Linking metabolism and epigenetic regulation in development of hepatocellular carcinoma

Laboratory Investigation

Volumn 93, Issue 9, 2013, Pages 983-990

  Puszyk, William Matthew ^a   Trinh, Thu Le ^a   Chapple, Sarah J ^b   Liu, Chen ^a,c  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

DNA methylation; EMT; epigenetics; hepatocellular carcinoma; metabolism; micro RNA; TET family

Indexed keywords

BETA CATENIN; DNA; METHIONINE ADENOSYLTRANSFERASE; METHIONINE ADENOSYLTRANSFERASE 1A; MICRORNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; TUMOR MARKER; UNCLASSIFIED DRUG;

CANCER SURVIVAL; CARBON CYCLE; CPG ISLAND; DNA METHYLATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENE MUTATION; HUMAN; LIVER CELL CARCINOMA; METABOLISM; METASTASIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; REVIEW;

EID: 84883430481     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2013.94     Document Type: Review

References (80)

1. Cucchetti A, Piscaglia F, Cescon M, et al. Conditional survival after hepatic resection for hepatocellular carcinoma in cirrhotic patients. Clin Cancer Res 2012;18:4397-4405.
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012;62:10-29.
3. Villanueva A, Hoshida Y. Depicting the role of TP53 in hepatocellular carcinoma progression. J Hepatol 2011;55:724-725.
4. Yang B, Guo M, Herman JG, et al. Aberrant promoter methylation profiles of tumor suppressor genes in hepatocellular carcinoma. Am J Pathol 2003;163:1101-1107.
5. Lee S, Lee HJ, Kim JH, et al. Aberrant CpG island hypermethylation along multistep hepatocarcinogenesis. Am J Pathol 2003;163: 1371-1378.
6. Katoh H, Shibata T, Kokubu A, et al. Epigenetic instability and chromosomal instability in hepatocellular carcinoma. Am J Pathol 2006;168:1375-1384.
7. Zhang C, Guo X, Jiang G, et al. CpG island methylator phenotype association with upregulated telomerase activity in hepatocellular carcinoma. Int J Cancer 2008;123:998-1004.
8. Tischoff I, Markwarth A, Witzigmann H, et al. Allele loss and epigenetic inactivation of 3p21.3 in malignant liver tumors. Int J Cancer 2005;115:684-689.
9. Um TH, Kim H, Oh BK, et al. Aberrant CpG island hypermethylation in dysplastic nodules and early HCC of hepatitis B virus-related human multistep hepatocarcinogenesis. J Hepatol 2011;54:939-947.
10. Liu H, Dong H, Robertson K, et al. DNA methylation suppresses expression of the urea cycle enzyme carbamoyl phosphate synthetase 1 (CPS1) in human hepatocellular carcinoma. Am J Pathol 2011; 178:652-661.
11. Tomasi ML, Li TW, Li M, et al. Inhibition of human methionine adenosyltransferase 1A transcription by coding region methylation. J Cell Physiol 2012;227:1583-1591.
12. Maier K, Hofmann U, Reuss M, et al. Dynamics and control of the central carbon metabolism in hepatoma cells. BMC Syst Biol 2010;4:54.
13. Warburg O, Wind F, Neglers E. in: Metabolism of tumours. pp 254-270 (Constable & Co: London, UK, 1930).
14. Stubbs M, Griffiths JR. The altered metabolism of tumors: HIF-1 and its role in the Warburg effect. Adv Enzyme Regul 2010;50:44-55.
15. WARBURG O. On respiratory impairment in cancer cells. Science 1956;124:269-70.
16. Garber K. Energy boost: the Warburg effect returns in a new theory of cancer. J Natl Cancer Inst 2004;96:1805-1806.
17. Kaelin WG. Cancer and altered metabolism: potential importance of hypoxia-inducible factor and 2-oxoglutarate-dependent dioxygenases. Cold Spring Harb Symp Quant Biol 2011;76:335-345.
18. Cyr AR, Domann FE. The redox basis of epigenetic modifications: from mechanisms to functional consequences. Antioxid Redox Signal 2011;15:551-589.
19. Yeluri S, Madhok B, Prasad KR, et al. Cancer's craving for sugar: an opportunity for clinical exploitation. J Cancer Res Clin Oncol 2009;135:867-877.
20. Semenza GL. HIF-1 mediates the Warburg effect in clear cell renal carcinoma. J Bioenerg Biomembr 2007;39:231-234.
21. Shimazu T, Hirschey MD, Newman J, et al. Suppression of oxidative stress by b-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 2013;339:211-214.
22. Shyh-Chang N, Locasale JW, Lyssiotis CA, et al. Influence of threonine metabolism on S-adenosylmethionine and histone methylation. Science 2013;339:222-226.
23. Shanbhogue AK, Prasad SR, Takahashi N, et al. Recent advances in cytogenetics and molecular biology of adult hepatocellular tumors: implications for imaging and management. Radiology 2011;258: 673-693.
