The molecular characteristics of DNA damage and repair related to P53 mutation for predicting the recurrence and immunotherapy response in hepatocellular carcinoma

Abstract Hepatocellular carcinoma (HCC) is one of the leading causes of cancer-related deaths globally, owing to its high recurrence rate of 50 to 70% within five years. Despite known associations of certain DNA damage and repair (DDR) genes with tumor recurrence and drug resistance, a comprehensive...

Full description

Saved in:
Bibliographic Details
Main Authors: Jiayao Ma, Diya Tang, Guangzu Cui, Xiangyang Zhang, Xinwen Wang, Yin Li, Erya Hu, Xin Zhou, Haicong Liu, Qingping Peng, Changjing Cai, Xiangying Deng, Shan Zeng, Yihong Chen, Zemin Xiao
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-025-99853-5
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849314686286168064
author Jiayao Ma
Diya Tang
Guangzu Cui
Xiangyang Zhang
Xinwen Wang
Yin Li
Erya Hu
Xin Zhou
Haicong Liu
Qingping Peng
Changjing Cai
Xiangying Deng
Shan Zeng
Yihong Chen
Zemin Xiao
author_facet Jiayao Ma
Diya Tang
Guangzu Cui
Xiangyang Zhang
Xinwen Wang
Yin Li
Erya Hu
Xin Zhou
Haicong Liu
Qingping Peng
Changjing Cai
Xiangying Deng
Shan Zeng
Yihong Chen
Zemin Xiao
author_sort Jiayao Ma
collection DOAJ
description Abstract Hepatocellular carcinoma (HCC) is one of the leading causes of cancer-related deaths globally, owing to its high recurrence rate of 50 to 70% within five years. Despite known associations of certain DNA damage and repair (DDR) genes with tumor recurrence and drug resistance, a comprehensive understanding of DDR pathways’ role in predicting HCC recurrence and therapeutic responses remains elusive. Addressing this gap could offer significant advancements in prognostic and therapeutic strategies for HCC. This study used 769 RNA sequencing samples from public datasets and 53 samples from Xiangya Hospital for DDR model training and validation. It came out that DDR pathways were significantly enriched in samples with P53 mutations. Next, among the 173 combinations of algorithms and parameters, CoxBoost + RSF, Lasso [fold = 10] + RSF, and Lasso [fold = 50] + RSF demonstrated the best performance. The average AUC values of 1 to 5 years and the average concordance index (C-index) value were around 0.7. The risk scores were increased in tumors with recurrence, P53 mutation, and higher TNM stages. High-risk groups, characterized by enriched DDR pathways, exhibited lower CD8 + T cell infiltration and poorer responses to immunotherapy using atezolizumab and bevacizumab, emphasizing the potential of DDR signatures as valuable prognostic and therapeutic biomarkers. In conclusion, the DDR signatures associated with P53 mutations can predict recurrence and therapeutic response in HCC, highlighting their potential as prognostic and therapeutic biomarkers.
format Article
id doaj-art-11d695fbe064488f81d24ca2f39f0b89
institution Kabale University
issn 2045-2322
language English
publishDate 2025-04-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj-art-11d695fbe064488f81d24ca2f39f0b892025-08-20T03:52:23ZengNature PortfolioScientific Reports2045-23222025-04-0115111710.1038/s41598-025-99853-5The molecular characteristics of DNA damage and repair related to P53 mutation for predicting the recurrence and immunotherapy response in hepatocellular carcinomaJiayao Ma0Diya Tang1Guangzu Cui2Xiangyang Zhang3Xinwen Wang4Yin Li5Erya Hu6Xin Zhou7Haicong Liu8Qingping Peng9Changjing Cai10Xiangying Deng11Shan Zeng12Yihong Chen13Zemin Xiao14Department of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Xiangya Hospital, Central South UniversityDepartment of Oncology, Changde Hospital, Xiangya School of Medicine, Central South University (The first people’s hospital of Changde city)Abstract Hepatocellular carcinoma (HCC) is one of the leading causes of cancer-related deaths globally, owing to its high recurrence rate of 50 to 70% within five years. Despite known associations of certain DNA damage and repair (DDR) genes with tumor recurrence and drug resistance, a comprehensive understanding of DDR pathways’ role in predicting HCC recurrence and therapeutic responses remains elusive. Addressing this gap could offer significant advancements in prognostic and therapeutic strategies for HCC. This study used 769 RNA sequencing samples from public datasets and 53 samples from Xiangya Hospital for DDR model training and validation. It came out that DDR pathways were significantly enriched in samples with P53 mutations. Next, among the 173 combinations of algorithms and parameters, CoxBoost + RSF, Lasso [fold = 10] + RSF, and Lasso [fold = 