Universal lung epithelium DNA methylation markers for detection of lung damage in liquid biopsies.


Journal

The European respiratory journal
ISSN: 1399-3003
Titre abrégé: Eur Respir J
Pays: England
ID NLM: 8803460

Informations de publication

Date de publication:
11 2022
Historique:
received: 06 12 2021
accepted: 15 03 2022
pubmed: 23 4 2022
medline: 8 11 2022
entrez: 22 4 2022
Statut: epublish

Résumé

Circulating biomarkers for lung damage are lacking. Lung epithelium-specific DNA methylation patterns can potentially report the presence of lung-derived cell-free DNA (cfDNA) in blood, as an indication of lung cell death. We sorted human lung alveolar and bronchial epithelial cells from surgical specimens, and obtained their methylomes using whole-genome bisulfite sequencing. We developed a PCR sequencing assay determining the methylation status of 17 loci with lung-specific methylation patterns, and used it to assess lung-derived cfDNA in the plasma of healthy volunteers and patients with lung disease. Loci that are uniquely unmethylated in alveolar or bronchial epithelial cells are enriched for enhancers controlling lung-specific genes. Methylation markers extracted from these methylomes revealed that normal lung cell turnover probably releases cfDNA into the air spaces, rather than to blood. People with advanced lung cancer show a massive elevation of lung cfDNA concentration in blood. Among individuals undergoing bronchoscopy, lung-derived cfDNA is observed in the plasma of those later diagnosed with lung cancer, and to a lesser extent in those diagnosed with other lung diseases. Lung cfDNA is also elevated in patients with acute exacerbation of COPD compared with patients with stable disease, and is associated with future exacerbation and mortality in these patients. Universal cfDNA methylation markers of normal lung epithelium allow for mutation-independent, sensitive and specific detection of lung-derived cfDNA, reporting on ongoing lung injury. Such markers can find broad utility in the study of normal and pathologic human lung dynamics.

Sections du résumé

BACKGROUND
Circulating biomarkers for lung damage are lacking. Lung epithelium-specific DNA methylation patterns can potentially report the presence of lung-derived cell-free DNA (cfDNA) in blood, as an indication of lung cell death.
METHODS
We sorted human lung alveolar and bronchial epithelial cells from surgical specimens, and obtained their methylomes using whole-genome bisulfite sequencing. We developed a PCR sequencing assay determining the methylation status of 17 loci with lung-specific methylation patterns, and used it to assess lung-derived cfDNA in the plasma of healthy volunteers and patients with lung disease.
RESULTS
Loci that are uniquely unmethylated in alveolar or bronchial epithelial cells are enriched for enhancers controlling lung-specific genes. Methylation markers extracted from these methylomes revealed that normal lung cell turnover probably releases cfDNA into the air spaces, rather than to blood. People with advanced lung cancer show a massive elevation of lung cfDNA concentration in blood. Among individuals undergoing bronchoscopy, lung-derived cfDNA is observed in the plasma of those later diagnosed with lung cancer, and to a lesser extent in those diagnosed with other lung diseases. Lung cfDNA is also elevated in patients with acute exacerbation of COPD compared with patients with stable disease, and is associated with future exacerbation and mortality in these patients.
CONCLUSIONS
Universal cfDNA methylation markers of normal lung epithelium allow for mutation-independent, sensitive and specific detection of lung-derived cfDNA, reporting on ongoing lung injury. Such markers can find broad utility in the study of normal and pathologic human lung dynamics.

Identifiants

pubmed: 35450968
pii: 13993003.03056-2021
doi: 10.1183/13993003.03056-2021
pii:
doi:

Substances chimiques

Cell-Free Nucleic Acids 0
Biomarkers 0
Biomarkers, Tumor 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Cancer Research UK
Pays : United Kingdom

Informations de copyright

Copyright ©The authors 2022. For reproduction rights and permissions contact permissions@ersnet.org.

Déclaration de conflit d'intérêts

Conflict of interest: G. Cann, H. Amini, P. Moradi and S. Nagaraju are employees of Grail LLC. J. Magenheim, B. Glaser, T. Kaplan, R. Shemer and Y. Dor have patents on cfDNA methylation markers and methods of analysis. All other authors have no conflict of interest.

Auteurs

Judith Magenheim (J)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.
Equal contributors.

Ariel Rokach (A)

Pulmonary Institute, Shaare Zedek Medical Center, Jerusalem and the Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.
Equal contributors.

Ayelet Peretz (A)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Netanel Loyfer (N)

School of Computer Science and Engineering, The Hebrew University of Jerusalem, Jerusalem, Israel.

Gordon Cann (G)

GRAIL LLC, Menlo Park, CA, USA.

Hamed Amini (H)

GRAIL LLC, Menlo Park, CA, USA.

Patriss Moradi (P)

GRAIL LLC, Menlo Park, CA, USA.

Sudharani Nagaraju (S)

GRAIL LLC, Menlo Park, CA, USA.

Wafa Sameer (W)

Hadassah Medical Center, Institute of Pulmonary Medicine, Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Assaf Cohen (A)

Pulmonary Institute, Shaare Zedek Medical Center, Jerusalem and the Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Ophir Fogel (O)

Pulmonary Institute, Shaare Zedek Medical Center, Jerusalem and the Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Rottem Kuint (R)

Hadassah Medical Center, Institute of Pulmonary Medicine, Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Avraham Abutbul (A)

Hadassah Medical Center, Institute of Pulmonary Medicine, Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Aiman Abu Rmeileh (A)

Hadassah Medical Center, Institute of Pulmonary Medicine, Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Mutaz Karameh (M)

Hadassah Medical Center, Institute of Pulmonary Medicine, Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Polina Cohen Goichman (P)

Hadassah Medical Center, Institute of Pulmonary Medicine, Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Ori Wald (O)

Dept of Cardiothoracic Surgery, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Amit Korach (A)

Dept of Cardiothoracic Surgery, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Daniel Neiman (D)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Ilana Fox-Fisher (I)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Joshua Moss (J)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Daniel Cohen (D)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Sheina Piyanzin (S)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Roni Ben Ami (R)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Ahmad Quteineh (A)

The Institute of Pediatric Gastroenterology and Nutrition, Shaare Zedek Medical Center, Jerusalem, Israel.

Eliahu Golomb (E)

Dept of Pathology, Shaare Zedek Medical Center, Hebrew University of Jerusalem, Jerusalem, Israel.

Ruth Shemer (R)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Benjamin Glaser (B)

Dept of Endocrinology and Metabolism, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Tommy Kaplan (T)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.
School of Computer Science and Engineering, The Hebrew University of Jerusalem, Jerusalem, Israel.

Zvi G Fridlender (ZG)

Hadassah Medical Center, Institute of Pulmonary Medicine, Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.
Z.G. Fridlender and Y. Dor contributed equally to this article as lead authors.

Yuval Dor (Y)

Dept of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel yuvald@ekmd.huji.ac.il.
Z.G. Fridlender and Y. Dor contributed equally to this article as lead authors.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH