Hepatitis B virus X protein promotes P3 transcript expression of the insulin-like growth factor 2 gene via inducing hypomethylation of P3 promoter in hepatocellular carcinoma

Liver International

Volumn 35, Issue 2, 2015, Pages 608-619

  Tang, Shaohui ^a   Hu, Wei ^b   Hu, Jianjun ^a   Wu, Shenglan ^a   Li, Junfeng ^a   Luo, Yuhong ^a   Cao, Mingrong ^a   Zhou, Hongke ^a   Jiang, Xiangwu ^a  

^a JINAN UNIVERSITY   (China)

^b WUHAN UNIVERSITY   (China)

Author keywords

Hepatitis B virus X protein; Hepatocellular carcinoma; Hypomethylation; Insulin like growth factor 2; Promoters

Indexed keywords

HEPATITIS B VIRUS X PROTEIN; MESSENGER RNA; SOMATOMEDIN B; IGF2 PROTEIN, HUMAN; LUCIFERASE; TRANSACTIVATOR PROTEIN;

ADULT; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CONTROLLED STUDY; CPG ISLAND; DISEASE FREE SURVIVAL; DNA METHYLATION; EPIGENETICS; FEMALE; FOLLOW UP; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CANCER CELL LINE; LIVER CELL CARCINOMA; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; P3 PROMOTER; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STABLE EXPRESSION; TRANSIENT EXPRESSION; TUMOR DIFFERENTIATION; UPREGULATION; WESTERN BLOTTING; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; HEPG2 CELL LINE; LIVER TUMOR; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; HEP G2 CELLS; HUMANS; INSULIN-LIKE GROWTH FACTOR II; LIVER NEOPLASMS; LUCIFERASES; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; TRANS-ACTIVATORS;

EID: 84921538205     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/liv.12469     Document Type: Article

References (55)

