BAL Cell Gene Expression Is Indicative of Outcome and Airway Basal Cell Involvement in Idiopathic Pulmonary Fibrosis
Idiopathic pulmonary fibrosis (IPF) is a fatal disease with a variable and unpredictable course. To determine whether BAL cell gene expression is predictive of survival in IPF. This retrospective study analyzed the BAL transcriptome of three independent IPF cohorts: Freiburg (Germany), Siena (Italy)...
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| Published in: | American journal of respiratory and critical care medicine Vol. 199; no. 5; pp. 622 - 630 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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United States
American Thoracic Society
01.03.2019
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| ISSN: | 1073-449X, 1535-4970, 1535-4970 |
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| Abstract | Idiopathic pulmonary fibrosis (IPF) is a fatal disease with a variable and unpredictable course.
To determine whether BAL cell gene expression is predictive of survival in IPF.
This retrospective study analyzed the BAL transcriptome of three independent IPF cohorts: Freiburg (Germany), Siena (Italy), and Leuven (Belgium) including 212 patients. BAL cells from 20 healthy volunteers, 26 patients with sarcoidosis stage III and IV, and 29 patients with chronic obstructive pulmonary disease were used as control subjects. Survival analysis was performed by Cox models and component-wise boosting. Presence of airway basal cells was tested by immunohistochemistry and flow cytometry.
A total of 1,582 genes were predictive of mortality in the IPF derivation cohort in univariate analyses adjusted for age and sex at false discovery rate less than 0.05. A nine-gene signature, derived from the discovery cohort (Freiburg), performed well in both replication cohorts, Siena (P < 0.0032) and Leuven (P = 0.0033). nCounter expression analysis confirmed the array results (P < 0.0001). The genes associated with mortality in BAL cells were significantly enriched for genes expressed in airway basal cells. Further analyses by gene expression, flow cytometry, and immunohistochemistry showed an increase in airway basal cells in BAL and tissues of IPF compared with control subjects, but not in chronic obstructive pulmonary disease or sarcoidosis.
Our results identify and validate a BAL signature that predicts mortality in IPF and improves the accuracy of outcome prediction based on clinical parameters. The BAL signature associated with mortality unmasks a potential role for airway basal cells in IPF. |
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| AbstractList | Idiopathic pulmonary fibrosis (IPF) is a fatal disease with a variable and unpredictable course.
To determine whether BAL cell gene expression is predictive of survival in IPF.
This retrospective study analyzed the BAL transcriptome of three independent IPF cohorts: Freiburg (Germany), Siena (Italy), and Leuven (Belgium) including 212 patients. BAL cells from 20 healthy volunteers, 26 patients with sarcoidosis stage III and IV, and 29 patients with chronic obstructive pulmonary disease were used as control subjects. Survival analysis was performed by Cox models and component-wise boosting. Presence of airway basal cells was tested by immunohistochemistry and flow cytometry.
A total of 1,582 genes were predictive of mortality in the IPF derivation cohort in univariate analyses adjusted for age and sex at false discovery rate less than 0.05. A nine-gene signature, derived from the discovery cohort (Freiburg), performed well in both replication cohorts, Siena (P < 0.0032) and Leuven (P = 0.0033). nCounter expression analysis confirmed the array results (P < 0.0001). The genes associated with mortality in BAL cells were significantly enriched for genes expressed in airway basal cells. Further analyses by gene expression, flow cytometry, and immunohistochemistry showed an increase in airway basal cells in BAL and tissues of IPF compared with control subjects, but not in chronic obstructive pulmonary disease or sarcoidosis.
