Epigenetic repression of E-cadherin expression by hepatitis B virus x antigen in liver cancer

Oncogene. 2012 Feb 2;31(5):563-72. doi: 10.1038/onc.2011.255. Epub 2011 Jun 27.

Abstract

Loss of E-cadherin is associated with acquisition of metastatic capacity. Numerous studies suggest that histone deacetylation and/or hypermethylation of CpG islands in E-cadherin gene (CDH1) are major mechanisms responsible for E-cadherin silencing in different tumors and cancer cell lines. The hepatitis B virus (HBV)-encoded X antigen, HBx, contributes importantly to the development of hepatocellular carcinoma using multiple mechanisms. Experiments were designed to test if in addition to CDH1 hypermethylation HBx promotes epigenetic modulation of E-cadherin transcriptional activity through histone deacetylation and miR-373. The relationships between HBx, E-cadherin, mSin3A, Snail-1 and miR-373 were evaluated in HBx expressing (HepG2X) and control (HepG2CAT) cells by western blotting, immunoprecipitation (IP), chromatin IP as well as by immunohistochemical staining of liver and tumor tissue sections from HBV-infected patients. In HepG2X cells, decreased levels of E-cadherin and elevated levels of mSin3A and Snail-1 were detected. Reciprocal IP with anti-HBx and anti-mSin3A demonstrated mutual binding. Furthermore, HBx-mSin3A colocalization was detected by immunofluorescent staining. HBx downregulated E-cadherin expression by the recruitment of the mSin3A/histone deacetylase complex to the Snail-binding sites in human CDH1. Histone deacetylation inhibition by Trichostatin-A treatment restored E-cadherin expression. Mir-373, a positive regulator of E-cadherin expression, was downregulated by HBx in HepG2X cells and tissue sections from HBV-infected patients. Thus, histone deacetylation of CDH1 and downregulation of miR-373, together with the previously demonstrated hypermethylation of CDH1 by HBx, may be important for the understanding of HBV-related carcinogenesis.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • Aged
  • Blotting, Western
  • Cadherins / genetics*
  • Cadherins / metabolism
  • Cells, Cultured
  • Chromatin Immunoprecipitation
  • DNA Methylation*
  • Female
  • Gene Expression Regulation, Neoplastic
  • Hep G2 Cells
  • Hepatocytes / cytology
  • Hepatocytes / metabolism
  • Humans
  • Liver / metabolism
  • Liver / pathology
  • Liver Neoplasms / genetics*
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Male
  • MicroRNAs / genetics
  • Middle Aged
  • Promoter Regions, Genetic / genetics
  • Protein Binding
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sin3 Histone Deacetylase and Corepressor Complex
  • Snail Family Transcription Factors
  • Trans-Activators / genetics*
  • Trans-Activators / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Viral Regulatory and Accessory Proteins

Substances

  • Cadherins
  • MIRN370 microRNA, human
  • MicroRNAs
  • Repressor Proteins
  • SIN3A transcription factor
  • SNAI1 protein, human
  • Snail Family Transcription Factors
  • Trans-Activators
  • Transcription Factors
  • Viral Regulatory and Accessory Proteins
  • hepatitis B virus X protein
  • Sin3 Histone Deacetylase and Corepressor Complex