24. van Malenstein H, van Pelt J, Verslype C. Molecular classification of hepatocellular carcinoma anno 2011. Eur J Cancer 2011;47:1789-1797.
25. Herath NI, Leggett BA, MacDonald GA. Review of genetic and epigenetic alterations in hepatocarcinogenesis. J Gastroenterol Hepatol 2006;21(1 Pt 1):15-21.
26. Calvisi DF, Ladu S, Gorden A, et al. Mechanistic and prognostic significance of aberrant methylation in the molecular pathogenesis of human hepatocellular carcinoma. J Clin Invest 2007;117: 2713-2722.
27. Li B, Liu W, Wang L, et al. CpG island methylator phenotype associated with tumor recurrence in tumor-node-metastasis stage I hepatocellular carcinoma. Ann Surg Oncol 2010;17:1917-1926.
28. Wu LM, Zhang F, Zhou L, et al. Predictive value of CpG island methylator phenotype for tumor recurrence in hepatitis B virusassociated hepatocellular carcinoma following liver transplantation. BMC Cancer 2010;10:399.
29. Wei X, Xiang T, Ren G, et al. miR-101 is down-regulated by the hepatitis B virus x protein and induces aberrant DNA methylation by targeting DNA methyltransferase 3A. Cell Signal 2013;25:439-446.
30. Liu JB, Zhang YX, Zhou SH, et al. CpG island methylator phenotype in plasma is associated with hepatocellular carcinoma prognosis. World J Gastroenterol 2011;17:4718-4724.
31. Liu WJ, Wang L, Wang JP, et al. Correlations of CpG island methylator phenotype and OPCML gene methylation to carcinogenesis of hepatocellular carcinoma. Ai Zheng 2006;25:696-700.
32. Cheng Y, Zhang C, Zhao J, et al. Correlation of CpG island methylator phenotype with poor prognosis in hepatocellular carcinoma. Exp Mol Pathol 2010;88:112-117.
33. Imai S, Guarente L. Ten years of NAD-dependent SIR2 family deacetylases: implications for metabolic diseases. Trends Pharmacol Sci 2010;31:212-220.
34. Ding W, You H, Dang H, et al. Epithelial-to-mesenchymal transition of murine liver tumor cells promotes invasion. Hepatology 2010;52: 945-953.
35. van Zijl F, Mall S, Machat G, et al. A human model of epithelial to mesenchymal transition to monitor drug efficacy in hepatocellular carcinoma progression. Mol Cancer Ther 2011;10:850-860.
36. Ogunwobi OO, Liu C. Hepatocyte growth factor upregulation promotes carcinogenesis and epithelial-mesenchymal transition in hepatocellular carcinoma via Akt and COX-2 pathways. Clin Exp Metastasis 2011;28:721-731.
37. Zhu H, Dong H, Eksioglu E, et al. Hepatitis C virus triggers apoptosis of a newly developed hepatoma cell line through antiviral defense system. Gastroenterology 2007;133:1649-1659.
38. Tang ZY. Hepatocellular carcinoma-cause, treatment and metastasis. World J Gastroenterol 2001;7:445-454.
39. Gregory PA, Bert AG, Paterson EL, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008;10:593-601.
40. Gregory PA, Bracken CP, Smith E, et al. An autocrine TGF-beta/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol Biol Cell 2011;22:1686-1698.
41. Neves R, Scheel C, Weinhold S, et al. Role of DNA methylation in miR-200c/141 cluster silencing in invasive breast cancer cells. BMC Res Notes 2010;3:219.
42. Vrba L, Jensen TJ, Garbe JC, et al. Role for DNA methylation in the regulation of miR-200c and miR-141 expression in normal and cancer cells. PLoS ONE 2010;5:e8697.
43. Wiklund ED, Bramsen JB, Hulf T, et al. Coordinated epigenetic repression of the miR-200 family and miR-205 in invasive bladder cancer. Int J Cancer 2011;128:1327-1334.
44. John B, Sander C, Marks DS. Prediction of human microRNA targets. Methods Mol Biol 2006;342:101-113.
45. Schmeier S, Schaefer U, Essack M, et al. Network analysis of microRNAs and their regulation in human ovarian cancer. BMC Syst Biol 2011;5:183.
46. Budhu A, Jia HL, Forgues M, et al. Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology 2008;47:897-907.
47. Eades G, Yao Y, Yang M, et al. miR-200a regulates SIRT1 expression and epithelial to mesenchymal transition (EMT)-like transformation in mammary epithelial cells. J Biol Chem 2011;286:25992-26002.
48. Tellez CS, Juri DE, Do K, et al. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res 2011;71:3087-3097.
49. Ma K, He Y, Zhang H, et al. DNA methylation-regulated miR-193a-3p dictates resistance of hepatocellular carcinoma to 5-fluorouracil via repression of SRSF2 expression. J Biol Chem 2012;287:5639-5649.
50. Howe EN, Cochrane DR, Richer JK. Targets of miR-200c mediate suppression of cell motility and anoikis resistance. Breast Cancer Res 2011;13:R45.
