Epigenetic modification induced by hepatitis B virus X protein via interaction with de novo DNA methyltransferase DNMT3A

Journal of Hepatology

Volumn 50, Issue 2, 2009, Pages 377-387

  Zheng, Da Li ^a,b   Zhang, Li ^b   Cheng, Na ^a,b   Xu, Xiao ^a,b   Deng, Qing ^a,b   Teng, Xiao Mei ^a,b   Wang, Ke Sheng ^b   Zhang, Xin ^b   Huang, Jian ^b   Han, Ze Guang ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b CHINESE NATIONAL HUMAN GENOME CENTER AT SHANGHAI   (China)

Author keywords

DNMT3A; Epigenetic modification; Hepatitis B virus X protein; Hepatocellular carcinoma

Indexed keywords

CDH6 PROTEIN; DNA METHYLTRANSFERASE 3A; HEPATITIS B VIRUS X PROTEIN; HISTONE DEACETYLASE 1; INTERLEUKIN 4 RECEPTOR; METALLOTHIONEIN I; PROTEIN; SOMATOMEDIN BINDING PROTEIN 3; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; DNA MODIFICATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIVER CELL CARCINOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY SEQUENCE;

CARCINOMA, HEPATOCELLULAR; CELL LINE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HEPATITIS B; HISTONE DEACETYLASES; HUMANS; LIVER NEOPLASMS; PROMOTER REGIONS, GENETIC; TRANS-ACTIVATORS;

EID: 58149310908     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2008.10.019     Document Type: Article

References (46)

