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G protein-coupled receptor 35 attenuates nonalcoholic steatohepatitis by reprogramming cholesterol homeostasis in hepatocytes

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Acta Pharmaceutica Sinica B 2023年第3期13卷 1128-1144页

作者： Xiaoli Wei Fan Yin Miaomiao Wu Qianqian Xie Xueqin Zhao Cheng Zhu Ruiqian Xie Chongqing Chen Menghua Liu Xueying Wang Ruixue Ren Guijie Kang Chenwen Zhu Jingjing Cong Hua Wang Xuefu Wang Department of Oncology the First Affiliated Hospital of Anhui Medical UniversityHefei 230036China Department of Pharmacy Huainan First People's Hospitalthe First Affiliated Hospital of Anhui University of Science and TechnologyHuainan 232001China School of Pharmacy Anhui Medical UniversityHefei 230032China Inflammation and Immune Mediated Diseases Laboratory of Anhui Province Anhui Medical UniversityHefei 230032China

Nonalcoholic fatty liver disease(NAFLD)is the most common chronic liver disease worldwide.Fat accumulation“sensitizes”the liver to insult and leads to nonalcoholic steatohepatitis(NASH).G protein-coupled receptor 35(GPR35)is involved in metabolic stresses,but its role in NAFLD is unknown.We report that hepatocyte GPR35 mitigates NASH by regulating hepatic cholesterol homeostasis.Specifically,we found that GPR35 overexpression in hepatocytes protected against high-fat/cholesterol/fructose(HFCF)diet-induced steatohepatitis,whereas loss of GPR35 had the opposite effect.Administration of the GPR35 agonist kynurenic acid(Kyna)suppressed HFCF diet-induced steatohepatitis in mice.Kyna/GPR35 induced expression of StAR-related lipid transfer protein 4(STARD4)through the ERK1/2 signaling pathway,ultimately resulting in hepatic cholesterol esterification and bile acid synthesis(BAS).The overexpression of STARD4 increased the expression of the BAS rate-limiting enzymes cytochrome P450 family 7 subfamily A member 1(CYP7A1)and CYP8B1,promoting the conversion of cholesterol to bile acid.The protective effect induced by GPR35 overexpression in hepatocytes disappeared in hepatocyte STARD4-knockdown mice.STARD4 overexpression in hepatocytes reversed the aggravation of HFCF diet-induced steatohepatitis caused by the loss of GPR35 expression in hepatocytes in mice.Our findings indicate that the GPR35–STARD4 axis is a promising therapeutic target for NAFLD.

关键词： G protein-coupled receptor 35 Kynurenic acid steatohepatitis Cholesterol Bile acid STARD4 ACAT2 CYP7A1

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Prognostic Relevance of Metabolic Dysfunction-associated steatohepatitis for Patients with Chronic Hepatitis B

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Journal of Clinical and Translational Hepatology 2023年第1期11卷 76-87页

作者： Manus Rugivarodom Ananya Pongpaibul Siwaporn Chainuvati Supot Nimanong Watcharasak Chotiyaputta Tawesak Tanwandee Phunchai Charatcharoenwitthaya Division of Gastroenterology Department of MedicineFaculty of Medicine Siriraj HospitalMahidol UniversityBangkokThailand Department of Pathology Faculty of Medicine Siriraj HospitalMahidol UniversityBangkokThailand

