Epigenetic Association Study Uncovered H3K27 Acetylation Enhancers and Dysregulated Genes in High-Fat-Diet-Induced Nonalcoholic Fatty Liver Disease in Rats

References

• Lee J , KimY , FrisoS , ChoiS-W. Epigenetics in non-alcoholic fatty liver disease. Mol. Aspects Med.54, 78–88 (2017).
   PubMed Web of Science ®Google Scholar
• Younossi Z , TackeF , ArreseMet al. Global perspectives on nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Hepatology69(6), 2672–2682 (2019).
   PubMed Web of Science ®Google Scholar
• Peverill W , PowellLW , SkoienR. Evolving concepts in the pathogenesis of NASH: beyond steatosis and inflammation. Int. J. Mol. Sci.15(5), 8591–8638 (2014).
   PubMed Web of Science ®Google Scholar
• Buzzetti E , PinzaniM , TsochatzisEA. The multiple-hit pathogenesis of non-alcoholic fatty liver disease (NAFLD). Metabolism65(8), 1038–1048 (2016).
   PubMed Web of Science ®Google Scholar
• Li Y-Y . Genetic and epigenetic variants influencing the development of nonalcoholic fatty liver disease. World J. Gastroenterol.18(45), 6546–6551 (2012).
   PubMed Web of Science ®Google Scholar
• Ashraf NU , AltarM. Epigenetics: an emerging field in the pathogenesis of nonalcoholic fatty liver disease. Mutat. Res. Rev. Mutat. Res.778, 1–12 (2018).
   PubMed Web of Science ®Google Scholar
• Ling C , RonnT. Epigenetics in human obesity and Type 2 diabetes. Cell Metab.29(5), 1028–1044 (2019).
   PubMed Web of Science ®Google Scholar
• Malmgren S , SpegelP , DanielssonAPet al. Coordinate changes in histone modifications, mRNA levels, and metabolite profiles in clonal INS-1 832/13 beta-cells accompany functional adaptations to lipotoxicity. J. Biol. Chem.288(17), 11973–11987 (2013).
   PubMed Web of Science ®Google Scholar
• Nammo T , UdagawaH , FunahashiNet al. Genome-wide profiling of histone H3K27 acetylation featured fatty acid signalling in pancreatic beta cells in diet-induced obesity in mice. Diabetologia61(12), 2608–2620 (2018).
   PubMed Web of Science ®Google Scholar
• Zhu Y , ZengQ , LiFet al. Dysregulated H3K27 acetylation is implicated in fatty liver hemorrhagic syndrome in chickens. Front. Genet.11, 574167 (2020).
   PubMed Web of Science ®Google Scholar
• Zhang T , ZhangZ , DongQ , XiongJ , ZhuB. Histone H3K27 acetylation is dispensable for enhancer activity in mouse embryonic stem cells. Genome Biol.21(1), 45 (2020).
   PubMed Web of Science ®Google Scholar
• Kimura H . Histone modifications for human epigenome analysis. J. Hum. Genet.58(7), 439–445 (2013).
   PubMed Web of Science ®Google Scholar
• Abuin JM , PichelJC , PenaTF , AmigoJ. BigBWA: approaching the Burrows-Wheeler aligner to big data technologies. Bioinformatics31(24), 4003–4005 (2015).
   PubMed Web of Science ®Google Scholar
• Zhang Y , LiuT , MeyerCAet al. Model-based analysis of ChIP-seq (MACS). Genome Biol.9(9), R137 (2008).
   PubMed Web of Science ®Google Scholar
• Quinlan AR , HallIM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics26(6), 841–842 (2010).
   PubMed Web of Science ®Google Scholar
• Villar D , BerthelotC , AldridgeSet al. Enhancer evolution across 20 mammalian species. Cell160(3), 554–566 (2015).
   PubMed Web of Science ®Google Scholar
• Salmon-Divon M , DvingeH , TammojaK , BertoneP. PeakAnalyzer: genome-wide annotation of chromatin binding and modification loci. BMC Bioinformatics11, 415 (2010).
   PubMed Web of Science ®Google Scholar
• Heinz S , BennerC , SpannNet al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell38(4), 576–589 (2010).
   PubMed Web of Science ®Google Scholar
• Li H , HandsakerB , WysokerAet al. The Sequence Alignment/Map format and SAMtools. Bioinformatics25(16), 2078–2079 (2009).
   PubMed Web of Science ®Google Scholar
• Love MI , HuberW , AndersS. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol.15(12), 550 (2014).
   PubMed Web of Science ®Google Scholar
• Dobin A , DavisCA , SchlesingerFet al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics29(1), 15–21 (2013).