1. Lok A.S., Heathcote E.J., and Hoofnagle J.H. Management of hepatitis B:2000-summary of a workshop. Gastroenterology 120 (2001) 1828-1853
2. Murakami S. Hepatitis B virus X protein: a multifunctional viral regulator. J Gastroenterol 36 (2001) 651-660
3. Chen H.S., Kaneko S., Girones R., Anderson R.W., Hornbuckle W.E., Tennant B.C., et al. The woodchuck hepatitis virus X gene is important for establishment of virus infection in woodchucks. J Virol 67 (1993) 1218-1226
4. Bouchard M.J., Wang L.H., and Schneider R.J. Calcium signaling by HBx protein in hepatitis B virus DNA replication. Science 294 (2001) 2376-2378
5. Kim C.M., Koike K., Saito I., Miyamura T., and Jay G. HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature 351 (1991) 317-320
6. Wang Y., Cui F., Lv Y., Li C., Xu X., Deng C., et al. HBsAg and HBx knocked into the p21 locus causes hepatocellular carcinoma in mice. Hepatology 39 (2004) 318-324
7. Bouchard M.J., and Schneider R.J. The enigmatic X gene of hepatitis B virus. J Virol 78 (2004) 12725-12734
8. Rui E., Moura P.R., Gonçalves K.A., Rooney R.J., and Kobarg J. Interaction of the hepatitis B virus protein HBx with the human transcription regulatory protein p120E4F in vitro. Virus Res 115 (2006) 31-42
9. Kim S., Park S.Y., Yong H., Famulski J.K., Chae S., Lee J.H., et al. HBV X protein targets hBubR1, which induces dysregulation of the mitotic checkpoint. Oncogene 27 (2008) 3457-3464
10. Lee A.T., Ren J., Wong E.T., Ban K.H., Lee L.A., and Lee C.G. The hepatitis B virus X protein sensitizes HepG2 cells to UV light-induced DNA damage. J Biol Chem 280 (2005) 33525-33535
11. Bouchard M.J., Wang L., and Schneider R.J. Activation of focal adhesion kinase by hepatitis B virus HBx protein: multiple functions in viral replication. J Virol 80 (2006) 4406-4414
12. Sidorkiewicz M., Jais J.P., Tralhao G., Morosan S., Giannini C., Brezillon N., et al. Gene modulation associated with inhibition of liver regeneration in hepatitis B virus X transgenic mice. World J Gastroenterol 14 (2008) 574-581
13. Hu Z., Zhang Z., Kim J.W., Huang Y., and Liang T.J. Altered proteolysis and global gene expression in hepatitis B virus X transgenic mouse liver. J Virol 80 (2006) 1405-1413
14. Ng R.K., Lau C.Y., Lee S.M., Tsui S.K., Fung K.P., and Waye M.M. cDNA microarray analysis of early gene expression profiles associated with hepatitis B virus X protein-mediated hepatocarcinogenesis. Biochem Biophys Res Commun 322 (2004) 827-835
15. Shim Y.H., Yoon G.S., Choi H.J., Chung Y.H., and Yu E. p16 hypermethylation in the early stage of hepatitis B virus associated hepatocarcinogenesis. Cancer Lett 190 (2003) 213-219
16. Zhong S., Tang M.W., Yeo W., Liu C., Lo Y.M., and Johnson P.J. Silencing of GSTP1 gene by CpG island DNA hypermethylation in HBV-associated hepatocellular carcinomas. Clin Cancer Res 8 (2002) 1087-1092
17. Chen T., and Li E. Structure and function of eukaryotic DNA methyltransferases. Curr Top Dev Biol 60 (2004) 55-89
18. Lee J.O., Kwun H.J., Jung J.K., Choi K.H., Min D.S., and Jang K.L. Hepatitis B virus X protein represses E-cadherin expression via activation of DNA methyltransferase 1. Oncogene 24 (2005) 6617-6625
19. Jung J.K., Arora P., Pagano J.S., and Jang K.L. Expression of DNA methyltransferase 1 is activated by hepatitis B virus X protein via a regulatory circuit involving the p16INK4a-cyclin D1-CDK 4/6-pRb-E2F1 pathway. Cancer Res 67 (2007) 5771-5778
20. Park I.Y., Sohn B.H., Yu E., Suh D.J., Chung Y.H., Lee J.H., et al. Aberrant epigenetic modifications in hepatocarcinogenesis induced by hepatitis B virus X protein. Gastroenterology 132 (2007) 1476-1494
21. Lin X., Yuan Z.H., Wu L., Ding J.P., and Wen Y.M. A single amino acid in the reverse transcriptase domain of hepatitis B virus affects virus replication efficiency. J Virol 75 (2001) 11827-11833
22. Lin X., Xu X., Huang Q.L., Liu Y.Q., Zheng D.L., Chen W.N., et al. Biological impacts of "hot-spot" mutations of hepatitis B virus X proteins are genotype B and C differentiated. World J Gastroenterol 11 (2005) 4703-4708
23. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402-408
24. Metzger E., Wissmann M., Yin N., Müller J.M., Schneider R., Peters A.H., et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437 (2005) 436-439
25. Herman J.G., Graff J.R., Myöhänen S., Nelkin B.D., and Baylin S.B. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 93 (1996) 9821-9826