Our results identify and validate a BAL signature that predicts mortality in IPF and improves the accuracy of outcome prediction based on clinical parameters. The BAL signature associated with mortality unmasks a potential role for airway basal cells in IPF. Idiopathic pulmonary fibrosis (IPF) is a fatal disease with a variable and unpredictable course.RATIONALEIdiopathic pulmonary fibrosis (IPF) is a fatal disease with a variable and unpredictable course.To determine whether BAL cell gene expression is predictive of survival in IPF.OBJECTIVESTo determine whether BAL cell gene expression is predictive of survival in IPF.This retrospective study analyzed the BAL transcriptome of three independent IPF cohorts: Freiburg (Germany), Siena (Italy), and Leuven (Belgium) including 212 patients. BAL cells from 20 healthy volunteers, 26 patients with sarcoidosis stage III and IV, and 29 patients with chronic obstructive pulmonary disease were used as control subjects. Survival analysis was performed by Cox models and component-wise boosting. Presence of airway basal cells was tested by immunohistochemistry and flow cytometry.METHODSThis retrospective study analyzed the BAL transcriptome of three independent IPF cohorts: Freiburg (Germany), Siena (Italy), and Leuven (Belgium) including 212 patients. BAL cells from 20 healthy volunteers, 26 patients with sarcoidosis stage III and IV, and 29 patients with chronic obstructive pulmonary disease were used as control subjects. Survival analysis was performed by Cox models and component-wise boosting. Presence of airway basal cells was tested by immunohistochemistry and flow cytometry.A total of 1,582 genes were predictive of mortality in the IPF derivation cohort in univariate analyses adjusted for age and sex at false discovery rate less than 0.05. A nine-gene signature, derived from the discovery cohort (Freiburg), performed well in both replication cohorts, Siena (P < 0.0032) and Leuven (P = 0.0033). nCounter expression analysis confirmed the array results (P < 0.0001). The genes associated with mortality in BAL cells were significantly enriched for genes expressed in airway basal cells. Further analyses by gene expression, flow cytometry, and immunohistochemistry showed an increase in airway basal cells in BAL and tissues of IPF compared with control subjects, but not in chronic obstructive pulmonary disease or sarcoidosis.MEASUREMENTS AND MAIN RESULTSA total of 1,582 genes were predictive of mortality in the IPF derivation cohort in univariate analyses adjusted for age and sex at false discovery rate less than 0.05. A nine-gene signature, derived from the discovery cohort (Freiburg), performed well in both replication cohorts, Siena (P < 0.0032) and Leuven (P = 0.0033). nCounter expression analysis confirmed the array results (P < 0.0001). The genes associated with mortality in BAL cells were significantly enriched for genes expressed in airway basal cells. Further analyses by gene expression, flow cytometry, and immunohistochemistry showed an increase in airway basal cells in BAL and tissues of IPF compared with control subjects, but not in chronic obstructive pulmonary disease or sarcoidosis.Our results identify and validate a BAL signature that predicts mortality in IPF and improves the accuracy of outcome prediction based on clinical parameters. The BAL signature associated with mortality unmasks a potential role for airway basal cells in IPF.CONCLUSIONSOur results identify and validate a BAL signature that predicts mortality in IPF and improves the accuracy of outcome prediction based on clinical parameters. The BAL signature associated with mortality unmasks a potential role for airway basal cells in IPF. Rationale: Idiopathic pulmonary fibrosis (IPF) is a fatal disease with a variable and unpredictable course. Objectives: To determine whether BAL cell gene expression is predictive of survival in IPF. Methods: This retrospective study analyzed the BAL transcriptome of three independent IPF cohorts: Freiburg (Germany), Siena (Italy), and Leuven (Belgium) including 212 patients. BAL cells from 20 healthy volunteers, 26 patients with sarcoidosis stage III and IV, and 29 patients with chronic obstructive pulmonary disease were used as control subjects. Survival analysis was performed by Cox models and component-wise boosting. Presence of airway basal cells was tested by immunohistochemistry and flow cytometry. Measurements and Main Results: A total of 1,582 genes were predictive of mortality in the IPF derivation cohort in univariate analyses adjusted for age and sex at false discovery rate less than 0.05. A nine-gene