Mutational and low-coverage whole genome sequencing identifies actionable DNA repair alterations in prostate cancer plasma DNA

Abstract PARP inhibitors (PARPi), recently introduced for treating metastatic castration-resistant prostate cancer (mCRPC), have heightened interest in molecular profiling for pathogenic aberrations in homologous recombination DNA repair (HRR) genes in all mCRPC patients. Liquid biopsy offers a viab...

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Main Authors: Alessandra Virga, Milena Urbini, Maurizio Polano, Elisabetta Petracci, Gianluca Tedaldi, Giorgia Gurioli, Giorgia Marisi, Davide Angeli, Andrea Ambrosini-Spaltro, Giovanni De Luca, Ilaria Cangini, Valentina Zampiga, Giovanna Cenacchi, Giuseppe Toffoli, Chiara Casadei, Maria Concetta Cursano, Vincenza Conteduca, Ugo De Giorgi, Paola Ulivi
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-05384-4
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author Alessandra Virga
Milena Urbini
Maurizio Polano
Elisabetta Petracci
Gianluca Tedaldi
Giorgia Gurioli
Giorgia Marisi
Davide Angeli
Andrea Ambrosini-Spaltro
Giovanni De Luca
Ilaria Cangini
Valentina Zampiga
Giovanna Cenacchi
Giuseppe Toffoli
Chiara Casadei
Maria Concetta Cursano
Vincenza Conteduca
Ugo De Giorgi
Paola Ulivi
author_facet Alessandra Virga
Milena Urbini
Maurizio Polano
Elisabetta Petracci
Gianluca Tedaldi
Giorgia Gurioli
Giorgia Marisi
Davide Angeli
Andrea Ambrosini-Spaltro
Giovanni De Luca
Ilaria Cangini
Valentina Zampiga
Giovanna Cenacchi
Giuseppe Toffoli
Chiara Casadei
Maria Concetta Cursano
Vincenza Conteduca
Ugo De Giorgi
Paola Ulivi
author_sort Alessandra Virga
collection DOAJ
description Abstract PARP inhibitors (PARPi), recently introduced for treating metastatic castration-resistant prostate cancer (mCRPC), have heightened interest in molecular profiling for pathogenic aberrations in homologous recombination DNA repair (HRR) genes in all mCRPC patients. Liquid biopsy offers a viable alternative to archival tumor tissue for genetic analysis. In this study, we assessed the feasibility and utility of combining mutational panel sequencing with shallow whole genome sequencing (sWGS) to refine HRR status determination from plasma in prostate cancer (PCa) patients. The mutational profile of 16 HRR genes was assessed in 63 PCa patients: 28.6% of patients harbored putative pathogenic variants in HRR-related genes. A HRR-mutant status was defined for 10 patients (15.8%). Through the integration of sWGS data, plasma samples non-informative about somatic alterations were identified, and germline/somatic origin of HRR mutations was defined. Matched tumor tissue was available for 41 patients, with an 85.7% concordance rate between plasma and tissue mutational analyses. Additionally, we explored the copy number variation (CNV) profile using sWGS and it was found concordant with the literature PCa profiles. Our findings demonstrated that ctDNA analysis through liquid biopsy is a reliable alternative to tissue-based methods for identifying SNVs and CNVs. However, concordance was affected by ctDNA levels in plasma and clonal hematopoiesis. The data highlight the utility of integrating sWGS with targeted mutation analysis for comprehensive molecular profiling of PCa patients.
