Deciphering the Oncogenic Landscape of Hepatocytes Through Integrated Single‐Nucleus and Bulk RNA‐Seq of Hepatocellular Carcinoma

Abstract Hepatocellular carcinoma (HCC) is a major cause of cancer‐related mortality, while the hepatocyte mechanisms driving oncogenesis remains poorly understood. In this study, single‐nucleus RNA sequencing of samples from 22 HCC patients revealed 10 distinct hepatocyte subtypes, including benefi...

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Main Authors: Huanhou Su, Xuewen Zhou, Guanchuan Lin, Chaochao Luo, Wei Meng, Cui Lv, Yuting Chen, Zebin Wen, Xu Li, Yongzhang Wu, Changtai Xiao, Jian Yang, Jiameng Lu, Xingguang Luo, Yan Chen, Paul KH Tam, Chuanjiang Li, Haitao Sun, Xinghua Pan
Format: Article
Language:English
Published: Wiley 2025-04-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202412944
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author Huanhou Su
Xuewen Zhou
Guanchuan Lin
Chaochao Luo
Wei Meng
Cui Lv
Yuting Chen
Zebin Wen
Xu Li
Yongzhang Wu
Changtai Xiao
Jian Yang
Jiameng Lu
Xingguang Luo
Yan Chen
Paul KH Tam
Chuanjiang Li
Haitao Sun
Xinghua Pan
author_facet Huanhou Su
Xuewen Zhou
Guanchuan Lin
Chaochao Luo
Wei Meng
Cui Lv
Yuting Chen
Zebin Wen
Xu Li
Yongzhang Wu
Changtai Xiao
Jian Yang
Jiameng Lu
Xingguang Luo
Yan Chen
Paul KH Tam
Chuanjiang Li
Haitao Sun
Xinghua Pan
author_sort Huanhou Su
collection DOAJ
description Abstract Hepatocellular carcinoma (HCC) is a major cause of cancer‐related mortality, while the hepatocyte mechanisms driving oncogenesis remains poorly understood. In this study, single‐nucleus RNA sequencing of samples from 22 HCC patients revealed 10 distinct hepatocyte subtypes, including beneficial Hep0, predominantly malignant Hep2, and immunosuppressive Hep9. These subtypes were strongly associated with patient prognosis, confirmed in TCGA‐LIHC and Fudan HCC cohorts through hepatocyte composition deconvolution. A quantile‐based scoring method is developed to integrate data from 29 public HCC datasets, creating a Quantile Distribution Model (QDM) with excellent diagnostic accuracy (Area Under the Curve, AUC = 0.968‐0.982). QDM was employed to screen potential biomarkers, revealing that PDE7B functions as a key gene whose suppression promotes HCC progression. Guided by the genes specific to Hep0/2/9 subtypes, HCC is categorized into metabolic, inflammatory, and matrix classes, which are distinguishable in gene mutation frequencies, survival times, enriched pathways, and immune infiltration. Meanwhile, the sensitive drugs of the three HCC classes are identified, namely ouabain, teniposide, and TG‐101348. This study presents the largest single‐cell hepatocyte dataset to date, offering transformative insights into hepatocarcinogenesis and a comprehensive framework for advancing HCC diagnostics, prognostics, and personalized treatment strategies.
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spelling doaj-art-ab3dd8421be04dfdb9ce77f8722e7dc62025-08-20T02:16:22ZengWileyAdvanced Science2198-38442025-04-011214n/an/a10.1002/advs.202412944Deciphering the Oncogenic Landscape of Hepatocytes Through Integrated Single‐Nucleus and Bulk RNA‐Seq of Hepatocellular CarcinomaHuanhou Su0Xuewen Zhou1Guanchuan Lin2Chaochao Luo3Wei Meng4Cui Lv5Yuting Chen6Zebin Wen7Xu Li8Yongzhang Wu9Changtai Xiao10Jian Yang11Jiameng Lu12Xingguang Luo13Yan Chen14Paul KH Tam15Chuanjiang Li16Haitao Sun17Xinghua Pan18Department of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaDepartment of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaDepartment of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaDepartment of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaDepartment of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaClinical Biobank Center Microbiome Medicine Center Department of Laboratory Medicine Guangdong Provincial Clinical Research Center for Laboratory Medicine Zhujiang Hospital Southern Medical University Guangzhou 510280 ChinaDepartment of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaDepartment of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaDepartment of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaDepartment of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaDepartment of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaDepartment of Hepatobiliary Surgery I General Surgery Center and Guangdong Provincial Clinical and Engineering Center of Digital Medicine Zhujiang Hospital Southern Medical University Guangzhou 