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Research Paper

Epigenetic aberrations of gene expression in a rat model of hepatocellular carcinoma

, , , , , , , , , , , , ORCID Icon, , , , , & show all
Pages 1513-1534 | Received 02 Dec 2021, Accepted 14 Apr 2022, Published online: 03 May 2022

References

  • Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021;71(3):209–249.
  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65(1):5–29.
  • Singh S, Singh PP, Roberts LR, et al. Chemopreventive strategies in hepatocellular carcinoma. Nat Clin Pract Gastroenterol Hepatol. 2014;11(1):45–54.
  • Asada K, Kotake Y, Asada R, et al. LINE-1 hypomethylation in a choline-deficiency-induced liver cancer in rats: dependence on feeding period. J Biomed Biotechnol. 2006;2006:17142.
  • Park IY, Sohn BH, Yu E, et al. Aberrant epigenetic modifications in hepatocarcinogenesis induced by hepatitis B virus X protein. Gastroenterology. 2007;132(4):1476–1494.
  • Schafer DF, Sorrell MF. Hepatocellular carcinoma. Lancet. 1999;353(9160):1253–1257.
  • WCRF/AICR. Diet, Nutrition, Physical Activity and Liver Cancer. World cancer research fund international/American institute for cancer research 2015. World Cancer Research Fund International; 2015.
  • WCRF/AICR. Diet, Nutrition, Physical Activity and Cancer: a Global Perspective. Continuous update project report 2018; A summary of the third report.
  • Davila JA, Morgan RO, Shaib Y, et al. Diabetes increases the risk of hepatocellular carcinoma in the United States: a population based case control study. Gut. 2005;54(4):533–539.
  • Lu SC, Mato JM. Role of methionine adenosyltransferase and S-adenosylmethionine in alcohol-associated liver cancer. Alcohol. 2005;35(3):227–234.
  • Zapisek WF, Cronin GM, Lyn-Cook BD, et al. The onset of oncogene hypomethylation in the livers of rats fed methyl-deficient, amino acid-defined diets. Carcinogenesis. 1992;13(10):1869–1872.
  • Stefanska B, Huang J, Bhattacharyya B, et al. Definition of the landscape of promoter DNA hypomethylation in liver cancer. Cancer Res. 2011;71(17):5891–5903.
  • Stefanska B, Bouzelmat A, Huang J, et al. Discovery and validation of DNA hypomethylation biomarkers for liver cancer using HRM-specific probes. PloS one. 2013;8(8):e68439.
  • Stefanska B, Suderman M, Machnes Z, et al. Transcription onset of genes critical in liver carcinogenesis is epigenetically regulated by methylated DNA-binding protein MBD2. Carcinogenesis. 2013;34(12):2738–2749.
  • Pereira MA, Wang W, Kramer PM, et al. Prevention by methionine of dichloroacetic acid-induced liver cancer and DNA hypomethylation in mice. Toxicol Sci. 2004;77(2):243–248.
  • Rogers AE. Methyl donors in the diet and responses to chemical carcinogens. Am J Clin Nutr. 1995;61(3):659S–65S.
  • Toh TB, Lim JJ, Chow EK. Epigenetics of hepatocellular carcinoma. Clin Transl Med. 2019;8(1):13.
  • Jones PA, Ohtani H, Chakravarthy A, et al. Epigenetic therapy in immune-oncology. Nat Rev Cancer. 2019;19(3):151–161.
  • Beetch M, Harandi-Zadeh S, Shen K, et al. Dietary antioxidants remodel DNA methylation patterns in chronic disease. Br J Pharmacol. 2020;177(6):1382–1408.
  • Rasmussen KD, Helin K. Role of TET enzymes in DNA methylation, development, and cancer. Genes Dev. 2016;30(7):733–750.
  • Stefanska B, Cheishvili D, Suderman M, et al. Genome-wide study of hypomethylated and induced genes in liver cancer patients unravels novel anticancer targets. Clin Cancer Res off J Am Assoc Cancer Res. 2014;20(12):3118–3132.
  • Mayol G, Martin-Subero JI, Rios J, et al. DNA hypomethylation affects cancer-related biological functions and genes relevant in neuroblastoma pathogenesis. PloS one. 2012;7(11):e48401.
  • Cheishvili D, Boureau L, Szyf M. DNA demethylation and invasive cancer: implications for therapeutics. Br J Pharmacol. 2015;172(11):2705–2715.
