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SNORA23 inhibits HCC tumorigenesis by impairing the 2'-O-ribose methylation level of 28S rRNA

Cancer Biology & Medicine 2022年第1期19卷 104-119页

作者： Zhiyong Liu Yanan Pang Yin Jia Qin Qin Rui Wang Wei Li Jie Jing Haidong Liu Shanrong Liu Department of Laboratory Diagnostics Changhai HospitalSecond Military Medical UniversityShanghai 200433China Department of Gastroenterology and Hepatology Zhongshan HospitalFudan UniversityShanghai 200032China Department of Gastroenterology Changhai HospitalSecond Military Medical UniversityShanghai 200433China Shanghai Institute of Pancreatic Diseases Shanghai 200433China Department of Chemistry and State Key Laboratory of Molecular Engineering of Polymers Fudan UniversityShanghai 200433 China Department of General Surgery Changzheng HospitalSecond Military Medical UniversityShanghai 200433China Shanghai Fourth People’s Hospital Tongji University School of MedicineShanghai 200081China

Objective:The dysregulation of ribosome biogenesis is associated with the progression of numerous tumors,including hepatocellular carcinoma(HCC).Small nucleolar RNAs(sno RNAs)regulate ribosome biogenesis by guiding the modification of ribosomal RNAs(r RNAs).However,the underlying mechanism of this process in HCC remains elusive.Methods:RNA immunoprecipitation and sequencing were used to analyze RNAs targeted by ribosome proteins.The biological functions of SNORA23 were examined in HCC cells and a xenograft mouse model.To elucidate the underlying mechanisms,the 2′-O-ribose methylation level of r RNAs was evaluated by q PCR,and the key proteins in the PI3 K/Akt/m TOR pathway were detected using Western blot.Results:Twelve sno RNAs were found to co-exist in 4 cancer cell lines using RPS6 pull-down assays.SNORA23 was downregulated in HCC and correlated with the poor prognoses of HCC patients.SNORA23 inhibited the proliferation,migration,and invasion of HCC cells both in vitro and in vivo.We also found that SNORA23 regulated ribosome biogenesis by impairing 2′-O-ribose methylation of cytidine4506 of 28 S r RNA.Furthermore,SNORA23,which is regulated by the PI3 K/Akt/m TOR signaling pathway,significantly inhibited the phosphorylation of 4 E binding protein 1.SNORA23 and rapamycin blocked the PI3 K/AKT/m TOR signaling pathway and impaired HCC growth in vivo.Conclusions:SNORA23 exhibited antitumor effects in HCC and together with rapamycin,provided a promising therapeutic strategy for HCC treatment.

关键词： SNORA23 ribosome biogenesis rRNA methylation HCC

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CUL4B facilitates HBV replication by promoting HBx stabilization

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Cancer Biology & Medicine 2022年第1期19卷 120-131页

作者： Haixia Shan Bo Wang Xiaodong Zhang Hui Song Xi Li Yongxin Zou Baichun Jiang Huili Hu Hao Dou Changshun Shao Lifen Gao Chunhong Ma Xiaoyun Yang Xiaohong Liang Yaoqin Gong Key Laboratory for Experimental Teratology of the Ministry of Education Key Laboratory of Infection and Immunity of Shandong Province and Department of ImmunologySchool of Basic Medical SciencesShandong UniversityJinan 250012China Department of Laboratory Diagnosis Cangzhou Combination of Traditional Chinese and Western Medicine Hospital of Hebei ProvinceCangzhou 061000China Division of Gastroenterology and Hepatology Renji HospitalSchool of MedicineShanghai Jiao Tong UniversityShanghai Institute of Digestive DiseaseShanghai 200120China Ministry of Education Key Laboratory of Experimental Teratology and Institute of Molecular Medicine and Genetics School of Basic Medical SciencesShandong UniversityJinan 250012China Collaborative Innovation Center of Technology and Equipment for Biological Diagnosis and Therapy in Universities of Shandong Jinan 250012China Department of Gastroenterology Qilu HospitalShandong UniversityJinan 250012China

