Development and validation of a 14-CpG DNA methylation signature and drug targets for prognostic prediction in breast cancer

BackgroundBreast cancer (BC) is the most prevalent cancer among women and a leading cause of cancer-related deaths worldwide. Emerging evidence suggests that DNA methylation, a well-studied epigenetic modification, regulates various cellular processes critical for cancer development and progression...

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Main Authors: Bao-xing Tian, Zhi-xi Yu, Xia Qiu, Li-ping Chen, Yu-lian Zhuang, Qian Chen, Yan-hua Gu, Meng-jie Hou, Yi-fan Gu
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-03-01
Series:Frontiers in Medicine
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Online Access:https://www.frontiersin.org/articles/10.3389/fmed.2025.1548726/full
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author Bao-xing Tian
Zhi-xi Yu
Xia Qiu
Li-ping Chen
Yu-lian Zhuang
Qian Chen
Yan-hua Gu
Meng-jie Hou
Yi-fan Gu
author_facet Bao-xing Tian
Zhi-xi Yu
Xia Qiu
Li-ping Chen
Yu-lian Zhuang
Qian Chen
Yan-hua Gu
Meng-jie Hou
Yi-fan Gu
author_sort Bao-xing Tian
collection DOAJ
description BackgroundBreast cancer (BC) is the most prevalent cancer among women and a leading cause of cancer-related deaths worldwide. Emerging evidence suggests that DNA methylation, a well-studied epigenetic modification, regulates various cellular processes critical for cancer development and progression and holds promise as a biomarker for cancer diagnosis and prognosis, potentially enhancing the efficacy of precision therapies.MethodsWe developed a robust prognostic model for BC based on DNA methylation and clinical data from The Cancer Genome Atlas (TCGA) and Gene Expression Omnibus (GEO). We analyzed the association of the model with clinicopathological features, survival outcomes, and chemotherapy drug sensitivity.ResultsA set of 216 differentially methylated CpGs was identified by intersecting three datasets (TCGA, GSE22249, and GSE66695). Using univariate Cox proportional hazard and LASSO Cox regression analyses, we constructed a 14-CpG model significantly associated with progression-free interval (PFI), disease-specific survival (DSS), and overall survival (OS) in BC patients. Kaplan–Meier (KM) survival analysis, receiver operating characteristic (ROC) analysis, and nomogram validation confirmed the clinical value of the signature. The Cox analysis showed a significant association between the signature and PFI and DSS in BC patients. KM analysis effectively distinguished high-risk from low-risk patients, while ROC analysis demonstrated high sensitivity and specificity in predicting BC prognosis. A nomogram based on the signature effectively predicted 5- and 10-year PFI and DSS. Additionally, combining our model with clinical risk factors suggested that patients in the I–II & M+ subgroup could benefit from adjuvant chemotherapy regarding PFI, DSS, and OS. Gene Ontology (GO) functional enrichment and KEGG pathway analyses indicated that the top 3,000 differentially expressed genes (DEGs) were enriched in pathways related to DNA replication and repair and cell cycle regulation. Patients in the high-risk group might benefit from drugs targeting DNA replication and repair processes in tumor cells.ConclusionThe 14-CpG model serves as a useful biomarker for predicting prognosis in BC patients. When combined with TNM staging, it offers a potential strategy for individualized clinical decision-making, guiding personalized therapeutic regimen selection for clinicians.
