Revealing a novel Decorin-expressing tumor stromal subset in hepatocellular carcinoma via integrative analysis single-cell RNA sequencing

Abstract Hepatocellular carcinoma (HCC) remains a leading cause of cancer-related mortality, emphasizing the need for novel therapeutic strategies. Decorin (DCN), a chondroitin sulfate proteoglycan (CSPG), has been proposed as a tumor suppressor, yet its precise role in HCC and the tumor microenviro...

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Main Authors: Chi Hsiao, Wen-Chieh Liao, Ju-Pi Li, Yu-Cheng Chou, Yu-Lun Chou, Jeng-Rong Lin, Chia-Hua Chen, Chiung-Hui Liu
Format: Article
Language:English
Published: BMC 2025-05-01
Series:Cancer Cell International
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Online Access:https://doi.org/10.1186/s12935-025-03811-0
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author Chi Hsiao
Wen-Chieh Liao
Ju-Pi Li
Yu-Cheng Chou
Yu-Lun Chou
Jeng-Rong Lin
Chia-Hua Chen
Chiung-Hui Liu
author_facet Chi Hsiao
Wen-Chieh Liao
Ju-Pi Li
Yu-Cheng Chou
Yu-Lun Chou
Jeng-Rong Lin
Chia-Hua Chen
Chiung-Hui Liu
author_sort Chi Hsiao
collection DOAJ
description Abstract Hepatocellular carcinoma (HCC) remains a leading cause of cancer-related mortality, emphasizing the need for novel therapeutic strategies. Decorin (DCN), a chondroitin sulfate proteoglycan (CSPG), has been proposed as a tumor suppressor, yet its precise role in HCC and the tumor microenvironment (TME) remains underexplored. Through integrated analyses of bulk RNA and single-cell RNA sequencing datasets, we identified a distinct tumor stromal subset highly expressing DCN and associated chondroitin sulfate (CS) synthases. Our findings revealed that DCN expression is significantly downregulated in HCC tissue, but upregulated in peri-tumor stroma, where it correlates with better prognosis and reduced capsular invasion. Western blot analysis demonstrated that CS-DCN, the glycosylated form of DCN, plays a dominant role in this context. Single-cell clustering analysis identified a unique stromal subset in HCC characterized by elevated expression of DCN, CSPGs, and CS synthases, associated with extracellular matrix (ECM) remodeling and protective barrier functions. A six-gene DCN-associated signature derived from this subset, including DCN, BGN, SRPX, CHSY3, CHST3, and CHPF, was validated as a prognostic marker for HCC. Furthermore, functional assays demonstrated that CS-DCN significantly inhibited HCC cell proliferation and invasion. Our study highlights the critical role of DCN in HCC TME and provides insights into its therapeutic potential. Modulating CSPG pathways, particularly on CS-DCN-expressing stromal cells, may offer a promising approach for improving HCC treatment and patient outcomes.
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series Cancer Cell International
spelling doaj-art-ac1f21e4e3b34803885f02a353b56c512025-08-20T03:22:13ZengBMCCancer Cell International1475-28672025-05-0125111410.1186/s12935-025-03811-0Revealing a novel Decorin-expressing tumor stromal subset in hepatocellular carcinoma via integrative analysis single-cell RNA sequencingChi Hsiao0Wen-Chieh Liao1Ju-Pi Li2Yu-Cheng Chou3Yu-Lun Chou4Jeng-Rong Lin5Chia-Hua Chen6Chiung-Hui Liu7Doctoral Program in Tissue Engineering and Regenerative Medicine, College of Medicine, National Chung Hsing UniversityDoctoral Program in Tissue Engineering and Regenerative Medicine, College of Medicine, National Chung Hsing UniversityDepartment of Pathology, School of Medicine, Chung Shan Medical UniversityDepartment of Post-Baccalaureate Medicine, College of Medicine, National Chung Hsing UniversityDoctoral Program in Tissue Engineering and Regenerative Medicine, College of Medicine, National Chung Hsing UniversityDoctoral Program in Tissue Engineering and Regenerative Medicine, College of Medicine, National Chung Hsing UniversityDepartment of Anatomy, School of Medicine, Chang Gung UniversityDoctoral Program in Tissue Engineering and Regenerative Medicine, College of Medicine, National Chung Hsing UniversityAbstract Hepatocellular carcinoma (HCC) remains a leading cause of cancer-related mortality, emphasizing the need for novel therapeutic strategies. Decorin (DCN), a chondroitin sulfate proteoglycan (CSPG), has been proposed as a tumor suppressor, yet its precise role in HCC and the tumor microenvironment (TME) remains underexplored. Through integrated analyses of bulk RNA and single-cell RNA sequencing datasets, we identified a distinct tumor stromal subset highly expressing DCN and associated chondroitin sulfate (CS) synthases. Our findings revealed that DCN expression is significantly downregulated in HCC tissue, but upregulated in peri-tumor stroma, where it correlates with better prognosis and reduced capsular invasion. Western blot analysis demonstrated that CS-DCN, the glycosylated form of DCN, plays a dominant role in this context. Single-cell clustering analysis identified a unique stromal subset in HCC characterized by elevated expression of DCN, CSPGs, and CS synthases, associated with extracellular matrix (ECM) remodeling and protective barrier functions. A six-gene DCN-associated signature derived from this subset, including DCN, BGN, SRPX, CHSY3, CHST3, and CHPF, was validated as a prognostic marker for HCC. Furthermore, functional assays demonstrated that CS-DCN significantly inhibited HCC cell proliferation and invasion. Our study highlights the critical role of DCN in HCC TME and provides insights into its therapeutic potential. Modulating CSPG pathways, particularly on CS-DCN-expressing stromal cells, may offer a promising approach for improving HCC treatment and patient outcomes.https://doi.org/10.1186/s12935-025-03811-0Hepatocellular carcinomaTumor microenvironmentChondroitin polymerizing factorChondroitin sulfateDecorin
spellingShingle Chi Hsiao
Wen-Chieh Liao
Ju-Pi Li
Yu-Cheng Chou
Yu-Lun Chou
Jeng-Rong Lin
Chia-Hua Chen
Chiung-Hui Liu
Revealing a novel Decorin-expressing tumor stromal subset in hepatocellular carcinoma via integrative analysis single-cell RNA sequencing
Cancer Cell International
Hepatocellular carcinoma
Tumor microenvironment
Chondroitin polymerizing factor
Chondroitin sulfate
Decorin
title Revealing a novel Decorin-expressing tumor stromal subset in hepatocellular carcinoma via integrative analysis single-cell RNA sequencing
title_full Revealing a novel Decorin-expressing tumor stromal subset in hepatocellular carcinoma via integrative analysis single-cell RNA sequencing
title_fullStr Revealing a novel Decorin-expressing tumor stromal subset in hepatocellular carcinoma via integrative analysis single-cell RNA sequencing
title_full_unstemmed Revealing a novel Decorin-expressing tumor stromal subset in hepatocellular carcinoma via integrative analysis single-cell RNA sequencing
title_short Revealing a novel Decorin-expressing tumor stromal subset in hepatocellular carcinoma via integrative analysis single-cell RNA sequencing
title_sort revealing a novel decorin expressing tumor stromal subset in hepatocellular carcinoma via integrative analysis single cell rna sequencing
topic Hepatocellular carcinoma
Tumor microenvironment
Chondroitin polymerizing factor
Chondroitin sulfate
Decorin
url https://doi.org/10.1186/s12935-025-03811-0
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