Objective:Hepatitis B virus(HBV)infection is a major public health problem worldwide.However,the regulatory mechanisms underlying HBV replication remain unclear.Cullin 4 B-RING ubiquitin E3 ligase(CRL4 B)is involved in regulating diverse physiological and pathophysiological processes.In our study,we aimed to explain the role of CUL4 B in HBV infection.Methods:Cul4 b transgenic mice or conditional knockout mice,as well as liver cell lines with CUL4 B overexpression or knockdown,were used to assess the role of CUL4 B in HBV replication.Immunoprecipitation assays and immunofluorescence staining were performed to study the interaction between CUL4 B and HBx.Cycloheximide chase assays and in vivo ubiquitination assays were performed to evaluate the half-life and the ubiquitination status of HBx.Results:The hydrodynamics-based hepatitis B model in Cul4 b transgenic or conditional knockout mice indicated that CUL4 B promoted HBV replication(P<0.05).Moreover,the overexpression or knockdown system in human liver cell lines validated that CUL4 B increased HBV replication in an HBx-dependent manner.Importantly,immunoprecipitation assays and immunofluorescence staining showed an interaction between CUL4 B and HBx.Furthermore,CUL4 B upregulated HBx protein levels by inhibiting HBx ubiquitination and proteasomal degradation(P<0.05).Finally,a positive correlation between CUL4 B expression and HBV pg RNA level was observed in liver tissues from HBV-positive patients and HBV transgenic mice.Conclusions:CUL4 B enhances HBV replication by interacting with HBx and disrupting its ubiquitin-dependent proteasomal degradation.CUL4 B may therefore be a potential target for anti-HBV therapy.

关键词： CUL4B HBV ubiquitination HBx HCC

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Application and progress of the detection technologies in hepatocellular carcinoma

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Genes & Diseases 2023年第5期10卷 1857-1869页

作者： Qi Yan Yuan-song Sun Ran An Fang Liu Qi Fang Zhen Wang Tao Xu Lijian Chen Jian Du School of Basic Medical Sciences Anhui Medical UniversityHefeiAnhui 230032China Department of Emergency Surgery The Second Hospital of Anhui Medical UniversityHefeiAnhui 230032China Department of Anesthesiology The First Affiliated Hospital of Anhui Medical UniversityHefeiAnhui 230032China Inflammation and Immune Mediated Diseases Laboratory of Anhui Province Anhui Institute of Innovative DrugsSchool of PharmacyHefeiAnhui 230032China Institute for Liver Diseases of Anhui Medical University Anhui Medical UniversityHefeiAnhui 230032China

Hepatocellular carcinoma(HCC)has a very high incidence and fatality rate,and in most cases,it is already at an advanced stage when diagnosed.Therefore,early prevention and detection of HCC are two of the most effective strategies.However,the methods recommended in the practice guidelines for the detection of HCC cannot guarantee high sensitivity and specificity except for the liver biopsy,which is known as the“gold standard”.In this review,we divided the detection of HCC into pre-treatment diagnosis and post-treatment monitoring,and found that in addition to the traditional imaging detection and liver biopsy,alpha fetoprotein(AFP),lens culinaris-agglutinin-reactive fraction of AFP(AFP-L3),protein induced by vitamin K absence or antagonist-II(PIVKA-II)and other biomarkers are excellent biomarkers for HCC,especially when they are combined together.Most notably,the emerging liquid biopsy shows great promise in detecting HCC.In addition,lactic dehydrogenase(LDH),suppressor of cytokine signaling(SOCS)and other relevant biomarkers may become promising biomarkers for HCC post-treatment monitoring.Through the detailed introduction of the diagnostic technology of HCC,we can have a detailed understanding of its development process and then obtain some enlightenment from the diagnosis,to improve the diagnostic rate of HCC and reduce its mortality.

关键词： HCC Invasive diagnosis Minimally invasive diagnosis Noninvasive diagnosis Prognostic monitoring

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The Wnt/β-catenin signaling pathway in the tumor microenvironment of hepatocellular carcinoma

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Cancer Biology & Medicine 2022年第3期19卷 305-318页

作者： Kaiting Wang Xinyao Qiu Yan Zhao Hongyang Wang Lei Chen School of Life Sciences Fudan UniversityShanghai 200438China Fudan University Shanghai Cancer Center Department of OncologyShanghai Medical CollegeFudan UniversityShanghai 200032China Institute of Metabolism&Integrative Biology(IMIB) Fudan UniversityShanghai 200438China The International Cooperation Laboratory on Signal Transduction Eastern Hepatobiliary Surgery HospitalSecond Military Medical UniversityShanghai 200438China

The Wnt/β-catenin signaling pathway regulates many aspects of tumor biology,and many studies have focused on the role of this signaling pathway in tumor cells.However,it is now clear that tumor development and metastasis depend on the two-way interaction between cancer cells and their environment,thereby forming a tumor microenvironment(TME).In this review,we discuss how Wnt/β-catenin signaling regulates cross-interactions among different components of the TME,including immune cells,stem cells,tumor vasculature,and noncellular components of the TME in hepatocellular carcinoma.We also investigate their preclinical and clinical insights for primary liver cancer intervention,and explore the significance of using Wnt/β-catenin mutations as a biomarker to predict resistance in immunotherapy.

