary and Critical Care Medicine, University of Chicago, Chicago, Illinois; and – sequence: 30 givenname: Robert B. orcidid: 0000-0002-8909-356X surname: Hamanaka fullname: Hamanaka, Robert B. organization: Section of Pulmonary and Critical Care Medicine, University of Chicago, Chicago, Illinois; and – sequence: 31 givenname: Gökhan M. surname: Mutlu fullname: Mutlu, Gökhan M. organization: Section of Pulmonary and Critical Care Medicine, University of Chicago, Chicago, Illinois; and – sequence: 32 givenname: Anjana V. surname: Yeldandi fullname: Yeldandi, Anjana V. organization: Department of Pathology, and – sequence: 33 givenname: Stacy A. surname: Marshall fullname: Marshall, Stacy A. organization: Department of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, Illinois – sequence: 34 givenname: Ali surname: Shilatifard fullname: Shilatifard, Ali organization: Department of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, Illinois – sequence: 35 givenname: Luis A. N. surname: Amaral fullname: Amaral, Luis A. N. organization: Department of Chemical and Biological Engineering, Weinberg College of Arts and Sciences, Northwestern University, Evanston, Illinois – sequence: 36 givenname: Harris surname: Perlman fullname: Perlman, Harris organization: Division of Rheumatology, Department of Medicine – sequence: 37 givenname: Jacob I. surname: Sznajder fullname: Sznajder, Jacob I. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 38 givenname: A. Christine surname: Argento fullname: Argento, A. Christine organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine, Division of Thoracic Surgery, Department of Surgery – sequence: 39 givenname: Colin T. surname: Gillespie fullname: Gillespie, Colin T. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine, Division of Thoracic Surgery, Department of Surgery – sequence: 40 givenname: Jane surname: Dematte fullname: Dematte, Jane organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 41 givenname: Manu surname: Jain fullname: Jain, Manu organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 42 givenname: Benjamin D. orcidid: 0000-0001-5775-8427 surname: Singer fullname: Singer, Benjamin D. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine, Department of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, Illinois – sequence: 43 givenname: Karen M. surname: Ridge fullname: Ridge, Karen M. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 44 givenname: Anna P. surname: Lam fullname: Lam, Anna P. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 45 givenname: Ankit surname: Bharat fullname: Bharat, Ankit organization: Division of Thoracic Surgery, Department of Surgery – sequence: 46 givenname: Sangeeta M. surname: Bhorade fullname: Bhorade, Sangeeta M. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 47 givenname: Cara J. surname: Gottardi fullname: Gottardi, Cara J. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 48 givenname: G. R. Scott orcidid: 0000-0002-3114-5208 surname: Budinger fullname: Budinger, G. R. Scott organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine – sequence: 49 givenname: Alexander V. orcidid: 0000-0003-2879-3789 surname: Misharin fullname: Misharin, Alexander V. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30554520$$D View this record in MEDLINE/PubMed |
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| Keywords | RNA sequencing alveolar type II cells alveolar macrophages pulmonary fibrosis |
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| Snippet | The contributions of diverse cell populations in the human lung to pulmonary fibrosis pathogenesis are poorly understood. Single-cell RNA sequencing can reveal... Rationale: The contributions of diverse cell populations in the human lung to pulmonary fibrosis pathogenesis are poorly understood. Single-cell RNA sequencing... Rationale: The contributions of diverse cell populations in the human lung to pulmonary fibrosis pathogenesis are poorly understood. Single-cell RNA sequencing... |
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| SubjectTerms | Animals Biopsy Cells, Cultured - pathology Critical care Disease Disease Models, Animal Epithelial Cells - pathology Female Flow cytometry Gene expression Histology Humans Idiopathic Pulmonary Fibrosis - genetics Idiopathic Pulmonary Fibrosis - pathology Male Medicine Original Pathogenesis Patients Pulmonary fibrosis Sequence Analysis, RNA Stem Cells - pathology Thoracic surgery Transcriptome Transplants & implants |
| Title | Single-Cell Transcriptomic Analysis of Human Lung Provides Insights into the Pathobiology of Pulmonary Fibrosis |
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