   PubMed Web of Science ®Google Scholar
• Liao Y , SmythGK , ShiW. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics30(7), 923–930 (2014).
   PubMed Web of Science ®Google Scholar
• Takahashi JS , KumarV , NakashePet al. ChIP-seq and RNA-seq methods to study circadian control of transcription in mammals. Methods Enzymol.551, 285–321 (2015).
   PubMed Web of Science ®Google Scholar
• Szklarczyk D , MorrisJH , CookHet al. The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible. Nucleic Acids Res.45(D1), D362–D368 (2017).
   PubMed Web of Science ®Google Scholar
• Shannon P , MarkielA , OzierOet al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res.13(11), 2498–2504 (2003).
   PubMed Web of Science ®Google Scholar
• Vonhogen IGC , ElAzzouzi H , OlieslagersSet al. MiR-337-3p promotes adipocyte browning by inhibiting TWIST1. Cells9(4), 1056 (2020).
   PubMed Web of Science ®Google Scholar
• Da Costa KS . Structural analysis of viral infectivity factor of HIV type 1 and its interaction with A3G, EloC and EloB. PLOS ONE9(6), e89116 (2014).
   PubMed Web of Science ®Google Scholar
• Ahmad A , MandwieM , DreismannAKet al. Adeno-associated virus vector gene delivery elevates factor I levels and downregulates the complement alternative pathway in vivo. Hum. Gene Ther.32(21-22), 1370–1381 (2021).
   PubMed Web of Science ®Google Scholar
• Nakajima H , MurakamiY , MoriiEet al. Induction of eEF2-specific antitumor CTL responses in vivo by vaccination with eEF2-derived 9mer-peptides. Oncol. Rep.35(4), 1959–1966 (2016).
   PubMed Web of Science ®Google Scholar
• Ambrocio-Ortiz E , Perez-RubioG , Ramirez-VenegasAet al. Protective role of genetic variants in HSP90 genes-complex in COPD secondary to biomass-burning smoke exposure and non-severe COPD forms in tobacco smoking subjects. Curr. Issues Mol. Biol.43(2), 887–899 (2021).
   PubMed Web of Science ®Google Scholar
• Castruccio Castracani C , LonghitanoL , DistefanoAet al. Heme oxygenase-1 and carbon monoxide regulate growth and progression in glioblastoma cells. Mol. Neurobiol.57(5), 2436–2446 (2020).
   PubMed Web of Science ®Google Scholar
• Lai CQ , ParnellLD , OrdovasJM. The APOA1/C3/A4/A5 gene cluster, lipid metabolism and cardiovascular disease risk. Curr. Opin. Lipidol.16(2), 153–166 (2005).
   PubMed Web of Science ®Google Scholar
• Lee H , ChoiJY , JoungJG , JohJW , KimJM , HyunSH. Metabolism-associated gene signatures for FDG avidity on PET/CT and prognostic validation in hepatocellular carcinoma. Front. Oncol.12, 845900 (2022).
   PubMed Web of Science ®Google Scholar
• Barravecchia I , BarresiE , RussoCet al. Enriching the arsenal of pharmacological tools against MICAL2. Molecules26(24),7519 (2021).
   PubMed Web of Science ®Google Scholar
• He XQ , DongKZ , ShenJet al. Deficiency of the novel high mobility group protein HMGXB4 protects against systemic inflammation-induced endotoxemia in mice. Proc. Natl Acad. Sci. USA118(7),e2021862118 (2021).
   PubMed Web of Science ®Google Scholar
• Nikolaou N , GathercoleLL , MarchandLet al. AKR1D1 is a novel regulator of metabolic phenotype in human hepatocytes and is dysregulated in non-alcoholic fatty liver disease. Metabolism99, 67–80 (2019).
   PubMed Web of Science ®Google Scholar
• Karavia EA , PapachristouDJ , LiopetaK , TriantaphyllidouIE , DimitrakopoulosO , KypreosKE. Apolipoprotein A-I modulates processes associated with diet-induced nonalcoholic fatty liver disease in mice. Mol. Med.18, 901–912 (2012).
   PubMed Web of Science ®Google Scholar
• Chevre R , Trigueros-MotosL , CastanoDet al. Therapeutic modulation of the bile acid pool by Cyp8b1 knockdown protects against nonalcoholic fatty liver disease in mice. FASEB J.32(7), 3792–3802 (2018).
   PubMed Web of Science ®Google Scholar
• Chen LH , WuM , ZhangSNet al. Estrogen-related receptor gamma regulates hepatic triglyceride metabolism through phospholipase A2 G12B. FASEB J.33(7), 7942–7952 (2019).
