Serum DNA methylome of the colorectal cancer serrated pathway enables non‐invasive detection

The clinical relevance of the colorectal cancer serrated pathway is evident, but the screening of serrated lesions remains challenging. We aimed to characterize the serum methylome of the serrated pathway and to evaluate circulating cell‐free DNA (cfDNA) methylomes as a potential source of biomarker...

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Main Authors: María Gallardo‐Gómez, Lara Costas‐Ríos, Carlos A. Garcia‐Prieto, Lara Álvarez‐Rodríguez, Luis Bujanda, Maialen Barrero, Antoni Castells, Francesc Balaguer, Rodrigo Jover, Manel Esteller, Antoni Tardío Baiges, Joaquín González‐Carreró Fojón, Joaquín Cubiella, Loretta De Chiara
Format: Article
Language:English
Published: Wiley 2024-11-01
Series:Molecular Oncology
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Online Access:https://doi.org/10.1002/1878-0261.13573
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author María Gallardo‐Gómez
Lara Costas‐Ríos
Carlos A. Garcia‐Prieto
Lara Álvarez‐Rodríguez
Luis Bujanda
Maialen Barrero
Antoni Castells
Francesc Balaguer
Rodrigo Jover
Manel Esteller
Antoni Tardío Baiges
Joaquín González‐Carreró Fojón
Joaquín Cubiella
Loretta De Chiara
author_facet María Gallardo‐Gómez
Lara Costas‐Ríos
Carlos A. Garcia‐Prieto
Lara Álvarez‐Rodríguez
Luis Bujanda
Maialen Barrero
Antoni Castells
Francesc Balaguer
Rodrigo Jover
Manel Esteller
Antoni Tardío Baiges
Joaquín González‐Carreró Fojón
Joaquín Cubiella
Loretta De Chiara
author_sort María Gallardo‐Gómez
collection DOAJ
description The clinical relevance of the colorectal cancer serrated pathway is evident, but the screening of serrated lesions remains challenging. We aimed to characterize the serum methylome of the serrated pathway and to evaluate circulating cell‐free DNA (cfDNA) methylomes as a potential source of biomarkers for the non‐invasive detection of serrated lesions. We collected serum samples from individuals with serrated adenocarcinoma (SAC), traditional serrated adenomas, sessile serrated lesions, hyperplastic polyps and individuals with no colorectal findings. First, we quantified cfDNA methylation with the MethylationEPIC array. Then, we compared the methylation profiles with tissue and serum datasets. Finally, we evaluated the utility of serum cfDNA methylation biomarkers. We identified a differential methylation profile able to distinguish high‐risk serrated lesions from no serrated neoplasia, showing concordance with tissue methylation from SAC and sessile serrated lesions. Serum methylation profiles are pathway‐specific, clearly separating serrated lesions from conventional adenomas. The combination of ninjurin 2 (NINJ2) and glutamate‐rich 1 (ERICH1) methylation discriminated high‐risk serrated lesions and SAC with 91.4% sensitivity (64.4% specificity), while zinc finger protein 718 (ZNF718) methylation reported 100% sensitivity for the detection of SAC (96% specificity). This is the first study exploring the serum methylome of serrated lesions. Differential methylation of cfDNA can be used for the non‐invasive detection of colorectal serrated lesions.
