Discovery of methylated circulating DNA biomarkers for comprehensive non-invasive monitoring of treatment response in metastatic colorectal cancer

ObjectiveMutations in cell-free circulating DNA (cfDNA) have been studied for tracking disease relapse in colorectal cancer (CRC). This approach requires personalised assay design due to the lack of universally mutated genes. In contrast, early methylation alterations are restricted to defined genom...

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Published in:	Gut Vol. 67; no. 11; pp. 1995 - 2005
Main Authors:	Barault, Ludovic, Amatu, Alessio, Siravegna, Giulia, Ponzetti, Agostino, Moran, Sebastian, Cassingena, Andrea, Mussolin, Benedetta, Falcomatà, Chiara, Binder, Alexandra M, Cristiano, Carmen, Oddo, Daniele, Guarrera, Simonetta, Cancelliere, Carlotta, Bustreo, Sara, Bencardino, Katia, Maden, Sean, Vanzati, Alice, Zavattari, Patrizia, Matullo, Giuseppe, Truini, Mauro, Grady, William M, Racca, Patrizia, Michels, Karin B, Siena, Salvatore, Esteller, Manel, Bardelli, Alberto, Sartore-Bianchi, Andrea, Di Nicolantonio, Federica
Format:	Journal Article
Language:	English
Published:	England BMJ Publishing Group LTD 01.11.2018
Subjects:	Adult Aged Antineoplastic Agents - therapeutic use Biomarkers Biomarkers, Tumor - blood Biomarkers, Tumor - genetics Biopsy Cell Line, Tumor Cell-Free Nucleic Acids - drug effects Cell-Free Nucleic Acids - genetics Cell-Free Nucleic Acids - metabolism Chemotherapy Clinical trials Colorectal cancer Colorectal carcinoma Colorectal Neoplasms - drug therapy Colorectal Neoplasms - genetics Colorectal Neoplasms - metabolism Datasets Deoxyribonucleic acid DNA DNA methylation DNA Methylation - genetics DNA microarrays Drug Monitoring - methods Epigenetics Female Gene expression Genomes Humans Longitudinal Studies Male Metastases Metastasis Middle Aged Mutation Oligonucleotide Array Sequence Analysis - methods Patients Pharmacodynamics Polymerase Chain Reaction Population studies Studies Treatment Outcome Tumors screening tumour markers colorectal cancer chemotherapy methylation
ISSN:	0017-5749, 1468-3288, 1468-3288
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Abstract	ObjectiveMutations in cell-free circulating DNA (cfDNA) have been studied for tracking disease relapse in colorectal cancer (CRC). This approach requires personalised assay design due to the lack of universally mutated genes. In contrast, early methylation alterations are restricted to defined genomic loci allowing comprehensive assay design for population studies. Our objective was to identify cancer-specific methylated biomarkers which could be measured longitudinally in cfDNA (liquid biopsy) to monitor therapeutic outcome in patients with metastatic CRC (mCRC).DesignGenome-wide methylation microarrays of CRC cell lines (n=149) identified five cancer-specific methylated loci (EYA4, GRIA4, ITGA4, MAP3K14-AS1, MSC). Digital PCR assays were employed to measure methylation of these genes in tumour tissue DNA (n=82) and cfDNA from patients with mCRC (n=182). Plasma longitudinal assessment was performed in a patient subset treated with chemotherapy or targeted therapy.ResultsMethylation in at least one marker was detected in all tumour tissue samples and in 156 mCRC patient cfDNA samples (85.7%). Plasma marker prevalence was 71.4% for EYA4, 68.5% for GRIA4, 69.7% for ITGA4, 69.1% for MAP3K14-AS1% and 65.1% for MSC. Dynamics of methylation markers was not affected by treatment type and correlated with objective tumour response and progression-free survival.ConclusionThis five-gene methylation panel can be used to circumvent the absence of patient-specific mutations for monitoring tumour burden dynamics in liquid biopsy under different therapeutic regimens. This method might be proposed for assessing pharmacodynamics in clinical trials or when conventional imaging has limitations.