signature, derived from the discovery cohort (Freiburg), performed well in both replication cohorts, Siena (P < 0.0032) and Leuven (P = 0.0033). nCounter expression analysis confirmed the array results (P < 0.0001). The genes associated with mortality in BAL cells were significantly enriched for genes expressed in airway basal cells. Further analyses by gene expression, flow cytometry, and immunohistochemistry showed an increase in airway basal cells in BAL and tissues of IPF compared with control subjects, but not in chronic obstructive pulmonary disease or sarcoidosis. Conclusions: Our results identify and validate a BAL signature that predicts mortality in IPF and improves the accuracy of outcome prediction based on clinical parameters. The BAL signature associated with mortality unmasks a potential role for airway basal cells in IPF. |
| Author | Vuga, Louis Schupp, Jonas C. Bargagli, Elena Lynn, Heather Hohlfeld, Jens M. Herazo-Maya, Jose D. Rittinghausen, Susanne Violette, Shelia Hess, Moritz Jung, Birgit Kaminski, Naftali Xu, Yan Binder, Harald Prasse, Antje Quast, Karsten Krug, Norbert Jaeger, Benedikt Vanaudenaerde, Bart Kayser, Gian Rottoli, Paola Wuyts, Wim A. |
| Author_xml | – sequence: 1 givenname: Antje surname: Prasse fullname: Prasse, Antje organization: Department of Pulmonology, Hannover Medical School, Hannover, Germany, Department of Pneumology and, Fraunhofer Institute for Toxicology and Experimental Medicine, Hannover, Germany, German Center for Lung Research, BREATH, Hannover, Germany – sequence: 2 givenname: Harald surname: Binder fullname: Binder, Harald organization: Institute for Medical Biometry and Statistics, Faculty of Medicine and Medical Center, University of Freiburg, Freiburg, Germany – sequence: 3 givenname: Jonas C. surname: Schupp fullname: Schupp, Jonas C. organization: Department of Pneumology and – sequence: 4 givenname: Gian surname: Kayser fullname: Kayser, Gian organization: Institute of Surgical Pathology, University Medical Center, Freiburg, Germany – sequence: 5 givenname: Elena surname: Bargagli fullname: Bargagli, Elena organization: Respiratory Diseases and Lung Transplantation Unit, AOUS and Siena University, Siena, Italy – sequence: 6 givenname: Benedikt surname: Jaeger fullname: Jaeger, Benedikt organization: Fraunhofer Institute for Toxicology and Experimental Medicine, Hannover, Germany, German Center for Lung Research, BREATH, Hannover, Germany – sequence: 7 givenname: Moritz surname: Hess fullname: Hess, Moritz organization: Institute for Medical Biometry and Statistics, Faculty of Medicine and Medical Center, University of Freiburg, Freiburg, Germany – sequence: 8 givenname: Susanne surname: Rittinghausen fullname: Rittinghausen, Susanne organization: Fraunhofer Institute for Toxicology and Experimental Medicine, Hannover, Germany – sequence: 9 givenname: Louis surname: Vuga fullname: Vuga, Louis organization: Division of Respiratory Medicine, Simmons Center, University of Pittsburgh, Pittsburgh, Pennsylvania – sequence: 10 givenname: Heather surname: Lynn fullname: Lynn, Heather organization: Section of Pulmonary, Critical Care and Sleep Medicine, Yale School of Medicine, New Haven, Connecticut – sequence: 11 givenname: Shelia surname: Violette fullname: Violette, Shelia organization: Biogen Idec Inc., Cambridge, Massachusetts – sequence: 12 givenname: Birgit surname: Jung fullname: Jung, Birgit organization: Boehringer Ingelheim Pharma GmbH & Co. KG Research, Biberach, Germany – sequence: 13 givenname: Karsten surname: Quast fullname: Quast, Karsten organization: Boehringer Ingelheim Pharma GmbH & Co. KG Research, Biberach, Germany – sequence: 14 givenname: Bart surname: Vanaudenaerde fullname: Vanaudenaerde, Bart organization: Department of Respiratory Medicine, University Hospitals Leuven, Leuven, Belgium; and – sequence: 15 givenname: Yan surname: Xu fullname: Xu, Yan organization: Division of Neonatology, Perinatal and Pulmonary Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio – sequence: 16 givenname: Jens M. surname: Hohlfeld fullname: Hohlfeld, Jens M. organization: Fraunhofer Institute for Toxicology and Experimental Medicine, Hannover, Germany, German Center for Lung Research, BREATH, Hannover, Germany – sequence: 17 givenname: Norbert surname: Krug fullname: Krug, Norbert organization: Fraunhofer Institute for Toxicology and Experimental Medicine, Hannover, Germany, German Center for Lung Research, BREATH, Hannover, Germany – sequence: 18 givenname: Jose D. surname: Herazo-Maya fullname: Herazo-Maya, Jose D. organization: Section of Pulmonary, Critical Care and Sleep Medicine, Yale School