关键词： Wnt/β-catenin signaling HCC tumor microenvironment immunotherapy

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Bone metastasis of hepatocellular carcinoma:facts and hopes from clinical and translational perspectives

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Frontiers of Medicine 2022年第4期16卷 551-573页

作者： Zhao Huang Jingyuan Wen Yufei Wang Shenqi Han Zhen Li Xuemei Hu Dongling Zhu Zhenxiong Wang Junnan Liang Huifang Liang Xiao-ping Chen Bixiang Zhang Hepatic Surgery Center Tongji HospitalTongji Medical CollegeHuazhong University of Science and TechnologyWuhan 430030China Clinical Medical Research Center of Hepatic Surgery at Hubei Province Wuhan 430030China Hubei Key Laboratory of Hepato-Pancreatic-Biliary Diseases Tongji HospitalTongji Medical CollegeHuazhong University of Science and TechnologyWuhan 430030China Department of Radiology Tongji HospitalTongji Medical CollegeHuazhong University of Science and TechnologyWuhan 430030China Department of Nuclear Medicine and PET Tongji HospitalTongji Medical CollegeHuazhong University of Science and TechnologyWuhan 430030China Department of Radiology Guangzhou First People’s HospitalSchool of MedicineSouth China University of TechnologyGuangzhou 510180China Key Laboratory of Organ Transplantation Ministry of Education Key Laboratory of Organ TransplantationNational Health CommissionKey Laboratory of Organ TransplantationChinese Academy of Medical SciencesWuhan 430030China

Patients with hepatocellular carcinoma(HCC)and bone metastasis(BM)suffer from greatly reduced life quality and a dismal prognosis.However,BM in HCC has long been overlooked possibly due to its relatively low prevalence in previous decades.To date,no consensus or guidelines have been reached or formulated for the prevention and management of HCC BM.Our narrative review manifests the increasing incidence of HCC BM to sound the alarm for additional attention.The risk factors,diagnosis,prognosis,and therapeutic approaches of HCC BM are detailed to provide a panoramic view of this disease to clinicians and specialists.We further delineate an informative cancer bone metastatic cascade based on evidence from recent studies and point out the main factors responsible for the tumor-associated disruption of bone homeostasis and the formation of skeletal cancer lesions.We also present the advances in the pathological and molecular mechanisms of HCC BM to shed light on translational opportunities.Dilemmas and challenges in the treatment and investigation of HCC BM are outlined and discussed to encourage further endeavors in the exploration of underlying pathogenic and molecular mechanisms,as well as the development of novel effective therapies for HCC patients with BM.

关键词： HCC bone osteotropism clinical basic researches advances

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Hepatic SIRT6 deficit promotes liver tumorigenesis in the mice models

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Genes & Diseases 2022年第3期9卷 789-796页

作者： Mei Wang Linhua Lan Fan Yang Shan Jiang Haojun Xu Chengfei Zhang Guoren Zhou Hongping Xia Jinglin Xia Department of Pathology in the School of Basic Medical Sciences&Sir Run Run Hospital&State Key Laboratory of Reproductive Medicine&Key Laboratory of Antibody Technique of National Health Commission Nanjing Medical UniversityNanjingJiangsu 211166PR China Department of Immunology Medical School of Southeast UniversityNanjingJiangsu 210009PR China The First Affiliated Hospital of Wenzhou Medical University WenzhouZhejiang 325000PR China The First Affiliated Hospital of Chongqing Medical University Chongqing 400016PR China Jiangsu Cancer Hospital&Jiangsu Institute of Cancer Research The Affiliated Cancer Hospital of Nanjing Medical UniversityNanjingJiangsu 210009PR China

SIRT6 belongs to class III sirtuin family with NAD+-dependent histone deacetylase activities and controls multiple processes including aging,metabolism and inflammation.In recent years,increasing studies showed tumor suppressor role of SIRT6 in HCC development.We established a two-stage DEN followed CC14 induced liver carcinogenesis in the hepatic-specific SIRT6 HKO mice models and found that hepatic S1RT6 deficit significantly promotes liver injury and liver cancer through inhibition of the ERK1/2 pathway.SIRT6 was compensatory up-regulated in mice tumor tissues and human HCC cells and overexpressed SIRT6 inhibits tumor growth both in vitro and in vivo.Taken together,we provide a useful mouse model for delineating the molecular pathways involved in chronic liver diseases and primary liver cancer and suggest that SIRT6 can be a promising target for HCC therapies.