AbstractList	ObjectiveMutations in cell-free circulating DNA (cfDNA) have been studied for tracking disease relapse in colorectal cancer (CRC). This approach requires personalised assay design due to the lack of universally mutated genes. In contrast, early methylation alterations are restricted to defined genomic loci allowing comprehensive assay design for population studies. Our objective was to identify cancer-specific methylated biomarkers which could be measured longitudinally in cfDNA (liquid biopsy) to monitor therapeutic outcome in patients with metastatic CRC (mCRC).DesignGenome-wide methylation microarrays of CRC cell lines (n=149) identified five cancer-specific methylated loci (EYA4, GRIA4, ITGA4, MAP3K14-AS1, MSC). Digital PCR assays were employed to measure methylation of these genes in tumour tissue DNA (n=82) and cfDNA from patients with mCRC (n=182). Plasma longitudinal assessment was performed in a patient subset treated with chemotherapy or targeted therapy.ResultsMethylation in at least one marker was detected in all tumour tissue samples and in 156 mCRC patient cfDNA samples (85.7%). Plasma marker prevalence was 71.4% for EYA4, 68.5% for GRIA4, 69.7% for ITGA4, 69.1% for MAP3K14-AS1% and 65.1% for MSC. Dynamics of methylation markers was not affected by treatment type and correlated with objective tumour response and progression-free survival.ConclusionThis five-gene methylation panel can be used to circumvent the absence of patient-specific mutations for monitoring tumour burden dynamics in liquid biopsy under different therapeutic regimens. This method might be proposed for assessing pharmacodynamics in clinical trials or when conventional imaging has limitations. Mutations in cell-free circulating DNA (cfDNA) have been studied for tracking disease relapse in colorectal cancer (CRC). This approach requires personalised assay design due to the lack of universally mutated genes. In contrast, early methylation alterations are restricted to defined genomic loci allowing comprehensive assay design for population studies. Our objective was to identify cancer-specific methylated biomarkers which could be measured longitudinally in cfDNA (liquid biopsy) to monitor therapeutic outcome in patients with metastatic CRC (mCRC). Genome-wide methylation microarrays of CRC cell lines (n=149) identified five cancer-specific methylated loci ( , , , ). Digital PCR assays were employed to measure methylation of these genes in tumour tissue DNA (n=82) and cfDNA from patients with mCRC (n=182). Plasma longitudinal assessment was performed in a patient subset treated with chemotherapy or targeted therapy. Methylation in at least one marker was detected in all tumour tissue samples and in 156 mCRC patient cfDNA samples (85.7%). Plasma marker prevalence was 71.4% for , 68.5% for , 69.7% for , 69.1% for and 65.1% for . Dynamics of methylation markers was not affected by treatment type and correlated with objective tumour response and progression-free survival. This five-gene methylation panel can be used to circumvent the absence of patient-specific mutations for monitoring tumour burden dynamics in liquid biopsy under different therapeutic regimens. This method might be proposed for assessing pharmacodynamics in clinical trials or when conventional imaging has limitations. Mutations in cell-free circulating DNA (cfDNA) have been studied for tracking disease relapse in colorectal cancer (CRC). This approach requires personalised assay design due to the lack of universally mutated genes. In contrast, early methylation alterations are restricted to defined genomic loci allowing comprehensive assay design for population studies. Our objective was to identify cancer-specific methylated biomarkers which could be measured longitudinally in cfDNA (liquid biopsy) to monitor therapeutic outcome in patients with metastatic CRC (mCRC).OBJECTIVEMutations in cell-free circulating DNA (cfDNA) have been studied for tracking disease relapse in colorectal cancer (CRC). This approach requires personalised assay design due to the lack of universally mutated genes. In contrast, early methylation alterations are restricted to defined genomic loci allowing comprehensive assay design for population studies. Our objective was to identify cancer-specific methylated biomarkers which could be measured longitudinally in cfDNA (liquid biopsy) to monitor therapeutic outcome in patients with metastatic CRC (mCRC).Genome-wide methylation microarrays of CRC cell lines (n=149) identified five cancer-specific methylated loci (EYA4, GRIA4, ITGA4, MAP3K14-AS1, MSC). Digital PCR assays were employed to measure methylation of these genes in tumour tissue DNA (n=82) and cfDNA from patients with mCRC (n=182). Plasma longitudinal assessment was performed in a patient subset treated with chemotherapy or targeted therapy.DESIGNGenome-wide methylation microarrays of CRC cell lines (n=149) identified five cancer-specific methylated loci (EYA4, GRIA4, ITGA4, MAP3K14-AS1, MSC). Digital PCR assays were employed to measure methylation of these genes in tumour tissue DNA (n=82) and cfDNA from patients with mCRC (n=182). Plasma longitudinal assessment was performed in a patient subset treated with chemotherapy or targeted therapy.Methylation in at least one marker was detected in all tumour tissue samples and in 156 mCRC patient cfDNA samples (85.7%). Plasma marker prevalence was 71.4% for EYA4, 68.5% for GRIA4, 69.7% for ITGA4, 69.1% for MAP3K14-AS1% and 65.1% for MSC. Dynamics of methylation markers was not affected by treatment type and correlated with objective tumour response and progression-free survival.RESULTSMethylation in at least one marker was detected in all tumour tissue samples and in 156 mCRC patient cfDNA samples (85.7%). Plasma marker prevalence was 71.4% for EYA4, 68.5% for GRIA4, 69.7% for ITGA4, 69.1% for MAP3K14-AS1% and 65.1% for MSC. Dynamics of methylation markers was not affected by treatment type and correlated with objective tumour response and progression-free survival.This five-gene methylation panel can be used to circumvent the absence of patient-specific mutations for monitoring tumour burden dynamics in liquid biopsy under different therapeutic regimens. This method might be proposed for assessing pharmacodynamics in clinical trials or when conventional imaging has limitations.CONCLUSIONThis five-gene methylation panel can be used to circumvent the absence of patient-specific mutations for monitoring tumour burden dynamics in liquid biopsy under different therapeutic regimens. This method might be proposed for assessing pharmacodynamics in clinical trials or when conventional imaging has limitations.