  • Lubecka K, Flower K, Beetch M, et al. Loci-specific differences in blood DNA methylation in HBV-negative populations at risk for hepatocellular carcinoma development. Epigenetics. 2018;13(6):605–626.
  • Mansouri E, Khorsandi L, Abedi HA. Antioxidant effects of proanthocyanidin from grape seed on hepatic tissue injury in diabetic rats. Iran J Basic Med Sci. 2014;17(6):460–464.
  • Atasever A, Yaman D. The effects of grape seed and colchicine on carbon tetrachloride induced hepatic damage in rats. Exp Toxicol Pathol. 2014;66(8):361–365.
  • Charradi K, Elkahoui S, Karkouch I, et al. Protective effect of grape seed and skin extract against high-fat diet-induced liver steatosis and zinc depletion in rat. Dig Dis Sci. 2014;59(8):1768–1778.
  • Carter LG, D’Orazio JA, Pearson KJ. Resveratrol and cancer: focus on in vivo evidence. Endocr Relat Cancer. 2014;21(3):R209–25.
  • Lin HC, Chen YF, Hsu WH, et al. Resveratrol helps recovery from fatty liver and protects against hepatocellular carcinoma induced by hepatitis B virus X protein in a mouse model. Cancer Prev Res. 2012;5(7):952–962.
  • Rawat D, Chhonker SK, Naik RA, et al. Modulation of antioxidant enzymes, SIRT1 and NF-kappaB by resveratrol and nicotinamide in alcohol-aflatoxin B1-induced hepatocellular carcinoma. J Biochem Mol Toxicol. 2021;35(1):e22625.
  • Song Z, Zhou Z, Chen T, et al. S-adenosylmethionine (SAMe) protects against acute alcohol induced hepatotoxicity in mice. J Nutr Biochem. 2003;14(10):591–597.
  • Shen L, Fang J, Qiu D, et al. Correlation between DNA methylation and pathological changes in human hepatocellular carcinoma. Hepato-gastroenterology. 1998;45(23):1753–1759.
  • Mentch SJ, Mehrmohamadi M, Huang L, et al. Histone methylation dynamics and gene regulation occur through the sensing of one-carbon metabolism. Cell Metab. 2015;22(5):861–873.
  • De Cabo SF, Hazen MJ, Molero ML, et al. S-adenosyl-L-homocysteine: a non-cytotoxic hypomethylating agent. Experientia. 1994;50(7):658–659.
  • Li Z, Wang F, Liang B, et al. Methionine metabolism in chronic liver diseases: an update on molecular mechanism and therapeutic implication. Signal Transduct Target Ther. 2020;5(1):280.
  • Cheishvili D, Stefanska B, Yi C, et al. A common promoter hypomethylation signature in invasive breast, liver and prostate cancer cell lines reveals novel targets involved in cancer invasiveness. Oncotarget. 2015;6(32):33253–33268.
  • Nakae D, Yoshiji H, Mizumoto Y, et al. High incidence of hepatocellular carcinomas induced by a choline deficient L-amino acid defined diet in rats. Cancer Res. 1992;52(18):5042–5045.
  • Tsujiuchi T, Tsutsumi M, Sasaki Y, et al. Hypomethylation of CpG Sites and c-myc gene overexpression in hepatocellular carcinomas, but not hyperplastic nodules, induced by a choline-deficient L-amino acid-defined diet in rats. Jpn J Cancer Res: Gann. 1999;90(9):909–913.
  • Beetch M, Boycott C, Harandi-Zadeh S, et al. Pterostilbene leads to DNMT3B-mediated DNA methylation and silencing of OCT1-targeted oncogenes in breast cancer cells. J Nutr Biochem. 2021;98:108815.
  • Kim D, Pertea G, Trapnell C, et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14(4):R36.
  • Trapnell C, Roberts A, Goff L, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7(3):562–578.
  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550.
  • Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–140.
  • Song L, James SR, Kazim L, et al. Specific method for the determination of genomic DNA methylation by liquid chromatography-electrospray ionization tandem mass spectrometry. Anal Chem. 2005;77(2):504–510.
  • Lubecka K, Kurzava L, Flower K, et al. Stilbenoids remodel the DNA methylation patterns in breast cancer cells and inhibit oncogenic NOTCH signaling through epigenetic regulation of MAML2 transcriptional activity. Carcinogenesis. 2016;37(7):656–668.