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spelling doaj-art-5780069d56cb41e9b668abb56ae220382025-08-20T02:51:53ZengFrontiers Media S.A.Frontiers in Medicine2296-858X2025-03-011210.3389/fmed.2025.15487261548726Development and validation of a 14-CpG DNA methylation signature and drug targets for prognostic prediction in breast cancerBao-xing Tian0Zhi-xi Yu1Xia Qiu2Li-ping Chen3Yu-lian Zhuang4Qian Chen5Yan-hua Gu6Meng-jie Hou7Yi-fan Gu8Hongqiao International Institute of Medicine, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaShanghai Key Laboratory of Tissue Engineering, Department of Plastic and Reconstructive Surgery, Shanghai 9th People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Breast Surgery, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Breast Surgery, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Nursing, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Nursing, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Nursing, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaShanghai Key Laboratory of Tissue Engineering, Department of Plastic and Reconstructive Surgery, Shanghai 9th People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Breast Surgery, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaBackgroundBreast cancer (BC) is the most prevalent cancer among women and a leading cause of cancer-related deaths worldwide. Emerging evidence suggests that DNA methylation, a well-studied epigenetic modification, regulates various cellular processes critical for cancer development and progression and holds promise as a biomarker for cancer diagnosis and prognosis, potentially enhancing the efficacy of precision therapies.MethodsWe developed a robust prognostic model for BC based on DNA methylation and clinical data from The Cancer Genome Atlas (TCGA) and Gene Expression Omnibus (GEO). We analyzed the association of the model with clinicopathological features, survival outcomes, and chemotherapy drug sensitivity.ResultsA set of 216 differentially methylated CpGs was identified by intersecting three datasets (TCGA, GSE22249, and GSE66695). Using univariate Cox proportional hazard and LASSO Cox regression analyses, we constructed a 14-CpG model significantly associated with progression-free interval (PFI), disease-specific survival (DSS), and overall survival (OS) in BC patients. Kaplan–Meier (KM) survival analysis, receiver operating characteristic (ROC) analysis, and nomogram validation confirmed the clinical value of the signature. The Cox analysis showed a significant association between the signature and PFI and DSS in BC patients. KM analysis effectively distinguished high-risk from low-risk patients, while ROC analysis demonstrated high sensitivity and specificity in predicting BC prognosis. A nomogram based on the signature effectively predicted 5- and 10-year PFI and DSS. Additionally, combining our model with clinical risk factors suggested that patients in the I–II & M+ subgroup could benefit from adjuvant chemotherapy regarding PFI, DSS, and OS. Gene Ontology (GO) functional enrichment and KEGG pathway analyses indicated that the top 3,000 differentially expressed genes (DEGs) were enriched in pathways related to DNA replication and repair and cell cycle regulation. Patients in the high-risk group might benefit from drugs targeting DNA replication and repair processes in tumor cells.ConclusionThe 14-CpG model serves as a useful biomarker for predicting prognosis in BC patients. When combined with TNM staging, it offers a potential strategy for individualized clinical decision-making, guiding personalized therapeutic regimen selection for clinicians.https://www.frontiersin.org/articles/10.3389/fmed.2025.1548726/fullbreast cancerprognostic modelDNA methylationbiomarkerTCGAGEO
spellingShingle Bao-xing Tian
Zhi-xi Yu
Xia Qiu
Li-ping Chen
Yu-lian Zhuang
Qian Chen
Yan-hua Gu
Meng-jie Hou
Yi-fan Gu
Development and validation of a 14-CpG DNA methylation signature and drug targets for prognostic prediction in breast cancer
Frontiers in Medicine
breast cancer
prognostic model
DNA methylation
biomarker
TCGA
GEO
title Development and validation of a 14-CpG DNA methylation signature and drug targets for prognostic prediction in breast cancer
title_full Development and validation of a 14-CpG DNA methylation signature and drug targets for prognostic prediction in breast cancer
title_fullStr Development and validation of a 14-CpG DNA methylation signature and drug targets for prognostic prediction in breast cancer
title_full_unstemmed Development and validation of a 14-CpG DNA methylation signature and drug targets for prognostic prediction in breast cancer
title_short Development and validation of a 14-CpG DNA methylation signature and drug targets for prognostic prediction in breast cancer
title_sort development and validation of a 14 cpg dna methylation signature and drug targets for prognostic prediction in breast cancer
topic breast cancer
prognostic model
DNA methylation
biomarker
TCGA
GEO
url https://www.frontiersin.org/articles/10.3389/fmed.2025.1548726/full
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