50] + RSF demonstrated the best performance. The average AUC values of 1 to 5 years and the average concordance index (C-index) value were around 0.7. The risk scores were increased in tumors with recurrence, P53 mutation, and higher TNM stages. High-risk groups, characterized by enriched DDR pathways, exhibited lower CD8 + T cell infiltration and poorer responses to immunotherapy using atezolizumab and bevacizumab, emphasizing the potential of DDR signatures as valuable prognostic and therapeutic biomarkers. In conclusion, the DDR signatures associated with P53 mutations can predict recurrence and therapeutic response in HCC, highlighting their potential as prognostic and therapeutic biomarkers.https://doi.org/10.1038/s41598-025-99853-5P53 mutationDNA damage and repairHCC recurrencePrognostic modelImmunotherapy
spellingShingle Jiayao Ma
Diya Tang
Guangzu Cui
Xiangyang Zhang
Xinwen Wang
Yin Li
Erya Hu
Xin Zhou
Haicong Liu
Qingping Peng
Changjing Cai
Xiangying Deng
Shan Zeng
Yihong Chen
Zemin Xiao
The molecular characteristics of DNA damage and repair related to P53 mutation for predicting the recurrence and immunotherapy response in hepatocellular carcinoma
Scientific Reports
P53 mutation
DNA damage and repair
HCC recurrence
Prognostic model
Immunotherapy
title The molecular characteristics of DNA damage and repair related to P53 mutation for predicting the recurrence and immunotherapy response in hepatocellular carcinoma
title_full The molecular characteristics of DNA damage and repair related to P53 mutation for predicting the recurrence and immunotherapy response in hepatocellular carcinoma
title_fullStr The molecular characteristics of DNA damage and repair related to P53 mutation for predicting the recurrence and immunotherapy response in hepatocellular carcinoma
title_full_unstemmed The molecular characteristics of DNA damage and repair related to P53 mutation for predicting the recurrence and immunotherapy response in hepatocellular carcinoma
title_short The molecular characteristics of DNA damage and repair related to P53 mutation for predicting the recurrence and immunotherapy response in hepatocellular carcinoma
title_sort molecular characteristics of dna damage and repair related to p53 mutation for predicting the recurrence and immunotherapy response in hepatocellular carcinoma
topic P53 mutation
DNA damage and repair
HCC recurrence
Prognostic model
Immunotherapy
url https://doi.org/10.1038/s41598-025-99853-5
work_keys_str_mv AT jiayaoma themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT diyatang themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT guangzucui themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT xiangyangzhang themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT xinwenwang themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT yinli themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT eryahu themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT xinzhou themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT haicongliu themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT qingpingpeng themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT changjingcai themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT xiangyingdeng themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT shanzeng themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT yihongchen themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT zeminxiao themolecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT jiayaoma molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT diyatang molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT guangzucui molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT xiangyangzhang molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT xinwenwang molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT yinli molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT eryahu molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT xinzhou molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT haicongliu molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT qingpingpeng molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT changjingcai molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT xiangyingdeng molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT shanzeng molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT yihongchen molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma
AT zeminxiao molecularcharacteristicsofdnadamageandrepairrelatedtop53mutationforpredictingtherecurrenceandimmunotherapyresponseinhepatocellularcarcinoma