26. Han J., Ding L., Yuan B., Yang X., Wang X., Li J., et al. Hepatitis B virus X protein and the estrogen receptor variant lacking exon 5 inhibit estrogen receptor signaling in hepatoma cells. Nucleic Acids Res 34 (2006) 3095-3106
27. Warnecke P.M., and Bestor T.H. Cytosine methylation and human cancer. Curr Opin Oncol 12 (2000) 68-73
28. Goelz S.E., Vogelstein B., Hamilton S.R., and Feinberg A.P. Hypomethylation of DNA from benign and malignant human colon neoplasms. Science 22 (1985) 187-190
29. Santourlidis S., Florl A., Ackermann R., Wirtz H.C., and Schulz W.A. High frequency of alterations in DNA methylation in adenocarcinoma of the prostate. Prostate 39 (1999) 166-174
30. Chilukamarri L., Hancock A.L., Malik S., Zabkiewicz J., Baker J.A., Greenhough A., et al. Hypomethylation and aberrant expression of the glioma pathogenesis-related 1 gene in Wilms tumors. Neoplasia 9 (2007) 970-978
31. Smith I.M., Mydlarz W.K., Mithani S.K., and Califano J.A. DNA global hypomethylation in squamous cell head and neck cancer associated with smoking, alcohol consumption and stage. Int J Cancer 121 (2007) 1724-1728
32. Lin C.H., Hsieh S.Y., Sheen I.S., Lee W.C., Chen T.C., Shyu W.C., et al. Genome-wide hypomethylation in hepatocellular carcinogenesis. Cancer Res 61 (2001) 4238-4243
33. Li H.P., Leu Y.W., and Chang Y.S. Epigenetic changes in virus-associated human cancers. Cell Res 15 (2005) 262-271
34. Slack A., Cervoni N., Pinard M., and Szyf M. DNA methyltransferase is a downstream effector of cellular transformation triggered by simian virus 40 large T antigen. J Biol Chem 274 (1999) 10105-10112
35. Soejima K., Fang W., and Rollins B.J. DNA methyltransferase 3b contributes to oncogenic transformation induced by SV40T antigen and activated Ras. Oncogene 22 (2003) 4723-4733
36. Tsai C.N., Tsai C.L., Tse K.P., Chang H.Y., and Chang Y.S. The Epstein-Barr virus oncogene product, latent membrane protein 1, induces the down-regulation of E-cadherin gene expression via activation of DNA methyltransferases. Proc Natl Acad Sci USA 99 (2002) 10084-10089
37. Shamay M., Krithivas A., Zhang J., and Hayward S.D. Recruitment of the de novo DNA methyltransferase Dnmt3a by Kaposi's sarcoma-associated herpesvirus LANA. Proc Natl Acad Sci USA 103 (2006) 14554-14559
38. Courtade M., Carrera G., Paternain J.L., Martel S., Carre P.C., Folch J., et al. Metallothionein expression in human lung and its varying levels after lung transplantation. Toulouse Lung Transplantation Group. Chest 113 (1998) 371-378
39. Lu D.D., Chen Y.C., Zhang X.R., Cao X.R., Jiang H.Y., and Yao L. The relationship between metallothionein-1F (MT1F) gene and hepatocellular carcinoma. Yale J Biol Med 76 (2003) 55-62
40. Nelms K., Keegan A.D., Zamorano J., Ryan J.J., and Paul W.E. The IL-4 receptor: signaling mechanisms and biologic functions. Annu Rev Immunol 17 (1999) 701-738
41. Aoudjehane L., Podevin P., Scatton O., Jaffray P., Dusanter-Fourt I., Feldmann G., et al. Interleukin-4 induces human hepatocyte apoptosis through a Fas-independent pathway. FASEB J 21 (2007) 1433-1444
42. Shimoyama Y., Gotoh M., Terasaki T., Kitajima M., and Hirohashi S. Isolation and sequence analysis of human cadherin-6 complementary DNA for the full coding sequence and its expression in human carcinoma cells. Cancer Res 55 (1995) 2206-2211
43. Shimazui T., Yoshikawa K., Uemura H., Hirao Y., Saga S., and Akaza H. The level of cadherin-6 mRNA in peripheral blood is associated with the site of metastasis and with the subsequent occurrence of metastases in renal cell carcinoma. Cancer 101 (2004) 963-968
44. Calvisi D.F., Ladu S., Gorden A., Farina M., Lee J.S., Conner E.A., et al. Mechanistic and prognostic significance of aberrant methylation in the molecular pathogenesis of human hepatocellular carcinoma. J Clin Invest 117 (2007) 2713-2722
45. Aishima S., Basaki Y., Oda Y., Kuroda Y., Nishihara Y., Taguchi K., et al. High expression of insulin-like growth factor binding protein-3 is correlated with lower portal invasion and better prognosis in human hepatocellular carcinoma. Cancer Sci 97 (2006) 1182-1190
46. Lee S., Tarn C., Wang W.H., Chen S., Hullinger R.L., and Andrisani O.M. Hepatitis B virus X protein differentially regulates cell cycle progression in X-transforming versus nontransforming hepatocyte (AML12) cell lines. J Biol Chem 277 (2002) 8730-8740