关键词： ERK1/2 pathway HCC Liver carcinogenesis Mouse model SIRT6

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Overexpression of wild-type HRAS drives non-alcoholic steatohepatitis to hepatocellular carcinoma in mice

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Zoological Research 2024年第3期45卷 551-566页

作者： Chen Ling Su-Su Liu Yu-Ya Wang Gui-Tao Huo Yan-Wei Yang Nan Xu Hong Wang Yong Wu Yu-Fa Miao Rui Fu Yu-Wei Zhao Chang-Fa Fan College of Life Sciences Northwest UniversityProvincial Key Laboratory of Biotechnology of Shaanxi ProvinceXi’anShaanxi 710069China Division of Animal Model Research Institute for Laboratory Animal ResourcesNational Institutes for Food and Drug Control(NIFDC)Beijing 102629China National Center for Safety Evaluation of Drugs National Institutes for Food and Drug Control(NIFDC)Beijing 100176China Division of HIV/AIDS and Sexually Transmitted Virus Vaccines Institute for Biological Products ControlNational Institutes for Food and Drug Control(NIFDC)Beijing 102629China Division of Laboratory Animal Monitoring Institute for Laboratory Animal ResourcesNational Institutes for Food and Drug Control(NIFDC)Beijing 102629China

Hepatocellular carcinoma(HCC),a prevalent solid carcinoma of significant concern,is an aggressive and often fatal disease with increasing global incidence rates and poor therapeutic outcomes.The etiology and pathological progression of non-alcoholic steatohepatitis(NASH)-related HCC is multifactorial and multistage.However,no single animal model can accurately mimic the full NASH-related HCC pathological progression,posing considerable challenges to transition and mechanistic studies.Herein,a novel conditional inducible wild-type human HRAS overexpressed mouse model(HRAS-HCC)was established,demonstrating 100%morbidity and mortality within approximately one month under normal dietary and lifestyle conditions.Advanced symptoms of HCC such as ascites,thrombus,internal hemorrhage,jaundice,and lung metastasis were successfully replicated in mice.In-depth pathological features of NASH-related HCC were demonstrated by pathological staining,biochemical analyses,and typical marker gene detections.Combined murine anti-PD-1 and sorafenib treatment effectively prolonged mouse survival,further confirming the accuracy and reliability of the model.Based on protein-protein interaction(PPI)network and RNA sequencing analyses,we speculated that overexpression of HRAS may initiate the THBS1-COL4A3 axis to induce NASH with severe fibrosis,with subsequent progression to HCC.Collectively,our study successfully duplicated natural sequential progression in a single murine model over a very short period,providing an accurate and reliable preclinical tool for therapeutic evaluations targeting the NASH to HCC continuum.

关键词： HRAS THBS1 HCC driver factor NASH Fibrosis Cirrhosis HCC Treatment evaluation

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Immunobiology and immunotherapy of HCC:spotlight on innate and innate-like immune cells

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Cellular & Molecular Immunology 2021年第1期18卷 112-127页

作者： Benjamin Ruf Bernd Heinrich Tim F.Greten Gastrointestinal Malignancy Section Thoracic and Gastrointestinal Malignancies BranchCentre for Cancer ResearchNational Cancer InstituteNational Institutes of HealthBethesdaMD 20892USA NCI CCR Liver Cancer Program National Institutes of HealthBethesdaMD 20892USA

Immune-based therapies such as immune checkpoint inhibitors have revolutionized the systemic treatment of various cancer types.The therapeutic application of monoclonal antibodies targeting inhibitory pathways such as programmed cell death-1(PD-1)/programmed cell death ligand 1(PD-L1)and CTLA-4 to cells of the adaptive immune system has recently been shown to generate meaningful improvement in the clinical outcome of hepatocellular carcinoma(HCC).Nevertheless,current immunotherapeutic approaches induce durable responses in only a subset of HCC patients.Since immunologic mechanisms such as chronic inflammation due to chronic viral hepatitis or alcoholic and nonalcoholic fatty liver disease play a crucial role in the initiation,development,and progression of HCC,it is important to understand the underlying mechanisms shaping the unique tumor microenvironment of liver cancer.The liver is an immunologic organ with large populations of innate and innate-like immune cells and is exposed to bacterial,viral,and fungal antigens through the gut-liver axis.Here,we summarize and highlight the role of these cells in liver cancer and propose strategies to therapeutically target them.We also discuss current immunotherapeutic strategies in HCC and outline recent advances in our understanding of how the therapeutic potential of these agents might be enhanced.