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spelling doaj-art-c5b5d42ecbfb407d9bf214b8c7b2cdff2025-08-20T03:45:19ZengNature PortfolioScientific Reports2045-23222025-07-0115111410.1038/s41598-025-05384-4Mutational and low-coverage whole genome sequencing identifies actionable DNA repair alterations in prostate cancer plasma DNAAlessandra Virga0Milena Urbini1Maurizio Polano2Elisabetta Petracci3Gianluca Tedaldi4Giorgia Gurioli5Giorgia Marisi6Davide Angeli7Andrea Ambrosini-Spaltro8Giovanni De Luca9Ilaria Cangini10Valentina Zampiga11Giovanna Cenacchi12Giuseppe Toffoli13Chiara Casadei14Maria Concetta Cursano15Vincenza Conteduca16Ugo De Giorgi17Paola Ulivi18Biosciences Laboratory, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Biosciences Laboratory, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Experimental and Clinical Pharmacology Unit, Centro di Riferimento Oncologico di Aviano, Istituto di Ricovero e Cura a Carattere ScientificoUnit of Biostatistics and Clinical Trials, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Biosciences Laboratory, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Biosciences Laboratory, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Biosciences Laboratory, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Unit of Biostatistics and Clinical Trials, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Pathology Unit, “Morgagni-Pierantoni” Hospital, AUSL RomagnaPathology Unit, “Maurizio Bufalini” HospitalBiosciences Laboratory, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Biosciences Laboratory, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Department of Biomedical and Neuromotor Sciences (DIBINEM), University of BolognaExperimental and Clinical Pharmacology Unit, Centro di Riferimento Oncologico di Aviano, Istituto di Ricovero e Cura a Carattere ScientificoMedical Oncology, Breast & GYN Unit, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Department of Medical Oncology, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Department of Medical and Surgical Sciences, Unit of Medical Oncology and Biomolecular Therapy, University of FoggiaDepartment of Medical Oncology, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Biosciences Laboratory, IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori”Abstract PARP inhibitors (PARPi), recently introduced for treating metastatic castration-resistant prostate cancer (mCRPC), have heightened interest in molecular profiling for pathogenic aberrations in homologous recombination DNA repair (HRR) genes in all mCRPC patients. Liquid biopsy offers a viable alternative to archival tumor tissue for genetic analysis. In this study, we assessed the feasibility and utility of combining mutational panel sequencing with shallow whole genome sequencing (sWGS) to refine HRR status determination from plasma in prostate cancer (PCa) patients. The mutational profile of 16 HRR genes was assessed in 63 PCa patients: 28.6% of patients harbored putative pathogenic variants in HRR-related genes. A HRR-mutant status was defined for 10 patients (15.8%). Through the integration of sWGS data, plasma samples non-informative about somatic alterations were identified, and germline/somatic origin of HRR mutations was defined. Matched tumor tissue was available for 41 patients, with an 85.7% concordance rate between plasma and tissue mutational analyses. Additionally, we explored the copy number variation (CNV) profile using sWGS and it was found concordant with the literature PCa profiles. Our findings demonstrated that ctDNA analysis through liquid biopsy is a reliable alternative to tissue-based methods for identifying SNVs and CNVs. However, concordance was affected by ctDNA levels in plasma and clonal hematopoiesis. The data highlight the utility of integrating sWGS with targeted mutation analysis for comprehensive molecular profiling of PCa patients.https://doi.org/10.1038/s41598-025-05384-4Prostate cancerLiquid biopsyPARP inhibitorsLow-coverage WGS
spellingShingle Alessandra Virga
Milena Urbini
Maurizio Polano
Elisabetta Petracci
Gianluca Tedaldi
Giorgia Gurioli
Giorgia Marisi
Davide Angeli
Andrea Ambrosini-Spaltro
Giovanni De Luca
Ilaria Cangini
Valentina Zampiga
Giovanna Cenacchi
Giuseppe Toffoli
Chiara Casadei
Maria Concetta Cursano
Vincenza Conteduca
Ugo De Giorgi
Paola Ulivi
Mutational and low-coverage whole genome sequencing identifies actionable DNA repair alterations in prostate cancer plasma DNA
Scientific Reports
Prostate cancer
Liquid biopsy
PARP inhibitors
Low-coverage WGS
title Mutational and low-coverage whole genome sequencing identifies actionable DNA repair alterations in prostate cancer plasma DNA
title_full Mutational and low-coverage whole genome sequencing identifies actionable DNA repair alterations in prostate cancer plasma DNA
title_fullStr Mutational and low-coverage whole genome sequencing identifies actionable DNA repair alterations in prostate cancer plasma DNA
title_full_unstemmed Mutational and low-coverage whole genome sequencing identifies actionable DNA repair alterations in prostate cancer plasma DNA
title_short Mutational and low-coverage whole genome sequencing identifies actionable DNA repair alterations in prostate cancer plasma DNA
title_sort mutational and low coverage whole genome sequencing identifies actionable dna repair alterations in prostate cancer plasma dna
topic Prostate cancer
Liquid biopsy
PARP inhibitors
Low-coverage WGS
url https://doi.org/10.1038/s41598-025-05384-4
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