1. Kew MC. Epidemiology of hepatitis B virus infection, hepatocellular carcinoma, and hepatitis B virus-induced hepatocellular carcinoma. Pathol Biol 2010; 58: 273-7.
2. Henkler FF, Koshy R. Hepatitis B virus transcriptional activators: mechanisms and possible role in oncogenesis. J Viral Hepat 1996; 3: 109-21.
3. Ng SA, Lee C. Hepatitis B virus X gene and hepatocarcinogenesis. J Gastroenterol 2011; 46: 974-90.
4. Constância M, Hemberger M, Hughes J, et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 2002; 417: 945-8.
5. Humbel RE. Insulin-like growth factors I and II. Eur J Biochem 1990; 190: 445-62.
6. de Pagter-Holthuizen P, Jansen M, van Schaik FM, et al. The human insulin-like growth factor II contains two development-specific promoters. FEBS Lett 1987; 214: 259-64.
7. de Pagter-Holthuizen P, Jansen M, Van der Kammen RA, Van Schaik FMA, Sussenbach JS. Differential expression of the human insulin-like growth factor II gene. Characterization of the IGF-II mRNAs and an mRNA encoding a putative IGF-II-associated protein. Biochim Biophys Acta 1988; 950: 282-95.
8. Holthuizen P, Van der Lee FM, Ikejiri K, Yamamoto M, Sussenbach JS. Identification and initial characterization of a fourth leader exon and promoter of the human IGF-II gene. Biochim Biophys Acta 1990; 1087: 341-3.
9. Li X, Cui H, Sandstedt B, et al. Expression levels of the insulin-like growth factor-II gene (IGF2) in the human liver: developmental relationships of the four promoters. J Endocrinol 1996; 149: 117-24.
10. Li X, Nong Z, Ekström C, et al. Disrupted IGF2 promoter control by silencing of promoter P1 in human hepatocellular carcinoma. Cancer Res 1997; 57: 2048-54.
11. Chao W, D'Amore PA. IGF2: epigenetic regulation and role in development and disease. Cytokine Growth Factor Rev 2008; 19: 111-20.
12. Kalla Singh S, Tan QW, Brito C, et al. Differential insulin-like growth factor II (IGF-II) expression: a potential role for breast cancer survival disparity. Growth Horm IGF Res 2010; 20: 162-70.
13. Zuo QS, Yan R, Feng DX, et al. Loss of imprinting and abnormal expression of the insulin-like growth factor 2 gene in gastric cancer. Mol Carcinog 2011; 50: 390-6.
14. Lu L, Katsaros D, Wiley A, et al. Promoter-specific transcription of insulin-like growth factor-II in epithelial ovarian cancer. Gynecol Oncol 2006; 103: 990-5.
15. Sohda T, Yun K, Iwata K, Soejima H, Okumura M. Increased expression of insulin-like growth factor 2 in hepatocellular carcinoma is primarily regulated at the transcriptional level. Lab Invest 1996; 75: 307-11.
16. Breuhahn K, Schirmacher P. Reactivation of the insulin-like growth factor-II signaling pathway in human hepatocellular carcinoma. World J Gastroenterol 2008; 14: 1690-8.
17. Rogler CE, Yang D, Rossetti L, et al. Altered body composition and increased frequency of diverse malignancies in insulinlike growth factor-II transgenic mice. J Biol Chem 1994; 269: 13779-84.
18. Lin SB, Hsieh SH, Hsu HL, et al. Antisense oligodeoxynucleotides of IGF-II selectively inhibit growth of human hepatoma cells overproducing IGF-II. J Biochem 1997; 122: 717-22.
19. Ng IO, Lee JM, Srivastava G, Ng M. Expression of insulin-like growth factor II mRNA in hepatocellular carcinoma. J Gastroenterol Hepatol 1998; 13: 152-7.
20. Uchida K, Kondo M, Takeda S, et al. Altered transcriptional regulation of the insulin-like growth factor 2 gene in human hepatocellular carcinoma. Mol Carcinog 1997; 18: 193-8.
21. Tang SH, Yang DH, Huang W, et al. Differential promoter usage for insulin-like growth factor-II gene in Chinese hepatocellular carcinoma with hepatitis B virus infection. Cancer Detect Prev 2006; 30: 192-203.
22. Park BC, Huh MH, Seo JH. Differential expression of transforming growth factor α and insulin-like growth factor II in chronic active hepatitis B, cirrhosis and hepatocellular carcinoma. J Hepatol 1995; 22: 286-94.
23. Su Q, Liu YF, Zhang JF, et al. Expression of insulin-like growth factor II in hepatitis B, cirrhosis and hepatocellular carcinoma: its relationship with hepatitis B virus antigen expression. Hepatology 1994; 20: 788-99.
24. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science 2001; 293: 1068-70.
25. Jones PA. Epigenetics in carcinogenesis and cancer prevention. Ann N Y Acad Sci 2003; 983: 213-9.
26. Feninberg A. Cancer epigenetics takes center stage. Proc Natl Acad Sci U S A 2001; 98: 392-4.
27. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-8.
28. Liao B, Hu Y, Herrick DJ, Brewer G. The RNA-binding protein IMP-3 is a translational activator of insulin-like growth factor II leader-3 mRNA during proliferation of human K562 leukemia cells. J Biol Chem 2005; 280: 18517-24.