关键词： HCC immunotherapy innate immunity tumor microenvironment

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Expression and functions of transient receptor potential channels in liver diseases

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Acta Pharmaceutica Sinica B 2023年第2期13卷 445-459页

作者： Wenhui Wang Pengyu Liu Yalin Zhang Li Yan Michael X.Zhu Jin Wang Ye Yu Department of Pharmacology School of PharmacyChina Pharmaceutical UniversityNanjing 210009China Department of Medical Genetics and Developmental Biology School of Medicinethe Key Laboratory of Developmental Genes and Human DiseasesMinistry of EducationSoutheast UniversityNanjing 210009China School of Basic Medicine and Clinical Pharmacy and State Key Laboratory of Natural Medicines China Pharmaceutical UniversityNanjing 210009China Department of Integrative Biology and Pharmacology McGovern Medical Schoolthe University of Texas Health Science Center at HoustonHoustonTX 77030USA

Liver diseases constitute a major healthcare burden globally,including acute hepatic injury resulted from acetaminophen overdose,ischemia-reperfusion or hepatotropic viral infection and chronic hepatitis,alcoholic liver disease(ALD),non-alcoholic fatty liver disease(NAFLD)and hepatocellular carcinoma(HCC).Attainable treatment strategies for most liver diseases remain inadequate,highlighting the importance of substantial pathogenesis.The transient receptor potential(TRP)channels represent a versatile signalling mechanism regulating fundamental physiological processes in the liver.It is not surprising that liver diseases become a newly explored field to enrich our knowledge of TRP channels.Here,we discuss recent findings revealing TRP functions across the fundamental pathological course from early hepatocellular injury caused by various insults,to inflammation,subsequent fibrosis and hepatoma.We also explore expression levels of TRPs in liver tissues of ALD,NAFLD and HCC patients from Gene Expression Omnibus(GEO)or The Cancer Genome Atlas(TCGA)database and survival analysis estimated by Kaplan-Meier Plotter.At last,we address the therapeutical potential and challenges by pharmacologically targeting TRPs to treat liver diseases.The aim is to provide a better understanding of the implications of TRP channels in liver diseases,contributing to the discovery of novel therapeutic targets and efficient drugs.

关键词： TRP Liver disease Liver injury ALD NAFLD Fibrosis Inflammation HCC

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A smart dual-drug nanosystem based on coassembly of plant and food-derived natural products for synergistic HCC immunotherapy

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Acta Pharmaceutica Sinica B 2021年第1期11卷 246-257页

作者： Bingchen Zhang Jiali Jiang Pengyu Wu Junjie Zou Jingqing Le Juanfang Lin Chao Li Bangyue Luo Yongjie Zhang Rui Huang Jingwei Shao Fujian Provincial Key Laboratory of Cancer Metastasis Chemoprevention and Chemotherapy College of ChemistryFuzhou UniversityFuzhou 350116China Institute of Oceanography Minjiang UniversityFuzhou 350108China

Nanotechnology has emerged as an ideal approach for achieving the efficient chemo agent delivery.However,the potential toxicity and unclear internal metabolism of most nano-carriers was still a major obstacle for the clinical application.Herein,a novel"core-shell"co-assembly carrier-free nanosystem was constructed based on natural sources of ursolic acid(UA)and polyphenol(EGCG)with the EpCAM-aptamer modification for hepatocellular carcinoma(HCC)synergistic treatment.As the nature products derived from food-plant,UA and EGCG had good anticancer activities and low toxicity.With the simple and"green"method,the nanodrugs had the advantages of good stability,p H-responsive and strong penetration of tumor tissues,which was expected to increase tumor cellular uptake,long circulation and effectively avoid the potential defects of traditional carriers.The nanocomplex exhibited the low cytotoxicity in the normal cells in vitro,good biosafety of organic tissues and efficient tumor accumulation in vivo.Importantly,UA combined with EGCG showed the immunotherapy by activating the innate immunity and acquired immunity resulting in significant synergistic therapeutic effect.The research could provide new ideas for the research and development of self-assembly delivery system in the future,and offer effective intervention strategies for clinical HCC treatment.

关键词： Natural product Ursolic acid EGCG Aptamer Co-assembly Nanodrug HCC Synergistic treatment Immunotherapy

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