PLXDC1+ Tumor‐Associated Pancreatic Stellate Cells Promote Desmoplastic and Immunosuppressive Niche in Pancreatic Ductal Adenocarcinoma

Abstract Pancreatic stellate cells (PSCs) contribute to pancreatic ductal adenocarcinoma (PDAC) progression and therapeutic resistance, yet their detailed functions remain unclear. This study combined RNA sequencing and assay for transposase‐accessible chromatin using sequencing (ATAC‐seq) on sorted...

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Main Authors: Yanhua Du, Yizhou Zhao, Judong Li, Jiaxin Wang, Shenglan You, Yao Zhang, Li Zhang, Jihong Yang, Hamid Alinejad‐Rokny, Shujie Cheng, Chenghao Shao, Duowu Zou, Youqiong Ye
Format: Article
Language:English
Published: Wiley 2025-05-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202415756
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author Yanhua Du
Yizhou Zhao
Judong Li
Jiaxin Wang
Shenglan You
Yao Zhang
Li Zhang
Jihong Yang
Hamid Alinejad‐Rokny
Shujie Cheng
Chenghao Shao
Duowu Zou
Youqiong Ye
author_facet Yanhua Du
Yizhou Zhao
Judong Li
Jiaxin Wang
Shenglan You
Yao Zhang
Li Zhang
Jihong Yang
Hamid Alinejad‐Rokny
Shujie Cheng
Chenghao Shao
Duowu Zou
Youqiong Ye
author_sort Yanhua Du
collection DOAJ
description Abstract Pancreatic stellate cells (PSCs) contribute to pancreatic ductal adenocarcinoma (PDAC) progression and therapeutic resistance, yet their detailed functions remain unclear. This study combined RNA sequencing and assay for transposase‐accessible chromatin using sequencing (ATAC‐seq) on sorted PSCs from adjacent normal and PDAC tissues to investigate their transcriptional and epigenetic activation. PSCs heterogeneity and functions are characterized through bulk, single‐cell, and spatial transcriptomes, as well as in situ sequencing. The clinical relevance of PSCs in immunotherapy is assessed using an in‐house immune‐checkpoint blockade (ICB) treatment cohort. Findings showed that stress and hypoxia signaling activated PSCs in PDAC. Three common PSCs (CPSCs) and four tumor‐associated PSCs (TPSCs) are identified, each with distinct functions. CPSCs differentiated into CCL19+ TPSCs in immune‐enriched regions, MYH11+ TPSCs in the stromal region, and PLXDC1+ TPSCs, which exhibited cancer‐associated myofibroblasts (myCAFs) phenotype linked to poor prognosis. Notably, PLXDC1+ TPSCs, located near aggressive LRRC15+ myCAFs and SPP1+ macrophages, formed a desmoplastic and immunosuppressive niche around the tumor boundary, promoting CD8 T cell exhaustion. Single‐cell transcriptomics of PDAC patients treated with ICB revealed that PLXDC1+ TPSCs correlated with poor immunotherapy efficacy. Overall, this study provides key insights into PSCs in PDAC and potential therapeutic targets.
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spelling doaj-art-31b82fa7577e4025984e16ed6cc3960e2025-08-20T03:11:14ZengWileyAdvanced Science2198-38442025-05-011218n/an/a10.1002/advs.202415756PLXDC1+ Tumor‐Associated Pancreatic Stellate Cells Promote Desmoplastic and Immunosuppressive Niche in Pancreatic Ductal AdenocarcinomaYanhua Du0Yizhou Zhao1Judong Li2Jiaxin Wang3Shenglan You4Yao Zhang5Li Zhang6Jihong Yang7Hamid Alinejad‐Rokny8Shujie Cheng9Chenghao Shao10Duowu Zou11Youqiong Ye12Center for Immune‐Related Diseases at Shanghai Institute of Immunology Department of Gastroenterology Ruijin Hospital Shanghai Jiao Tong University School of Medicine Shanghai 200001 ChinaCenter for Immune‐Related Diseases at Shanghai Institute of Immunology Department of Gastroenterology Ruijin Hospital Shanghai Jiao Tong University School of Medicine Shanghai 200001 ChinaDepartment of Pancreatic‐biliary Surgery Changzheng Hospital Naval Medical University Shanghai 200003 ChinaCenter for Immune‐Related Diseases at Shanghai Institute of Immunology Department of Gastroenterology Ruijin Hospital Shanghai Jiao Tong University School of Medicine Shanghai 200001 ChinaCenter for Immune‐Related Diseases at Shanghai Institute of Immunology Department of Gastroenterology Ruijin Hospital Shanghai Jiao Tong University School of Medicine Shanghai 200001 ChinaCenter for Immune‐Related Diseases at Shanghai Institute of Immunology Department of Gastroenterology Ruijin Hospital Shanghai Jiao Tong University School of Medicine Shanghai 200001 ChinaCenter for Immune‐Related Diseases at Shanghai Institute of Immunology