Background and Aims:Metabolic dysfunction-associated fatty liver disease(MAFLD)is prevalent in patients with chronic hepatitis B(CHB).The effect of the histologic MAFLD phenotype on long-term CHB outcomes is unknown.We performed a longitudinal study to determine the prognostic relevance of biopsy-proven hepatic steatosis and steatohepatitis for CHB patients.Methods:Clinical and laboratory data were obtained from CHB patients who underwent liver biopsy during 2002–2008 and were treated with antiviral drugs.A hepatopathologist reviewed the biopsy specimens.Cox proportional hazards regression was used to estimate the adjusted hazard ratio(aHR)of outcomes,including all-cause mortality,liver transplantation,and liver-related events.Results:In accordance with Brunt’s classification,408 patients had steatohepatitis(n=34),“steatosis but not steatohepatitis”(n=118),or“non-steatosis”(n=256).All steatohepatitis patients had features of metabolic dysfunction.Over a mean follow-up of 13.8±3.1 years,18 patients died or underwent liver transplantation.In multivariate-adjusted analysis,steatohepatitis(aHR,6.37;95%confidence interval[CI]:1.59–25.5)compared with non-steatosis and advanced fibrosis(aHR,11.3;95%CI:1.32–96.3)compared with no fibrosis were associated with overall mortality/liver transplantation.Thirty-five patients developed 43 liver-related events,among which 32 were hepatocellular carcinoma.These events were associated with steatohepatitis(aHR,5.55;95%CI:2.01–15.3)compared with non-steatosis and advanced fibrosis(aHR,6.23;95%CI:1.75–22.2)compared with no fibrosis.The steatosis but not steatohepatitis group had a nonsignificantly higher risk of overall mortality and liver-related events.Conclusions:Metabolic dysfunction-associated steatohepatitis increased the risk of long-term mortality/transplantation and liver-related events in CHB patients.

关键词： Chronic hepatitis B steatohepatitis Liver histology Long-term prognosis

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Alcoholic vs. Nonalcoholic steatohepatitis: Vascular Branching Heterogeneity on Magnetic Resonance Imaging as a Diagnostic Marker

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Journal of Clinical and Translational Hepatology 2023年第3期11卷 534-539页

作者： Daniel Garrido Nicholas Noverati Justin Robbins Jaydev K.Dave Haresh Naringrekar Donald G.Mitchell Dina Halegoua-De Marzio Department of Medicine Division of Gastroenterology and HepatologyThomas Jefferson University HospitalPhiladelphiaPAUSA Department of Medicine Thomas Jefferson University HospitalPhiladelphiaPAUSA Department of Radiology Thomas Jefferson University HospitalPhiladelphiaPAUSA

Background and Aims: Distinguishing alcoholic steato-hepatitis (ASH) and nonalcoholic steatohepatitis (NASH) with biopsy alone is often difficult without a reliable clinical con-text. A novel finding on liver imaging, perivascular branching heterogeneity, has shown promise in distinguishing between these chronic liver diseases. Our study investigated the role of this finding on imaging to differentiate between ASH and NASH. The aim of this study was to determine the utility and reproducibility of this novel radiographic marker to help dis-tinguish ASH from NASH. Methods: This was a retrospective cohort study conducted between 2016 and 2020 in patients with both liver biopsy-confirmed steatohepatitis/chronic hep-atitis and abdominal magnetic resonance imaging within 13 months of each other. Two radiologists, blinded to patient clinical history and diagnosis, categorized the appearance of the liver as: 1- homogeneity, 2- mild heterogeneity, 3- mod-erate heterogeneity, 4- possible perivascular branching, 5- definite perivascular branching. Results: Of the 90 patients in the study, 60 were identified as NASH and 30 as ASH. The area under the curve (AUC) for both reader 1 and 2 when us-ing the 5-point scale was 0.69 (CI: 0.56-0.82, p=0.006) and 0.72 (CI: 0.60-0.85, p=0.001), respectively. The positive predictive value (PPV) for identification of ASH when scoring 5 was 64.7% and 66.7% for reader 1 and 2, respectively. In-terclass correlation coefficient was 0.74 in patients with ASH, indicating moderate reliability among both readers. Conclu-sions: Identification of this perivascular branching pattern on imaging is a promising novel diagnostic marker that can be used with other methods to help distinguish between ASH and NASH.

关键词： Alcoholic liver diseases steatohepatitis Magnetic resonance imag-ing Nonalcoholic fatty liver disease

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Changes in the terminology and diagnostic criteria of non-alcoholic fatty liver disease:Implications and opportunities

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World Journal of Gastrointestinal Pathophysiology 2024年第1期15卷 1-8页

作者： Muhammed Mubarak Javed I.Kazi Department of Histopathology Sindh Institute of Urology and TransplantationKarachi 74200Pakistan