of Medicine, New Haven, Connecticut – sequence: 19 givenname: Paola surname: Rottoli fullname: Rottoli, Paola organization: Respiratory Diseases and Lung Transplantation Unit, AOUS and Siena University, Siena, Italy – sequence: 20 givenname: Wim A. surname: Wuyts fullname: Wuyts, Wim A. organization: Department of Respiratory Medicine, University Hospitals Leuven, Leuven, Belgium; and – sequence: 21 givenname: Naftali surname: Kaminski fullname: Kaminski, Naftali organization: Section of Pulmonary, Critical Care and Sleep Medicine, Yale School of Medicine, New Haven, Connecticut |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30141961$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright American Thoracic Society Mar 1, 2019 Copyright © 2019 by the American Thoracic Society 2019 |
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| PublicationDate | 2019-03-01 20190301 |
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| PublicationTitle | American journal of respiratory and critical care medicine |
| PublicationTitleAlternate | Am J Respir Crit Care Med |
| PublicationYear | 2019 |
| Publisher | American Thoracic Society |
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| References | bib14 bib15 Prasse A (bib12) 2015; 191 bib13 bib10 bib32 bib11 bib30 bib31 bib29 bib27 bib28 bib25 bib26 bib23 bib24 bib22 bib20 bib9 bib7 bib8 bib5 bib18 bib6 bib19 bib3 bib16 Kaminski N (bib21) 2003; 29 bib4 bib17 bib1 bib2 30183332 - Am J Respir Crit Care Med. 2019 Mar 1;199(5):555-557. doi: 10.1164/rccm.201808-1557ED |
| References_xml | – ident: bib25 doi: 10.1016/j.oooo.2016.05.018 – ident: bib18 doi: 10.1073/pnas.0601231103 – ident: bib20 doi: 10.1242/dmm.006031 – ident: bib6 doi: 10.1164/ajrccm.185.12.1329 – ident: bib13 doi: 10.1164/ajrccm.161.2.ats3-00 – ident: bib5 doi: 10.1126/scitranslmed.3005964 – ident: bib26 doi: 10.1097/01.LAB.0000032380.82232.67 – ident: bib1 doi: 10.7326/0003-4819-142-12_Part_1-200506210-00005 – ident: bib30 doi: 10.1016/S0140-6736(11)60052-4 – ident: bib9 doi: 10.1164/rccm.200808-1313OC – ident: bib29 doi: 10.1136/thx.21.3.272 – ident: bib7 doi: 10.1001/jama.2013.5827 – ident: bib27 doi: 10.1164/rccm.201308-1483ST – ident: bib11 doi: 10.1371/journal.ppat.1004923 – ident: bib14 doi: 10.1164/rccm.2009-040GL – ident: bib31 doi: 10.1016/j.cell.2011.10.001 – ident: bib8 doi: 10.1164/rccm.201202-0320ST – ident: bib16 doi: 10.1371/journal.pone.0018378 – ident: bib19 doi: 10.1172/jci.insight.90558 – ident: bib17 doi: 10.1186/1471-2105-9-14 – ident: bib4 doi: 10.1164/rccm.200808-1201OC – ident: bib2 doi: 10.7326/0003-4819-156-10-201205150-00004 – ident: bib10 doi: 10.1164/rccm.200509-1518OC – ident: bib28 doi: 10.1136/thx.2010.151555 – ident: bib32 doi: 10.1038/nature14112 – ident: bib3 doi: 10.1164/rccm.201105-0840OC – volume: 29 start-page: S32 issue: 3 year: 2003 ident: bib21 publication-title: Am J Respir Cell Mol Biol – ident: bib24 doi: 10.1164/rccm.201403-0541OC – ident: bib22 doi: 10.1136/thoraxjnl-2012-202943 – ident: bib15 doi: 10.1164/rccm.201506-1063ST – volume: 191 start-page: A6358 year: 2015 ident: bib12 publication-title: Am J Respir Crit Care Med – ident: bib23 doi: 10.1378/chest.07-1948 – reference: 30183332 - Am J Respir Crit Care Med. 2019 Mar 1;199(5):555-557. doi: 10.1164/rccm.201808-1557ED |
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| Snippet | Idiopathic pulmonary fibrosis (IPF) is a fatal disease with a variable and unpredictable course.
To determine whether BAL cell gene expression is predictive of... Rationale: Idiopathic pulmonary fibrosis (IPF) is a fatal disease with a variable and unpredictable course. Objectives: To determine whether BAL cell gene... Idiopathic pulmonary fibrosis (IPF) is a fatal disease with a variable and unpredictable course.RATIONALEIdiopathic pulmonary fibrosis (IPF) is a fatal disease... |
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| SubjectTerms | Age Aged Biopsy Bronchoalveolar Lavage Fluid - cytology Chronic obstructive pulmonary disease Female Flow cytometry Gene Expression Gene Expression Profiling Humans Idiopathic Pulmonary Fibrosis - metabolism Idiopathic Pulmonary Fibrosis - mortality Male Mortality Oligonucleotide Array Sequence Analysis Original Physiology Pneumonia Predictive Value of Tests Proportional Hazards Models Pulmonary fibrosis Respiratory Mucosa - metabolism Retrospective Studies Sarcoidosis Stem cells Survival Analysis Thorax Transplants & implants |
| Title | BAL Cell Gene Expression Is Indicative of Outcome and Airway Basal Cell Involvement in Idiopathic Pulmonary Fibrosis |
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