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spelling doaj-art-52a5b5b7bba14705bc89a233d4909de92025-08-20T02:13:15ZengWileyMolecular Oncology1574-78911878-02612024-11-0118112696271310.1002/1878-0261.13573Serum DNA methylome of the colorectal cancer serrated pathway enables non‐invasive detectionMaría Gallardo‐Gómez0Lara Costas‐Ríos1Carlos A. Garcia‐Prieto2Lara Álvarez‐Rodríguez3Luis Bujanda4Maialen Barrero5Antoni Castells6Francesc Balaguer7Rodrigo Jover8Manel Esteller9Antoni Tardío Baiges10Joaquín González‐Carreró Fojón11Joaquín Cubiella12Loretta De Chiara13CINBIO, Universidade de Vigo SpainCINBIO, Universidade de Vigo SpainJosep Carreras Leukaemia Research Institute (IJC) Badalona SpainCINBIO, Universidade de Vigo SpainDepartment of Gastroenterology, Biodonostia Health Research Institute, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd) Universidad del País Vasco (UPV/EHU) San Sebastián SpainDepartment of Oncology Hospital Universitario Donostia San Sebastián SpainGastroenterology Department, Hospital Clínic, IDIBAPS, CIBERehd University of Barcelona SpainGastroenterology Department, Hospital Clínic, IDIBAPS, CIBERehd University of Barcelona SpainServicio de Medicina Digestiva, Hospital General Universitario Dr. Balmis ISABIAL Universidad Miguel Hernández Alicante SpainJosep Carreras Leukaemia Research Institute (IJC) Badalona SpainDepartment of Pathology Hospital Álvaro Cunqueiro, Instituto de Investigación Biomédica Galicia Sur Vigo SpainDepartment of Pathology Hospital Álvaro Cunqueiro, Instituto de Investigación Biomédica Galicia Sur Vigo SpainDepartment of Gastroenterology Complexo Hospitalario Universitario de Ourense, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd) Ourense SpainCINBIO, Universidade de Vigo SpainThe clinical relevance of the colorectal cancer serrated pathway is evident, but the screening of serrated lesions remains challenging. We aimed to characterize the serum methylome of the serrated pathway and to evaluate circulating cell‐free DNA (cfDNA) methylomes as a potential source of biomarkers for the non‐invasive detection of serrated lesions. We collected serum samples from individuals with serrated adenocarcinoma (SAC), traditional serrated adenomas, sessile serrated lesions, hyperplastic polyps and individuals with no colorectal findings. First, we quantified cfDNA methylation with the MethylationEPIC array. Then, we compared the methylation profiles with tissue and serum datasets. Finally, we evaluated the utility of serum cfDNA methylation biomarkers. We identified a differential methylation profile able to distinguish high‐risk serrated lesions from no serrated neoplasia, showing concordance with tissue methylation from SAC and sessile serrated lesions. Serum methylation profiles are pathway‐specific, clearly separating serrated lesions from conventional adenomas. The combination of ninjurin 2 (NINJ2) and glutamate‐rich 1 (ERICH1) methylation discriminated high‐risk serrated lesions and SAC with 91.4% sensitivity (64.4% specificity), while zinc finger protein 718 (ZNF718) methylation reported 100% sensitivity for the detection of SAC (96% specificity). This is the first study exploring the serum methylome of serrated lesions. Differential methylation of cfDNA can be used for the non‐invasive detection of colorectal serrated lesions.https://doi.org/10.1002/1878-0261.13573circulating cell‐free DNADNA methylationnon‐invasive biomarkersscreeningserrated colorectal cancerserrated lesions
spellingShingle María Gallardo‐Gómez
Lara Costas‐Ríos
Carlos A. Garcia‐Prieto
Lara Álvarez‐Rodríguez
Luis Bujanda
Maialen Barrero
Antoni Castells
Francesc Balaguer
Rodrigo Jover
Manel Esteller
Antoni Tardío Baiges
Joaquín González‐Carreró Fojón
Joaquín Cubiella
Loretta De Chiara
Serum DNA methylome of the colorectal cancer serrated pathway enables non‐invasive detection
Molecular Oncology
circulating cell‐free DNA
DNA methylation
non‐invasive biomarkers
screening
serrated colorectal cancer
serrated lesions
title Serum DNA methylome of the colorectal cancer serrated pathway enables non‐invasive detection
title_full Serum DNA methylome of the colorectal cancer serrated pathway enables non‐invasive detection
title_fullStr Serum DNA methylome of the colorectal cancer serrated pathway enables non‐invasive detection
title_full_unstemmed Serum DNA methylome of the colorectal cancer serrated pathway enables non‐invasive detection
title_short Serum DNA methylome of the colorectal cancer serrated pathway enables non‐invasive detection
title_sort serum dna methylome of the colorectal cancer serrated pathway enables non invasive detection
topic circulating cell‐free DNA
DNA methylation
non‐invasive biomarkers
screening
serrated colorectal cancer
serrated lesions
url https://doi.org/10.1002/1878-0261.13573
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