Fatty liver disease(FLD)is a highly prevalent pathological liver disorder.It has many and varied etiologies and has heterogeneous clinical course and outcome.Its proper nomenclature and classification have been problematic since its initial recognition.Traditionally,it was divided into two main categories:Alcoholassociated liver disease and nonalcoholic FLD(NAFLD).Among these,the latter condition has been plagued with nomenclature and classification issues.The two main objections to its use have been the use of negative(non-alcoholic)and stigmatizing(fatty)terms in its nomenclature.Numerous attempts were made to address these issues but none achieved universal acceptance.Just recently,NAFLD has received a new nomenclature from an international collaborative effort based on a rigorous scientific methodology.FLD has been renamed steatotic liver disease(SLD),and NAFLD as metabolic dysfunction-associated SLD.Metabolic dysfunction-associated steatohepatitis was chosen as the replacement terminology for non-alcoholic steatohepatitis.This is a significant positive change in the nomenclature and categorization of FLD and will likely have a major impact on research,diagnosis,treatment,and prognosis of the disease in the future.

关键词： Fatty liver disease Metabolic syndrome Non-alcoholic fatty liver disease Steatotic liver disease steatohepatitis

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Steatosis and steatohepatitis in postmortem material from Northwestern Greece

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World Journal of Gastroenterology 2010年第31期16卷 3944-3949页

作者： Christos D Zois Gerasimos H Baltayiannis Anna Bekiari Anna Goussia Peter Karayiannis Michalis Doukas Demetrios Demopoulos Antigoni Mitsellou Theodoros Vougiouklakis Vasiliki Mitsi Epameinondas V Tsianos 1st Department of Internal Medicine and Hepato-Gastroenterology Unit Medical SchoolUniversity of Ioannina Laboratory of Pathology Medical SchoolUniversity Hospital of Ioannina Department of Medicine Hepatology Sec-tionDivision of MedicineImperial College LondonVariety Wing Floor DSt.Mary's Campus Norfolk Place London W2 1PGLondonUnited Kingdom Department of Forensic Medicine and Toxicology Medical SchoolUniversity of Ioannina

AIM: To determine the prevalence of steatosis and steatohepatitis in a series of autopsies in Northwestern Greece. METHODS: Liver biopsy material from a total of 600 autopsies performed over a period of 2 years (2006-2008) to def ine the cause of death was subjected to histological examination. Patient demographic data were also collected. Tissue sections were stained with different dyes for the evaluation of liver architecture, degree of fibrosis and other pathological conditions when necessary. RESULTS: Satisfactory tissue samples for histological evaluation were available in 498 cases (341 male, 157 female) with a mean age of 64.51 ± 17.78 years. In total, 144 (28.9%) had normal liver histology, 156 (31.3%) had evidence of steatosis, and 198 (39.8%) had typical histological findings of steatohepatitis. The most common causes of death were ischemic heart disease with or without myocardial infarction (43.4%), and traffic accidents (13.4%). CONCLUSION: A high prevalence of steatosis and steatohepatitis was detected in postmortem biopsies from Northwestern Greece. Since both diseases can have serious clinical consequences, they should be considered as an important threat to the health of the general population in Greece.

关键词： Fatty liver Non-alcoholic liver disease Steatosis steatohepatitis Autopsy

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Effect of Soothing Gan(Liver) and Invigorating Pi(Spleen) Recipes on TLR4-p38 MAPK Pathway in Kupffer Cells of Non-alcoholic steatohepatitis Rats

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Chinese Journal of Integrative Medicine 2019年第3期25卷 216-224页

作者： GONG Xiang-wen XU Yong-jian YANG Qin-he LIANG Yin-ji ZHANG Yu-pei WANG Guan-long LI Yuan-yuan School of Chinese Medicine Jinan University