  • Brown SE, Suderman MJ, Hallett M, et al. DNA demethylation induced by the methyl-CpG-binding domain protein MBD3. Gene. 2008;420(2):99–106.
  • Pogribny IP, Poirier LA, James SJ. Differential sensitivity to loss of cytosine methyl groups within the hepatic p53 gene of folate/methyl deficient rats. Carcinogenesis. 1995;16(11):2863–2867.
  • Alzahrani AM, Rajendran P. The multifarious link between Cytochrome P450s and cancer. Oxid Med Cell Longev. 2020;2020:3028387.
  • Wang X, He C, Hu X. LIM homeobox transcription factors, a novel subfamily which plays an important role in cancer (review). Oncol Rep. 2014;31(5):1975–1985.
  • Sherman BT, Huang da W, Tan Q, et al. DAVID Knowledgebase: a gene-centered database integrating heterogeneous gene annotation resources to facilitate high-throughput gene functional analysis. BMC Bioinformatics. 2007;8(1):426.
  • Rajas F, Dentin R, Cannella Miliano A, et al. The absence of hepatic glucose-6 phosphatase/ChREBP couple is incompatible with survival in mice. Mol Metab. 2021;43:101108.
  • Trepo E, Romeo S, Zucman-Rossi J, et al. PNPLA3 gene in liver diseases. J Hepatol. 2016;65(2):399–412.
  • Liu G, Hou G, Li L, et al. Potential diagnostic and prognostic marker dimethylglycine dehydrogenase (DMGDH) suppresses hepatocellular carcinoma metastasis in vitro and in vivo. Oncotarget. 2016;7(22):32607–32616.
  • Jin B, Gong Z, Yang N, et al. Downregulation of betaine homocysteine methyltransferase (BHMT) in hepatocellular carcinoma associates with poor prognosis. Tumour Biol. 2016;37(5):5911–5917.
  • Luka Z, Mudd SH, Wagner C. Glycine N-methyltransferase and regulation of S-adenosylmethionine levels. J Biol Chem. 2009;284(34):22507–22511.
  • Vitvitsky V, Thomas M, Ghorpade A, et al. A functional transsulfuration pathway in the brain links to glutathione homeostasis. J Biol Chem. 2006;281(47):35785–35793.
  • Krajka-Kuzniak V, Paluszczak J, Baer-Dubowska W. The Nrf2-ARE signaling pathway: an update on its regulation and possible role in cancer prevention and treatment. Pharmacol Rep. 2017;69(3):393–402.
  • Pitot HC, Hikita H, Dragan Y, et al. Review article: the stages of gastrointestinal carcinogenesis–application of rodent models to human disease. Aliment Pharmacol Ther. 2000;14 Suppl 1:153–160.
  • Bannasch P. Preneoplastic lesions as end points in carcinogenicity testing. I. Hepatic preneoplasia. Carcinogenesis. 1986;7(5):689–695.
  • Han Q, Wang X, Liao X, et al. Diagnostic and prognostic value of WNT family gene expression in hepatitis B virusrelated hepatocellular carcinoma. Oncol Rep. 2019;42(3):895–910.
  • Hu JW, Ding GY, Fu PY, et al. Identification of FOS as a candidate risk gene for liver cancer by integrated bioinformatic analysis. Biomed Res Int. 2020;2020:6784138.
  • Bedon L, Dal Bo M, Mossenta M, et al. A novel epigenetic machine learning model to define risk of progression for hepatocellular carcinoma patients. Int J Mol Sci. 2021;23(1):22.
  • Song ZB, Yu Y, Zhang GP, et al. Genomic instability of mutation-derived gene prognostic signatures for hepatocellular carcinoma. Front Cell Dev Biol. 2021;9:728574.
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674.
  • Gao H, Zhou X, Li H, et al. Role of matrix metallopeptidase 12 in the development of hepatocellular carcinoma. J Invest Surg. 2021 Apr; 34(4):366–372.
  • He M-K, Le Y, Zhang Y-F, et al. Matrix metalloproteinase 12 expression is associated with tumor FOXP3+ regulatory T cell infiltration and poor prognosis in hepatocellular carcinoma. Oncol Lett. 2018;16(1):475–482.