510280 ChinaPrecision Regenerative Medicine Research Centre Medical Science Division and State Key Laboratory of Quality Research in Chinese Medicine Macau University of Science and Technology Macao 999078 ChinaDepartment of Psychiatry Yale University School of Medicine New Haven CT 06510 USAPrecision Regenerative Medicine Research Centre Medical Science Division and State Key Laboratory of Quality Research in Chinese Medicine Macau University of Science and Technology Macao 999078 ChinaPrecision Regenerative Medicine Research Centre Medical Science Division and State Key Laboratory of Quality Research in Chinese Medicine Macau University of Science and Technology Macao 999078 ChinaDivision of Hepatobiliopancreatic Surgery Department of General Surgery Nanfang Hospital Southern Medical University Guangzhou Guangdong 510515 ChinaClinical Biobank Center Microbiome Medicine Center Department of Laboratory Medicine Guangdong Provincial Clinical Research Center for Laboratory Medicine Zhujiang Hospital Southern Medical University Guangzhou 510280 ChinaDepartment of Biochemistry and Molecular Biology School of Basic Medical Sciences Southern Medical University and Guangdong Provincial Key Laboratory of Single Cell Technology and Application Guangzhou 510515 ChinaAbstract Hepatocellular carcinoma (HCC) is a major cause of cancer‐related mortality, while the hepatocyte mechanisms driving oncogenesis remains poorly understood. In this study, single‐nucleus RNA sequencing of samples from 22 HCC patients revealed 10 distinct hepatocyte subtypes, including beneficial Hep0, predominantly malignant Hep2, and immunosuppressive Hep9. These subtypes were strongly associated with patient prognosis, confirmed in TCGA‐LIHC and Fudan HCC cohorts through hepatocyte composition deconvolution. A quantile‐based scoring method is developed to integrate data from 29 public HCC datasets, creating a Quantile Distribution Model (QDM) with excellent diagnostic accuracy (Area Under the Curve, AUC = 0.968‐0.982). QDM was employed to screen potential biomarkers, revealing that PDE7B functions as a key gene whose suppression promotes HCC progression. Guided by the genes specific to Hep0/2/9 subtypes, HCC is categorized into metabolic, inflammatory, and matrix classes, which are distinguishable in gene mutation frequencies, survival times, enriched pathways, and immune infiltration. Meanwhile, the sensitive drugs of the three HCC classes are identified, namely ouabain, teniposide, and TG‐101348. This study presents the largest single‐cell hepatocyte dataset to date, offering transformative insights into hepatocarcinogenesis and a comprehensive framework for advancing HCC diagnostics, prognostics, and personalized treatment strategies.https://doi.org/10.1002/advs.202412944hepatocellular carcinoma classificationhepatocyte subtypemetabolic pathwayquantile distribution modelsingle‐cell transcriptomics
spellingShingle Huanhou Su
Xuewen Zhou
Guanchuan Lin
Chaochao Luo
Wei Meng
Cui Lv
Yuting Chen
Zebin Wen
Xu Li
Yongzhang Wu
Changtai Xiao
Jian Yang
Jiameng Lu
Xingguang Luo
Yan Chen
Paul KH Tam
Chuanjiang Li
Haitao Sun
Xinghua Pan
Deciphering the Oncogenic Landscape of Hepatocytes Through Integrated Single‐Nucleus and Bulk RNA‐Seq of Hepatocellular Carcinoma
Advanced Science
hepatocellular carcinoma classification
hepatocyte subtype
metabolic pathway
quantile distribution model
single‐cell transcriptomics
title Deciphering the Oncogenic Landscape of Hepatocytes Through Integrated Single‐Nucleus and Bulk RNA‐Seq of Hepatocellular Carcinoma
title_full Deciphering the Oncogenic Landscape of Hepatocytes Through Integrated Single‐Nucleus and Bulk RNA‐Seq of Hepatocellular Carcinoma
title_fullStr Deciphering the Oncogenic Landscape of Hepatocytes Through Integrated Single‐Nucleus and Bulk RNA‐Seq of Hepatocellular Carcinoma
title_full_unstemmed Deciphering the Oncogenic Landscape of Hepatocytes Through Integrated Single‐Nucleus and Bulk RNA‐Seq of Hepatocellular Carcinoma
title_short Deciphering the Oncogenic Landscape of Hepatocytes Through Integrated Single‐Nucleus and Bulk RNA‐Seq of Hepatocellular Carcinoma
title_sort deciphering the oncogenic landscape of hepatocytes through integrated single nucleus and bulk rna seq of hepatocellular carcinoma
topic hepatocellular carcinoma classification
hepatocyte subtype
metabolic pathway
quantile distribution model
single‐cell transcriptomics
url https://doi.org/10.1002/advs.202412944
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