Objective: To investigate the mechanism of inflammatory-mediated toll-like receptor 4(TLR4)-p38 mitogen-activated protein kinase(p38 MAPK) pathway in Kupffer cells(KCs) of non-alcoholic steatohepatitis(NASH) rats and the intervention effect of soothing Gan(Liver) and invigorating Pi(Spleen) recipes on this pathway. Methods: After 1 week of acclimatization, 120 Sprague-Dawley male rats were randomly divided into 8 groups using a random number table(n=15 per group): normal group, model group, low-dose Chaihu Shugan Powder(柴胡疏肝散, CHSG) group(3.2 g/kg), high-dose CHSG group(9.6 g/kg), low-dose Shenling Baizhu Powder(参苓白术散, SLBZ) group(10 g/kg), high-dose SLBZ(30 g/kg) group, and low-and highdose integrated recipe(L-IR, H-IR) groups. All rats in the model and treatment groups were fed with a high-fat diet(HFD). The treatments were administrated by gastrogavage once daily and lasted for 26 weeks. The liver tissues were detected with hematoxylin-eosin(HE) and oil red O staining. Levels of liver lipids, serum lipids and transaminases were measured. KCs were isolated from the livers of rats to evaluate the mRNA expressions of TLR4 and p38 MAPK by real-time fluorescence quantitative polymerase chain reaction, and proteins expressions of TLR4, p-p38 MAPK and p38 MAPK by Western blot. Levels of inflammatory cytokines including tumor necrosis factor α(TNF-α), interleukin(IL)-1 and IL-6 in KCs were measured by enzyme-linked immunosorbent assay. Results: After 26 weeks of HFD feeding, HE and oil red O staining showed that the NASH model rats successfully reproduced typical pathogenesis and histopathological features. Compared with the normal group, the model group exhibited significant increases in body weight, liver weight, liver index, serum levels of total cholesterol(TC), triglyceride(TG), low-density lipoprotein cholesterol, and aspartate aminotransferase as well as TC and TG levels in liver tissues, and significant decrease in serum level of high-density lipoprotein cholesterol(P<0.05 or P<0.01), while those indices were

关键词： non-alcoholic steatohepatitis soothing Gan (Liver)and invigorating Pi (Spleen)recipes Kupffer cel toll-like receptor 4-p38 mitogen-activated protein kinase signaling pathway inflammation,Chinese medicine

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Value of controlled attenuation parameter in fibrosis prediction in nonalcoholic steatohepatitis

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World Journal of Gastroenterology 2019年第33期25卷 4959-4969页

作者： Jung Il Lee Hyun Woong Lee Kwan Sik Lee Department of Internal Medicine Gangnam Severance Hospital Yonsei University College of Medicine

BACKGROUND Liver stiffness measurement(LSM)tends to overestimate fibrosis stage in nonalcoholic fatty liver disease(NAFLD).Controlled attenuation parameter(CAP),provided by LSM device,has been introduced for noninvasive quantification of hepatic steatosis.AIM To determine the role of CAP values in predicting liver fibrosis stage by LSM in nonalcoholic steatohepatitis(NASH).METHODS One hundred eighty-four patients with biopsy proven NASH had LSM and CAP evaluated at baseline.Among them,130 patients had 1-year follow up LSM and analyzed for the changes of LSM after pioglitazone or ursodeoxycholic acid(UDCA)treatment.RESULTS In Kleiner fibrosis stage F0-1,LSM values increased at higher CAP tertile(P=0.001),and in F2,at middle and higher tertiles(P=0.027).No difference across CAP tertiles was noticed in F3-4(P=0.752).Receiver operating characteristic curve for LSM cutoff in diagnosis of F≥2 identified 8.05 kPa for lower CAP tertile,9.35 kPa for middle,and 10.55 kPa for high tertile.When changes in proportion of significant fibrosis(F≥2)were assessed among pioglitazone and UDCA treated patients considering CAP values,pioglitazone treated patients demonstrated decrease in proportion of high LSM.CONCLUSION In patient with NAFLD,interpretation of LSM in association with CAP scores may provide helpful information sparing unnecessary liver biopsy.

关键词： Fibroscan Controlled attenuation parameter Liver stiffness Nonalcoholic steatohepatitis Liver fibrosis

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INT-767 improves histopathological features in a dietinduced ob/ob mouse model of biopsy-confirmed nonalcoholic steatohepatitis

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World Journal of Gastroenterology 2018年第2期24卷 195-210页

作者： Jonathan D Roth Michael Feigh Sanne S Veidal Louise KD Fensholdt Kristoffer T Rigbolt Henrik H Hansen Li C Chen Mathieu Petitjean Weslyn Friley Niels Vrang Jacob Jelsing Mark Young Intercept Pharmaceuticals Intercept PharmaceuticalsSan DiegoCA 92121United States Gubra Hoersholm DK-2970Denmark PharmaNest Genesis Imaging ServicesPrincetonNJ 08540United States Qualyst Transporter Solutions DurhamNC 27713United States