   PubMed Web of Science ®Google Scholar
• Park D , KimE , LeeH , ShinEA , LeeH , LeeJW. Tetraspanin TM4SF5 in hepatocytes negatively modulates SLC27A transporters during acute fatty acid supply. Arch. Biochem. Biophys.710, 109004 (2021).
   PubMed Web of Science ®Google Scholar
• Chambers KF , DayPE , AboufarragHT , KroonPA. Polyphenol effects on cholesterol metabolism via bile acid biosynthesis, CYP7A1: a review. Nutrients11(11), 2588 (2019).
   PubMed Web of Science ®Google Scholar
• Lee HY , BirkenfeldAL , JornayvazFRet al. Apolipoprotein CIII overexpressing mice are predisposed to diet-induced hepatic steatosis and hepatic insulin resistance. Hepatology54(5), 1650–1660 (2011).
   PubMed Web of Science ®Google Scholar
• Govaere O , CockellS , TiniakosDet al. Transcriptomic profiling across the nonalcoholic fatty liver disease spectrum reveals gene signatures for steatohepatitis and fibrosis. Sci. Transl. Med.12(572), eaba4448 (2020).
   PubMed Web of Science ®Google Scholar
• Chen D , GaoX , WangJet al. Activation of hepatic iNKT2 cells by α-GalCer ameliorates hepatic steatosis induced by high-fat diet in C57BL/6J mice. Int. Immunopharmacol.74, 105727 (2019).
   PubMed Web of Science ®Google Scholar
• Hedjazifar S , KhatibShahidi R , HammarstedtAet al. The novel adipokine Gremlin 1 antagonizes insulin action and is increased in Type 2 diabetes and NAFLD/NASH. Diabetes69(3), 331–341 (2020).
   PubMed Web of Science ®Google Scholar
• Mackay DJG , CallawayJLA , MarksSMet al. Hypomethylation of multiple imprinted loci in individuals with transient neonatal diabetes is associated with mutations in ZFP57. Nat. Genet.40(8), 949–951 (2008).
   PubMed Web of Science ®Google Scholar
• Sheng X , WangM , LuM , XiB , ShengH , ZangYQ. Rhein ameliorates fatty liver disease through negative energy balance, hepatic lipogenic regulation, and immunomodulation in diet-induced obese mice. Am. J. Physiol. Endocrinol. Metab.300(5), e886–e893 (2011).
   PubMed Web of Science ®Google Scholar
• Swisa A , AvrahamiD , EdenNet al. PAX6 maintains β cell identity by repressing genes of alternative islet cell types. J. Clin. Invest.127(1), 230–243 (2017).
   PubMed Web of Science ®Google Scholar
• Zhang Y , GeX , LiYet al. TWIST2 and the PPAR signaling pathway are important in the progression of nonalcoholic steatohepatitis. Lipids Health Dis.20(1), 39 (2021).
   PubMed Web of Science ®Google Scholar
• Fraszczak J , MoroyT. The transcription factors GFI1 and GFI1B as modulators of the innate and acquired immune response. Adv. Immunol.149, 35–94 (2021).
   PubMed Web of Science ®Google Scholar
• Jia X , ZhaiT. Integrated analysis of multiple microarray studies to identify novel gene signatures in non-alcoholic fatty liver disease. Front. Endocrinol. (Lausanne)10, 599 (2019).
   PubMed Web of Science ®Google Scholar
• Liu QL , YangM , FuXKet al. Activation of farnesoid X receptor promotes triglycerides lowering by suppressing phospholipase A2 G12B expression. Mol. Cell. Endocrinol.436(C), 93–101 (2016).
   PubMed Web of Science ®Google Scholar
• Zhou W , MadridP , FluittA , StahlA , XieXS. Development and validation of a high-throughput screening assay for human long-chain fatty acid transport proteins 4 and 5. J. Biomol. Screen.15(5), 488–497 (2010).
   PubMedGoogle Scholar
• Li T , ChandaD , ZhangY , ChoiHS , ChiangJY. Glucose stimulates cholesterol 7alpha-hydroxylase gene transcription in human hepatocytes. J. Lipid Res.51(4), 832–842 (2010).
   PubMed Web of Science ®Google Scholar
• Stevanović J , BelezaJ , CoxitoP , AscensãoA , MagalhãesJ. Physical exercise and liver ‘fitness’: role of mitochondrial function and epigenetics-related mechanisms in non-alcoholic fatty liver disease. Mol. Metab.32, 1–142020).
   PubMed Web of Science ®Google Scholar