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Dietary Cholesterol Drives Fatty Liver-Associated Liver Cancer By Hepatology ORIGINAL RESEARCH Dietary cholesterol drives fatty liver- associated liver Gut: first published as 10.1136/gutjnl-2019-319664 on 21 July 2020. Downloaded from cancer by modulating gut microbiota and metabolites Xiang Zhang,1 Olabisi Oluwabukola Coker,1 Eagle SH Chu,1 Kaili Fu,1 Harry C H Lau ,1 Yi- Xiang Wang,2 Anthony W H Chan,3 Hong Wei,4,5 Xiaoyong Yang,6 Joseph J Y Sung,1 Jun Yu 1 ► Additional material is ABSTRACT Significance of this study published online only. To view Objective Non- alcoholic fatty liver disease (NAFLD)- please visit the journal online associated hepatocellular carcinoma (HCC) is an (http:// dx. doi. org/ 10. 1136/ What is already known on this subject? gutjnl- 2019- 319664). increasing healthcare burden worldwide. We examined the role of dietary cholesterol in driving NAFLD–HCC ► Non- alcoholic fatty liver disease (NAFLD)- For numbered affiliations see associated hepatocellular carcinoma (HCC) is end of article. through modulating gut microbiota and its metabolites. Design High-fat/high- cholesterol (HFHC), high- fat/ an increasing healthcare burden worldwide. ► Cholesterol is a major lipotoxic molecule. Correspondence to low- cholesterol or normal chow diet was fed to C57BL/6 Jun Yu, Institute of Digestive male littermates for 14 months. Cholesterol-lowering What are the new findings? Disease and The Department drug atorvastatin was administered to HFHC- fed mice. ► High- fat high- cholesterol diet (HFHC) of Medicine and Therapeutics, Germ-free mice were transplanted with stools from Chinese University of Hong spontaneously and sequentially induced fatty Kong, New Territories, Hong mice fed different diets to determine the direct role liver, steatohepatitis, fibrosis and NAFLD–HCC Kong; junyu@ cuhk. edu. hk of cholesterol modulated- microbiota in NAFLD–HCC. development, while high- fat low- cholesterol Gut microbiota was analysed by 16S rRNA sequencing diet induced only hepatic steatosis in male XZ and OOC are co-first authors. and serum metabolites by liquid chromatography– mice. mass spectrometry (LC–MS) metabolomic analysis. Received 19 August 2019 ► Dietary cholesterol- induced NAFLD–HCC Revised 4 June 2020 Faecal microbial compositions were examined in 59 formation was associated with gut microbiota Accepted 15 June 2020 hypercholesterolemia patients and 39 healthy controls. dysbiosis. The microbiota composition changed Results High dietary cholesterol led to the sequential along stages of NAFLD–HCC formation: progression of steatosis, steatohepatitis, fibrosis and Mucispirillum, Desulfovibrio, Anaerotruncus http://gut.bmj.com/ eventually HCC in mice, concomitant with insulin and Desulfovibrionaceae were sequentially resistance. Cholesterol- induced NAFLD–HCC formation increased; while Bifidobacterium and was associated with gut microbiota dysbiosis. The Bacteroides were depleted in HFHC- fed microbiota composition clustered distinctly along stages mice, which was corroborated in human of steatosis, steatohepatitis and HCC. Mucispirillum, hypercholesteremia patients. Desulfovibrio, Anaerotruncus and Desulfovibrionaceae ► Gut bacterial metabolites alteration including increased sequentially; while Bifidobacterium and increased serum taurocholic acid (TCA) on September 24, 2021 by guest. Protected copyright. Bacteroides were depleted in HFHC-fed mice, which was and depleted 3- indolepropionic acid (IPA) corroborated in human hypercholesteremia patients. was found in NAFLD–HCC. IPA inhibited Dietary cholesterol induced gut bacterial metabolites cholesterol- induced lipid accumulation and cell alteration including increased taurocholic acid and proliferation, while TCA aggravated cholesterol- decreased 3-indolepropionic acid. Germ-free mice induced triglyceride accumulation in human gavaged with stools from mice fed HFHC manifested normal immortalised hepatocyte cell line. hepatic lipid accumulation, inflammation and cell ► Germ- free mice gavaged with stools from proliferation. Moreover, atorvastatin restored cholesterol- HFHC- fed mice manifested hepatic lipid induced gut microbiota dysbiosis and completely accumulation, inflammation and cell prevented NAFLD–HCC development. proliferation, in consistence with donor mice Conclusions Dietary cholesterol drives NAFLD–HCC phenomes. formation by inducing alteration of gut microbiota and ► Anticholesterol treatment restored dietary metabolites in mice. Cholesterol inhibitory therapy and © Author(s) (or their cholesterol- induced gut microbiota dysbiosis employer(s)) 2020. Re- use gut microbiota manipulation may be effective strategies and completely prevented NAFLD–HCC permitted under CC BY- NC. No for NAFLD–HCC prevention. formation. commercial re- use. See rights and permissions. Published How