AIM To characterize the efficacy of the dual FXR/TGR5 receptor agonist INT-767 upon histological endpoints in a rodent model of diet-induced and biopsy-confirmed non-alcoholic steatohepatitis(NASH).METHODS The effects of INT-767 on histological features of NASH were assessed in two studies using Lep^(ob/ob)(ob/ob) NASH mice fed the AMLN diet(high fat with transfat, cholesterol and fructose). In a proof-of-conceptstudy, Lep^(ob/ob)(ob/ob) NASH mice were first dosed with INT-767(3 or 10 mg/kg for 8 wk). A second ob/ob NASH study compared INT-767(3 and 10 mg/kg) to obeticholic acid(OCA)(10 or 30 mg/kg; 16 wk). Primary histological endpoints included qualitative and quantitative assessments of NASH. Other metabolic and plasma endpoints were also assessed. A comparative assessment of INT-767 and OCA effects on drug distribution and hepatic gene expression was performed in C57 Bl/6 mice on standard chow. C57 Bl/6 mice were orally dosed with INT-767 or OCA(1-30 mg/kg) for 2 wk, and expression levels of candidate genes were assessed by RNA sequencing and tissue drug levels were measured by liquid chromatography tandem-mass spectrometry.RESULTS INT-767 dose-dependently(3 and 10 mg/kg, PO, QD, 8 wk) improved qualitative morphometric scores on steatohepatitis severity, inflammatory infiltrates and fibrosis stage. Quantitative morphometric analyses revealed that INT-767 reduced parenchymal collagen area, collagen fiber density, inflammation(assessed by Galectin-3 immunohistochemistry) and hepatocyte lipid droplet area following INT-767 treatment. In a comparative study(16 wk), the FXR agonists OCA(10 and 30 mg/kg) and INT-767(3 and 10 mg/kg) both improved NASH histopathology, with INT-767 exerting greater therapeutic potency and efficacy than OCA. Mechanistic studies suggest that both drugs accumulate similarly within the liver and ileum, however, the effects of INT-767 may be driven by enhanced hepatic, but not ileal, FXR function. CONCLUSION These findings confirm the potential utility of FXR and dual FXR/TGR5 activation a

关键词： Non-alcoholic steatohepatitis INT-767 Obeticholic acid Liver biopsy FXR TGR5 Mouse model

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Arachidyl amido cholanoic acid improves liver glucose and lipid homeostasis in nonalcoholic steatohepatitis via AMPK and mTOR regulation

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World Journal of Gastroenterology 2020年第34期26卷 5101-5117页

作者： David Fernández-Ramos Fernando Lopitz-Otsoa Laura Delacruz-Villar Jon Bilbao Martina Pagano Laura Mosca Maider Bizkarguenaga Marina Serrano-Macia Mikel Azkargorta Marta Iruarrizaga-Lejarreta Jesús Sot Darya Tsvirkun Sebastiaan Martijn van Liempd Felix M Goni Cristina Alonso María Luz Martínez-Chantar Felix Elortza Liat Hayardeny Shelly C Lu JoséM Mato Precision Medicine and Metabolism Laboratory Centro de Investigación Cooperativa en Biociencias(CIC bioGUNE)Derio 48160BizkaiaSpain CIBERehd-Centro de Investigación Biomédica en Red de enfermedades hepáticas y digestivas Madrid 28029Spain Department of Precision Medicine University of Campania"Luigi Vanvitelli"Naples 80138Italy Liver Disease Laboratory Centro de Investigación Cooperativa en Biociencias(CIC bioGUNE)Derio 48160Spain Proteomics Platform Centro de Investigación Cooperativa en Biociencias(CIC bioGUNE)Derio 48160Spain OWL Metabolomics Derio 48160Spain Instituto Biofisika(UPV/EHU CSIC)Leioa 48940SpainDepartamento de Bioquímica y Biología MolecularUniversidad del País VascoLeioa 48940Spain Pre-clinical and Chemistry Manufacturing and ControlsGalmed PharmaceuticalsTel Aviv 6578317Israel Metabolomics Platform Centro de Investigación Cooperativa en Biociencias(CIC bioGUNE)Derio 48160Spain Division of Digestive and Liver Diseases Cedars-Sinai Medical CenterLos AngelesCA 90048United States