29. Zhu YZ, Zhu R, Shi LG, et al. Hepatitis B virus X protein promotes hypermethylation of p16INK4A promoter through upregulation of DNA methyltransferases in hepatocarcinogenesis. Exp Mol Pathol 2010; 89: 268-75.
30. Detich N, Bovenzi V, Szyf M. Valproate induces replication-independent active DNA demethylation. J Biol Chem 2003; 278: 27586-92.
31. Jiang J, Wei Y, Shen J, et al. Functional interaction of E1AF and Sp1 in glioma invasion. Mol Cell Biol 2007; 27: 8770-82.
32. Pei R, Calame K. Differential stability of c-myc mRNAS in a cell-free system. Mol Cell Biol 1988; 8: 2860-8.
33. Qiu LW, Yao DF, Zong L, et al. Abnormal expression of insulin-like growth factor-II and its dynamic quantitative analysis at different stages of hepatocellular carcinoma development. Hepatobiliary Pancreat Dis Int 2008; 7: 406-11.
34. Nussbaum T, Samarin J, Ehemann V, et al. Autocrine insulin-like growth factor-II stimulation of tumor cell migration is a progression step in human hepatocarcinogenesis. Hepatology 2008; 48: 146-56.
35. Dransfield DT, Cohen EH, Chang Q, et al. A human monoclonal antibody against insulin-like growth factor-II blocks the growth of human hepatocellular carcinoma cell lines in vitro and in vivo. Mol Cancer Ther 2010; 9: 1809-19.
36. Tang SH, Yang DH, Huang W, et al. Hypomethylated P4 promoter induces expression of the insulin-like growth factor-II gene in hepatocellular carcinoma in a Chinese population. Clin Cancer Res 2006; 12: 4171-7.
37. Tian Y, Hu Y, Wang Z, et al. Hepatitis B virus regulates Raf1 expression in HepG2.2.15 cells by enhancing its promoter activity. Arch Virol 2011; 156: 869-74.
38. Kong GY, Zhang JP, Zhang S, et al. Hepatitis B virus X protein promotes hepatoma cell proliferation via upregulation of MEKK2. Acta Pharmacol Sin 2011; 32: 1173-80.
39. Shi XY, Zhang YY, Zhou XW, et al. Hepatitis B virus X protein regulates the mEZH2 promoter via the E2F1-binding site in AML12 cells. Chin J Cancer 2011; 30: 273-9.
40. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002; 18: 1427-31.
41. Tusnády GE, Simon I, Váradi A, Arányi T. BiSearch: primer-design and search tool for PCR on bisulfite-treated genomes. Nucleic Acids Res 2005; 33: e9.
42. Patterson K, Molloy L, Qu W, Clark S. DNA methylation: bisulphite modification and analysis. J Vis Exp 2011; pii: 3170.
43. Lee JO, Kwun HJ, Jung JK, et al. Hepatitis B virus X protein represses E-cadherin expression via activation of DNA methyltransferase 1. Oncogene 2005; 24: 6617-25.
44. Park IY, Sohn BH, Yu E, et al. Aberrant epigenetic modifications in hepatocarcinogenesis induced by hepatitis B virus X protein. Gastroenterology 2007; 132: 1476-94.
45. Zhu YZ, Zhu R, Fan J, et al. Hepatitis B virus X protein induces hypermethylation of p16(INK4A) promoter via DNA methyltransferases in the early stage of HBV-associated hepatocarcinogenesis. J Viral Hepat 2010; 17: 98-107.
46. Yan J, Lu Q, Dong J, et al. Hepatitis B virus X protein suppresses caveolin-1 expression in hepatocellular carcinoma by regulating DNA methylation. BMC Cancer 2012; 12: 353.
47. Tong A, Gou L, Lau QC, et al. Proteomic profiling identifies aberrant epigenetic modifications induced by hepatitis B virus X protein. J Proteome Res 2009; 8: 1037-46.
48. Zheng DL, Zhang L, Cheng N, et al. Epigenetic modification induced by hepatitis B virus X protein via interaction with de novo DNA methyltransferase DNMT3A. J Hepatol 2009; 50: 377-87.
49. Ding R, Han S, Lu Y, et al. Overexpressed Id-1 is associated with patient prognosis and HBx expression in hepatitis B virus-related hepatocellular carcinoma. Cancer Biol Ther 2010; 10: 299-307.
50. Xia L, Huang W, Tian D, et al. Upregulated FoxM1 expression induced by hepatitis B virus X protein promotes tumor metastasis and indicates poor prognosis in hepatitis B virus-related hepatocellular carcinoma. J Hepatol 2012; 57: 600-12.
51. Ou DP, Tao YM, Tang FQ, Yang LY. The hepatitis B virus X protein promotes hepatocellular carcinoma metastasis by upregulation of matrix metalloproteinases. Int J Cancer 2007; 120: 1208-14.
52. Lewis BC, Klimstra DS, Socci ND, et al. The absence of p53 promotes metastasis in a novel somatic mouse model for hepatocellular carcinoma. Mol Cell Biol 2005; 25: 1228-37.
53. Chen YW, Boyartchuk V, Lewis BC. Differential roles of insulin-like growth factor receptor- and insulin receptor-mediated signaling in the phenotypes of hepatocellular carcinoma cells. Neoplasia 2009; 11: 835-45.
54. Dong ZZ, Yao DF, Yao DB, et al. Expression and alteration of insulin-like growth factor II - messenger RNA in hepatoma tissues and peripheral blood of patients with hepatocellular carcinoma. World J Gastroenterol 2005; 11: 4655-60.
55. Bège T, Le Treut YP, Hardwigsen J, et al. Prognostic factors after resection for hepatocellular carcinoma in nonfibrotic or moderately fibrotic liver. Gastrointest Surg 2007; 11: 619-25.