The role of epigenetic regulation in pancreatic ductal adenocarcinoma progression and drug response: an integrative genomic and pharmacological prognostic prediction model

BackgroundPancreatic ductal adenocarcinoma (PDAC) is a highly lethal malignancy with poor prognosis. Epigenetic dysregulation plays a crucial role in PDAC progression, but its comprehensive landscape and clinical implications remain unclear.MethodsWe integrated single-cell RNA sequencing, bulk RNA s...

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Main Authors: Kang Fu, Junzhe Su, Yiming Zhou, Xiaotong Chen, Xiao Hu
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Pharmacology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphar.2024.1498031/full
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author Kang Fu
Junzhe Su
Yiming Zhou
Xiaotong Chen
Xiao Hu
author_facet Kang Fu
Junzhe Su
Yiming Zhou
Xiaotong Chen
Xiao Hu
author_sort Kang Fu
collection DOAJ
description BackgroundPancreatic ductal adenocarcinoma (PDAC) is a highly lethal malignancy with poor prognosis. Epigenetic dysregulation plays a crucial role in PDAC progression, but its comprehensive landscape and clinical implications remain unclear.MethodsWe integrated single-cell RNA sequencing, bulk RNA sequencing, and clinical data from multiple public databases. Single-cell analysis was performed using Seurat and hdWGCNA packages to reveal cell heterogeneity and epigenetic features. Weighted gene co-expression network analysis (WGCNA) identified key epigenetic modules. A machine learning-based prognostic model was constructed using multiple algorithms, including Lasso and Random Survival Forest. We further analyzed mutations, immune microenvironment, and drug sensitivity associated with the epigenetic risk score.ResultsSingle-cell analysis revealed distinct epigenetic patterns across different cell types in PDAC. WGCNA identified key modules associated with histone modifications and DNA methylation. Our machine learning model, based on 17 epigenetic genes, showed robust prognostic value (AUC >0.7 for 1-, 3-, and 5-year survival) and outperformed existing models. High-risk patients exhibited distinct mutation patterns, including higher frequencies of KRAS and TP53 mutations. Low-risk patients showed higher immune and stromal scores, with increased infiltration of CD8+ T cells and M2 macrophages. Drug sensitivity analysis revealed differential responses to various therapeutic agents between high- and low-risk groups, with low-risk patients showing higher sensitivity to EGFR and MEK inhibitors.ConclusionOur study provides a comprehensive landscape of epigenetic regulation in PDAC at single-cell resolution and establishes a robust epigenetics-based prognostic model. The integration of epigenetic features with mutation profiles, immune microenvironment, and drug sensitivity offers new insights into PDAC heterogeneity and potential therapeutic strategies. These findings pave the way for personalized medicine in PDAC management and highlight the importance of epigenetic regulation in cancer research.
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spelling doaj-art-8d5f886d48e447fcab5c5ebb3c441c212025-08-20T02:13:01ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122024-11-011510.3389/fphar.2024.14980311498031The role of epigenetic regulation in pancreatic ductal adenocarcinoma progression and drug response: an integrative genomic and pharmacological prognostic prediction modelKang FuJunzhe SuYiming ZhouXiaotong ChenXiao HuBackgroundPancreatic ductal adenocarcinoma (PDAC) is a highly lethal malignancy with poor prognosis. Epigenetic dysregulation plays a crucial role in PDAC progression, but its comprehensive landscape and clinical implications remain unclear.MethodsWe integrated single-cell RNA sequencing, bulk RNA sequencing, and clinical data from multiple public databases. Single-cell analysis was performed using Seurat and hdWGCNA packages to reveal cell heterogeneity and epigenetic features. Weighted gene co-expression network analysis (WGCNA) identified key epigenetic modules. A machine learning-based prognostic model was constructed using multiple algorithms, including Lasso and Random Survival Forest. We further analyzed mutations, immune microenvironment, and drug sensitivity associated with the epigenetic risk score.ResultsSingle-cell analysis revealed distinct epigenetic patterns across different cell types in PDAC. WGCNA identified key modules associated with histone modifications and DNA methylation. Our machine learning model, based on 17 epigenetic genes, showed robust prognostic value (AUC >0.7 for 1-, 3-, and 5-year survival) and outperformed existing models. High-risk patients exhibited distinct mutation patterns, including higher frequencies of KRAS and TP53 mutations. Low-risk patients showed higher immune and stromal scores, with increased infiltration of CD8+ T cells and M2 macrophages. Drug sensitivity analysis revealed differential responses to various therapeutic agents between high- and low-risk groups, with low-risk patients showing higher sensitivity to EGFR and MEK inhibitors.ConclusionOur study provides a comprehensive landscape of epigenetic regulation in PDAC at single-cell resolution and establishes a robust epigenetics-based prognostic model. The integration of epigenetic features with mutation profiles, immune microenvironment, and drug sensitivity offers new insights into PDAC heterogeneity and potential therapeutic strategies. These findings pave the way for personalized medicine in PDAC management and highlight the importance of epigenetic regulation in cancer research.https://www.frontiersin.org/articles/10.3389/fphar.2024.1498031/fullpancreatic ductal adenocarcinomaepigenetic regulationsingle-cell RNA sequencingmachine learningprognostic modeltumor microenvironment
spellingShingle Kang Fu
Junzhe Su
Yiming Zhou
Xiaotong Chen
Xiao Hu
The role of epigenetic regulation in pancreatic ductal adenocarcinoma progression and drug response: an integrative genomic and pharmacological prognostic prediction model
Frontiers in Pharmacology
pancreatic ductal adenocarcinoma
epigenetic regulation
single-cell RNA sequencing
machine learning
prognostic model
tumor microenvironment
title The role of epigenetic regulation in pancreatic ductal adenocarcinoma progression and drug response: an integrative genomic and pharmacological prognostic prediction model
title_full The role of epigenetic regulation in pancreatic ductal adenocarcinoma progression and drug response: an integrative genomic and pharmacological prognostic prediction model
title_fullStr The role of epigenetic regulation in pancreatic ductal adenocarcinoma progression and drug response: an integrative genomic and pharmacological prognostic prediction model
title_full_unstemmed The role of epigenetic regulation in pancreatic ductal adenocarcinoma progression and drug response: an integrative genomic and pharmacological prognostic prediction model
title_short The role of epigenetic regulation in pancreatic ductal adenocarcinoma progression and drug response: an integrative genomic and pharmacological prognostic prediction model
title_sort role of epigenetic regulation in pancreatic ductal adenocarcinoma progression and drug response an integrative genomic and pharmacological prognostic prediction model
topic pancreatic ductal adenocarcinoma
epigenetic regulation
single-cell RNA sequencing
machine learning
prognostic model
tumor microenvironment
url https://www.frontiersin.org/articles/10.3389/fphar.2024.1498031/full
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