BACKGROUND Arachidyl amido cholanoic acid(Aramchol)is a potent downregulator of hepatic stearoyl-CoA desaturase 1(SCD1)protein expression that reduces liver triglycerides and fibrosis in animal models of steatohepatitis.In a phase IIb clinical trial in patients with nonalcoholic steatohepatitis(NASH),52 wk of treatment with Aramchol reduced blood levels of glycated hemoglobin A1c,an indicator of glycemic control.AIM To assess lipid and glucose metabolism in mouse hepatocytes and in a NASH mouse model[induced with a 0.1%methionine and choline deficient diet(0.1MCD)]after treatment with Aramchol.METHODS Isolated primary mouse hepatocytes were incubated with 20μmol/L Aramchol or vehicle for 48 h.Subsequently,analyses were performed including Western blot,proteomics by mass spectrometry,and fluxomic analysis with 13C-uniformly labeled glucose.For the in vivo part of the study,male C57BL/6J mice were randomly fed a control or 0.1MCD for 4 wk and received 1 or 5 mg/kg/d Aramchol or vehicle by intragastric gavage for the last 2 wk.Liver metabolomics were assessed using ultra-high-performance liquid chromatography-time of flight-MS for the determination of glucose metabolism-related metabolites.RESULTS Combination of proteomics and Western blot analyses showed increased AMPK activity while the activity of nutrient sensor mTORC1 was decreased by Aramchol in hepatocytes.This translated into changes in the content of their downstream targets including proteins involved in fatty acid(FA)synthesis and oxidation[PACCα/β(S79),SCD1,CPT1A/B,HADHA,and HADHB],oxidative phosphorylation(NDUFA9,NDUFB11,NDUFS1,NDUFV1,ETFDH,and UQCRC2),tricarboxylic acid(TCA)cycle(MDH2,SUCLA2,and SUCLG2),and ribosome(P-p70S6K[T389]and P-S6[S235/S236]).Flux experiments with 13Cuniformely labeled glucose showed that TCA cycle cataplerosis was reduced by Aramchol in hepatocytes,as indicated by the increase in the number of rounds that malate remained in the TCA cycle.Finally,liver metabolomic analysis showed that glucose homeostasis was improved by Aramcho

关键词： Nonalcoholic fatty liver disease steatohepatitis Methionine and choline deficient diet Tricarboxylic acid cycle Hemoglobin A1c Stearoyl-CoA desaturase 1

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Mouse models for investigating the underlying mechanisms of nonalcoholic steatohepatitis-derived hepatocellular carcinoma

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World Journal of Gastroenterology 2018年第18期24卷 1989-1994页

作者： Kazuki Takakura Tsunekazu Oikawa Yoichi Tomita Yusuke Mizuno Masanori Nakano Chisato Saeki Yuichi Torisu Masayuki Saruta Division of Gastroenterology and Hepatology Department of Internal Medicine The Jikei University School of Medicine

As the incidence of hepatocellular carcinoma(HCC) caused by infection with the hepatotropic viruses hepatitis B and hepatitis C decreases, greater attention has become focused on HCC caused by nonalcoholic steatohepatitis(NASH), an advanced form of nonalcoholic fatty liver disease which has shown increasing prevalence in correspondence with the overall increase in metabolic syndrome over the recent decades. Several clinical population studies have shown a positive relationship between NASH and HCC, while also providing initial insights into the underlying mechanisms of HCC development from NASH. Research into the pathological progression of NASH to HCC has advanced by use of several beneficial rodent models. In this review, we summarize the established mouse models for preclinical research of NASH-associated HCC and discuss the underlying hepatic mechanisms of NASH-related tumorigenesis identified to date that could lead to new targets for treatment and prevention.

关键词： Hepatocellular carcinoma Nonalcoholic steatohepatitis Nonalcoholic fatty liver disease

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