might it impact on clinical practice in the by BMJ. foreseeable future? INTRODUCTION Our findings indicate that anticholesterol drug To cite: Zhang X, Coker OO, Non- alcoholic fatty liver disease (NAFLD) is the ► Chu ESH, et al. Gut Epub and manipulation of the gut microbiota might hepatic manifestation of metabolic syndrome, ahead of print: [please represent effective strategies in preventing include Day Month Year]. which encompasses a spectrum of liver pathologies NAFLD–HCC. doi:10.1136/ that range from simple steatosis to non- alcoholic gutjnl-2019-319664 steatohepatitis (NASH).1 NASH can progress to Zhang X, et al. Gut 2020;0:1–14. doi:10.1136/gutjnl-2019-319664 1 Hepatology hepatic cirrhosis, end- stage liver failure and hepatocellular carci- stored at −80°C for further experiments. Mice stool samples noma (HCC).2 Currently, NAFLD is a major cause of morbidity were collected for bacterial 16S rRNA gene sequencing and oral and a healthcare burden worldwide. Large population-based gavage. Gut: first published as 10.1136/gutjnl-2019-319664 on 21 July 2020. Downloaded from cohort studies demonstrate that the prevalence of NAFLD–HCC C57BL/6 male germ- free mice (7 weeks) were bred at the has increased by fourfold in the last decade compared with 2.5- Department of Laboratory Animal Science at the Third Military fold for hepatitis, making it the most rapidly growing indication Medical University in Chongqing, China. Adult mice (8 weeks for liver transplantation.3 Lipotoxicity drives the progression of old) were divided into three groups (11–28 mice per group), NASH, fibrosis/cirrhosis, and even HCC.4 Among hepatic lipid and gavaged twice at 0 and 7 months with stools obtained from species, cholesterol is considered a major lipotoxic molecule conventional mice fed with NC, HFLC, HFHC or HFHC mice in NASH development.4 The liver is central to the regulation treated with atorvastatin for 14 months. Briefly, 1 g of stool of systemic cholesterol homeostasis. Abnormalities in hepatic samples were homogenised in 5 mL of phosphate buffered saline cholesterol homeostasis have been demonstrated in both human (PBS). Recipient mice were then transplanted with 200 μL of and experimental models of NASH.5 6 We have revealed that the suspension by gastric gavage. Mice from each group were squalene epoxidase, a rate- limiting enzyme in cholesterol biosyn- randomly selected and sacrificed at 8, 10 or 14 months following thesis, drives NAFLD–HCC development.7 Dietary cholesterol transplantation. has an important impact on plasma and hepatic cholesterol Additional methods are provided in online supplementary file homeostasis.5 Although the contribution of dietary cholesterol 1. to NASH progression has been reported,5 8 the role and patho- genic basis of long-term cholesterol treatment on spontaneous RESULTS and progressive NAFLD–HCC development are unknown. Dietary cholesterol drives the development of NAFLD–HCC The intestinal microbiota has a symbiotic relationship with spontaneously its host and contributes nutrients and energy by metabolising To examine the role of dietary cholesterol in the evolution of dietary components including cholesterol in the large intes- steatosis, NASH, fibrosis and subsequent NAFLD–HCC, mice tine.9 Several studies have suggested that the gut microbiome were fed with HFHC,17 HFLC or NC. Serum level of alpha- represents an environmental factor contributing to the devel- fetoprotein (AFP, marker for liver cancer) was monitored at opment of NAFLD and its progression to NAFLD–HCC.10 11 different time points (3, 8, 10, 12 and 14 months). An elevated Microbe- derived metabolites, such as bile acid, short- chain AFP level was observed at month 10 (107.1±127.9 ng/mL), fatty acids and trimethylamine and the signalling pathways they which was further increased at month 12 (151.6±129.3 ng/mL) affect may contribute to NAFLD development.12 13 In partic- and month 14 (174.2±203.1 ng/mL) in mice fed with HFHC ular, 3-(4- hydroxyphenyl) lactate, a metabolite derived from gut compared with HFLC (50.9±7.5 ng/mL in HFLC) or NC microbiome, has a shared gene‐effect with both hepatic steatosis (59.7±20.9 ng/mL) at month 14 (figure 1A). MRI scan showed and fibrosis.14 Moreover, the alteration of gut microbiota profile liver tumours in HFHC-fed mice but not in HFLC-fed or by dietary cholesterol has been reported.15 However, whether gut NC-fed mice at month 14 (figure 1B). Mice were then harvested microbiota dysbiosis is the cause or effect of dietary cholesterol- http://gut.bmj.com/ at month 14. Liver tumours were identified in 68% (13/19) of induced NASH and NAFLD–HCC progression remains unclear. mice fed with HFHC but not in mice fed with HFLC or NC diet The present study was performed to determine the role and (figure 1C). Histological examination of liver
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