51. Diaz G, Melis M, Tice A, et al. Identification of microRNAs specifically expressed in hepatitis C virus-associated hepatocellular carcinoma. Int J Cancer 2013;133:816-824.
52. Liu J, Liu W, Ying H, et al. Analysis of microRNA expression profile induced by AICAR in mouse hepatocytes. Gene 2013;512:364-372.
53. Mudd SH, Poole JR. Labile methyl balances for normal humans on various dietary regimens. Metabolism 1975;24:721-735.
54. Mart́nez-López N, Varela-Rey M, Ariz U, et al. S-adenosylmethionine and proliferation: new pathways, new targets. Biochem Soc Trans 2008;36(Pt 5):848-852.
55. Santamaŕa E, Muñoz J, Fernandez-Irigoyen J, et al. Molecular profiling of hepatocellular in human liver diseases. J Proteome Res 2006;5: 944-953.
56. Wang YC, Tang FY, Chen SY, et al. Glycine-N methyltransferase expression in HepG2 cells is involved in methyl group homeostasis by regulating transmethylation kinetics and DNA methylation. J Nutr 2011;141:777-782.
57. Teng YW, Mehedint MG, Garrow TA, et al. Deletion of betainehomocysteine S-methyltransferase in mice perturbs choline and 1-carbon metabolism, resulting in fatty liver and hepatocellular carcinomas. J Biol Chem 2011;286:36258-36267.
58. Avila MA, Berasain C, Torres L, et al. Reduced mRNA abundance of the main enzymes involved in methionine metabolism in human liver cirrhosis and hepatocellular carcinoma. J Hepatol 2000;33:907-914.
59. Fausto N. Growth factors in liver development, regeneration and carcinogenesis. Prog Growth Factor Res 1991;3:219-234.
60. Liu F, Schaphorst KL, Verin AD, et al. Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: potential role of glycogen synthase kinase-3beta. FASEB J 2002;16:950-962.
61. Simon LM, Robin ED, Theodore J. Differences in oxygen-dependent regulation of enzymes between tumor and normal cell systems in culture. J Cell Physiol 1981;108:393-400.
62. Kaelin WG. The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat Rev Cancer 2008;8:865-873.
63. Robey IF, Lien AD, Welsh SJ, et al. Hypoxia-inducible factor-1alpha and the glycolytic phenotype in tumors. Neoplasia 2005;7:324-330.
64. Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009;324:929-930.
65. Tahiliani M, Koh KP, Shen Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009;324:930-935.
66. Ito S, D'Alessio AC, Taranova OV, et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010;466:1129-1133.
67. Hershey AD, Dixon J, Chase M. Nucleic acid economy in bacteria infected with bacteriophage T2. I. Purine and pyrimidine composition. J Gen Physiol 1953;36:777-789.
68. Booth MJ, Branco MR, Ficz G, et al. Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 2012;336:934-937.
69. Xu Y, Wu F, Tan L, et al. Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 2011;42:451-464.
70. Wu H, Zhang Y. Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev 2011;25:2436-2452.
71. Jin SG, Kadam S, Pfeifer GP. Examination of the specificity of DNA methylation profiling techniques towards 5-methylcytosine and 5-hydroxymethylcytosine. Nucleic Acids Res 2010;38:e125.
72. Jin SG, Wu X, Li AX, et al. Genomic mapping of 5-hydroxymethylcytosine in the human brain. Nucleic Acids Res 2011;39:5015-5024.
73. Kudo Y, Tateishi K, Yamamoto K, et al. Loss of 5-hydroxymethylcytosine is accompanied with malignant cellular transformation. Cancer Sci 2012;103:670-676.
74. Yang H, Liu Y, Bai F, et al. Tumor development is associated with decrease of TET gene expression and 5-methylcytosine hydroxylation. Oncogene 2013;32:663-669.
75. Yang H, Magilnick N, Noureddin M, et al. Effect of hepatocyte growth factor on methionine adenosyltransferase genes and growth is cell density-dependent in HepG2 cells. J Cell Physiol 2007;210:766-773.
76. Stroud H, Feng S, Morey Kinney S, et al. 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells. Genome Biol 2011;12:R54.
77. Williams K, Christensen J, Pedersen MT, et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 2011;473:343-348.
78. Shen YC, Ou DL, Hsu C, et al. Activating oxidative phosphorylation by a pyruvate dehydrogenase kinase inhibitor overcomes sorafenib resistance of hepatocellular carcinoma. Br J Cancer 2013;108: 72-81.
79. Calcutt NA, Lopez VL, Bautista AD, et al. Peripheral neuropathy in rats exposed to dichloroacetate. J Neuropathol Exp Neurol 2009;68: 985-993.
80. MacKenzie ED, Selak MA, Tennant DA, et al. Cell-permeating alphaketoglutarate derivatives alleviate pseudohypoxia in succinate dehydrogenase-deficient cells. Mol Cell Biol 2007;27:3282-3289.