Department of Gastroenterology Ruijin Hospital Shanghai Jiao Tong University School of Medicine Shanghai 200001 ChinaDepartment of Hepatobiliary Surgery Hebei Key Laboratory of General Surgery for Digital Medicine Affiliated Hospital of Hebei University Baoding 071000 ChinaUNSW BioMedical Machine Learning Lab (BML) School of Biomedical Engineering UNSW Sydney Sydney NSW 2052 AustraliaDepartment of Hepatobiliary Surgery Hebei Key Laboratory of General Surgery for Digital Medicine Affiliated Hospital of Hebei University Baoding 071000 ChinaDepartment of Pancreatic‐biliary Surgery Changzheng Hospital Naval Medical University Shanghai 200003 ChinaCenter for Immune‐Related Diseases at Shanghai Institute of Immunology Department of Gastroenterology Ruijin Hospital Shanghai Jiao Tong University School of Medicine Shanghai 200001 ChinaCenter for Immune‐Related Diseases at Shanghai Institute of Immunology Department of Gastroenterology Ruijin Hospital Shanghai Jiao Tong University School of Medicine Shanghai 200001 ChinaAbstract Pancreatic stellate cells (PSCs) contribute to pancreatic ductal adenocarcinoma (PDAC) progression and therapeutic resistance, yet their detailed functions remain unclear. This study combined RNA sequencing and assay for transposase‐accessible chromatin using sequencing (ATAC‐seq) on sorted PSCs from adjacent normal and PDAC tissues to investigate their transcriptional and epigenetic activation. PSCs heterogeneity and functions are characterized through bulk, single‐cell, and spatial transcriptomes, as well as in situ sequencing. The clinical relevance of PSCs in immunotherapy is assessed using an in‐house immune‐checkpoint blockade (ICB) treatment cohort. Findings showed that stress and hypoxia signaling activated PSCs in PDAC. Three common PSCs (CPSCs) and four tumor‐associated PSCs (TPSCs) are identified, each with distinct functions. CPSCs differentiated into CCL19+ TPSCs in immune‐enriched regions, MYH11+ TPSCs in the stromal region, and PLXDC1+ TPSCs, which exhibited cancer‐associated myofibroblasts (myCAFs) phenotype linked to poor prognosis. Notably, PLXDC1+ TPSCs, located near aggressive LRRC15+ myCAFs and SPP1+ macrophages, formed a desmoplastic and immunosuppressive niche around the tumor boundary, promoting CD8 T cell exhaustion. Single‐cell transcriptomics of PDAC patients treated with ICB revealed that PLXDC1+ TPSCs correlated with poor immunotherapy efficacy. Overall, this study provides key insights into PSCs in PDAC and potential therapeutic targets.https://doi.org/10.1002/advs.202415756activation, heterogeneityimmunotherapy resistancepancreatic stellate cells (PSCs); PLXDC1+ tumor‐associated PSCssingle‐cell and spatial transcriptomes
spellingShingle Yanhua Du
Yizhou Zhao
Judong Li
Jiaxin Wang
Shenglan You
Yao Zhang
Li Zhang
Jihong Yang
Hamid Alinejad‐Rokny
Shujie Cheng
Chenghao Shao
Duowu Zou
Youqiong Ye
PLXDC1+ Tumor‐Associated Pancreatic Stellate Cells Promote Desmoplastic and Immunosuppressive Niche in Pancreatic Ductal Adenocarcinoma
Advanced Science
activation, heterogeneity
immunotherapy resistance
pancreatic stellate cells (PSCs); PLXDC1+ tumor‐associated PSCs
single‐cell and spatial transcriptomes
title PLXDC1+ Tumor‐Associated Pancreatic Stellate Cells Promote Desmoplastic and Immunosuppressive Niche in Pancreatic Ductal Adenocarcinoma
title_full PLXDC1+ Tumor‐Associated Pancreatic Stellate Cells Promote Desmoplastic and Immunosuppressive Niche in Pancreatic Ductal Adenocarcinoma
title_fullStr PLXDC1+ Tumor‐Associated Pancreatic Stellate Cells Promote Desmoplastic and Immunosuppressive Niche in Pancreatic Ductal Adenocarcinoma
title_full_unstemmed PLXDC1+ Tumor‐Associated Pancreatic Stellate Cells Promote Desmoplastic and Immunosuppressive Niche in Pancreatic Ductal Adenocarcinoma
title_short PLXDC1+ Tumor‐Associated Pancreatic Stellate Cells Promote Desmoplastic and Immunosuppressive Niche in Pancreatic Ductal Adenocarcinoma
title_sort plxdc1 tumor associated pancreatic stellate cells promote desmoplastic and immunosuppressive niche in pancreatic ductal adenocarcinoma
topic activation, heterogeneity
immunotherapy resistance
pancreatic stellate cells (PSCs); PLXDC1+ tumor‐associated PSCs
single‐cell and spatial transcriptomes
url https://doi.org/10.1002/advs.202415756
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