Author	Michels, Karin B Cassingena, Andrea Oddo, Daniele Bustreo, Sara Matullo, Giuseppe Cristiano, Carmen Esteller, Manel Di Nicolantonio, Federica Sartore-Bianchi, Andrea Bencardino, Katia Falcomatà, Chiara Racca, Patrizia Zavattari, Patrizia Barault, Ludovic Grady, William M Truini, Mauro Siravegna, Giulia Guarrera, Simonetta Moran, Sebastian Siena, Salvatore Maden, Sean Bardelli, Alberto Vanzati, Alice Ponzetti, Agostino Binder, Alexandra M Amatu, Alessio Mussolin, Benedetta Cancelliere, Carlotta
AuthorAffiliation	12 Department of Physiological Sciences II, School of Medicine, University of Barcelona, Barcelona, Catalonia, Spain 6 Cancer Epigenetics and Biology Program, Bellvitge Biomedical Research Institute, L’Hospitalet, Barcelona, Catalonia, Spain 2 Candiolo Cancer Institute-FPO, IRCCS, SP 142 km 3.95, 10060 Candiolo (TO), Italy 4 FIRC Institute of Molecular Oncology (IFOM), Milano, Italy 3 Niguarda Cancer Center, Grande Ospedale Metropolitano Niguarda, Milan, Italy 10 Department of Medicine, University of Washington School of Medicine, Seattle, WA 1 Department of Oncology, University of Torino, SP 142 km 3.95, 10060 Candiolo (TO), Italy 9 Unit of Biology and Genetics, Dept. Biomedical Sciences, University of Cagliari, Italy 5 Colorectal Cancer Unit, Medical Oncology Division 1, AOU Città della Salute e della Scienza, San Giovanni Battista Hospital, Turin, Italy 8 Clinical Research Division, Fred Hutchinson Cancer Research Center, Seattle, WA 7 Department of Epidemiology, Fielding School of Public Hea
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Candiolo Cancer Institute-FPO, IRCCS, Candiolo, Italy
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/28982739$$D View this record in MEDLINE/PubMed
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Snippet	ObjectiveMutations in cell-free circulating DNA (cfDNA) have been studied for tracking disease relapse in colorectal cancer (CRC). This approach requires... Mutations in cell-free circulating DNA (cfDNA) have been studied for tracking disease relapse in colorectal cancer (CRC). This approach requires personalised...
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StartPage	1995
SubjectTerms	Adult Aged Antineoplastic Agents - therapeutic use Biomarkers Biomarkers, Tumor - blood Biomarkers, Tumor - genetics Biopsy Cell Line, Tumor Cell-Free Nucleic Acids - drug effects Cell-Free Nucleic Acids - genetics Cell-Free Nucleic Acids - metabolism Chemotherapy Clinical trials Colorectal cancer Colorectal carcinoma Colorectal Neoplasms - drug therapy Colorectal Neoplasms - genetics Colorectal Neoplasms - metabolism Datasets Deoxyribonucleic acid DNA DNA methylation DNA Methylation - genetics DNA microarrays Drug Monitoring - methods Epigenetics Female Gene expression Genomes Humans Longitudinal Studies Male Metastases Metastasis Middle Aged Mutation Oligonucleotide Array Sequence Analysis - methods Patients Pharmacodynamics Polymerase Chain Reaction Population studies Studies Treatment Outcome Tumors
Title	Discovery of methylated circulating DNA biomarkers for comprehensive non-invasive monitoring of treatment response in metastatic colorectal cancer
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