  • Xue TC, Zou JH, Chen RX, et al. Spatial localization of the JAG1/notch1/osteopontin cascade modulates extrahepatic metastasis in hepatocellular carcinoma. Int J Oncol. 2014;45(5):1883–1890.
  • Wang W, Smits R, Hao H, et al. Wnt/beta-catenin signaling in liver cancers. Cancers (Basel). 2019;11(7):926.
  • Sicklick JK, Li YX, Jayaraman A, et al. Dysregulation of the Hedgehog pathway in human hepatocarcinogenesis. Carcinogenesis. 2006;27(4):748–757.
  • Xuan Z, Zhao F, Wang J, et al. Genome-wide promoter extraction and analysis in human, mouse, and rat. Genome Biol. 2005;6(8):R72.
  • Zhang Y, Petropoulos S, Liu J, et al. The signature of liver cancer in immune cells DNA methylation. Clin Epigenetics. 2018;10(1):8.
  • Shirai K, Nagae G, Seki M, et al. TET1 upregulation drives cancer cell growth through aberrant enhancer hydroxymethylation of HMGA2 in hepatocellular carcinoma. Cancer Sci. 2021;112(7):2855–2869.
  • Pogribny IP, Ross SA, Wise C, et al. Irreversible global DNA hypomethylation as a key step in hepatocarcinogenesis induced by dietary methyl deficiency. Mutat Res. 2006;593(1–2):80–87.
  • Shimizu K, Onishi M, Sugata E, et al. Disturbance of DNA methylation patterns in the early phase of hepatocarcinogenesis induced by a choline-deficient L-amino acid-defined diet in rats. Cancer Sci. 2007;98(9):1318–1322.
  • Pogribny IP, Basnakian AG, Miller BJ, et al. Breaks in genomic DNA and within the p53 gene are associated with hypomethylation in livers of folate/methyl-deficient rats. Cancer Res. 1995;55(9):1894–1901.
  • Wang B, Majumder S, Nuovo G, et al. Role of microRNA-155 at early stages of hepatocarcinogenesis induced by choline-deficient and amino acid-defined diet in C57BL/6 mice. Hepatology. 2009;50(4):1152–1161.
  • Hebbard L, George J. Animal models of nonalcoholic fatty liver disease. Nat Clin Pract Gastroenterol Hepatol. 2011;8(1):35–44.
  • Wei G, An P, Vaid KA, et al. Comparison of murine steatohepatitis models identifies a dietary intervention with robust fibrosis, ductular reaction, and rapid progression to cirrhosis and cancer. Am J Physiol Gastrointest Liver Physiol. 2020;318(1):G174–G88.
  • Coller HA. Is cancer a metabolic disease? Am J Pathol. 2014;184(1):4–17.
  • Sharma U, Rando OJ. Metabolic Inputs into the Epigenome. Cell Metab. 2017;25(3):544–558.
  • Yin R, Mao SQ, Zhao B, et al. Ascorbic acid enhances Tet-mediated 5-methylcytosine oxidation and promotes DNA demethylation in mammals. J Am Chem Soc. 2013;135(28):10396–10403.
  • Peng D, Ge G, Gong Y, et al. Vitamin C increases 5-hydroxymethylcytosine level and inhibits the growth of bladder cancer. Clin Epigenetics. 2018;10(1):94.
  • Pascale RM, Feo CF, Calvisi DF, et al. Deregulation of methionine metabolism as determinant of progression and prognosis of hepatocellular carcinoma. Transl Gastroenterol Hepatol. 2018;3:36.
  • Liu W, Wu G, Xiong F, et al. Advances in the DNA methylation hydroxylase TET1. Biomark Res. 2021;9(1):76.
  • Good CR, Panjarian S, Kelly AD, et al. TET1-mediated hypomethylation activates oncogenic signaling in triple-negative breast cancer. Cancer Res. 2018;78(15):4–17.
  • Bao B, Teslow EA, Mitrea C, et al. Role of TET1 and 5hmC in an obesity-linked pathway driving cancer stem cells in triple-negative breast cancer. Mol Cancer Res. 2020;18(12):1803–1814.
  • Xie BY, Lv QY, Ning CC, et al. TET1-GPER-PI3K/AKT pathway is involved in insulin-driven endometrial cancer cell proliferation. Biochem Biophys Res Commun. 2017;482(4):857–862.