Histone deacetylase inhibitor suberoylanilide hydroxamic acid suppresses the pro-oncogenic effects induced by hepatitis B virus pre-S2 mutant oncoprotein and represents a potential chemopreventive agent in high-risk chronic HBV patients

Carcinogenesis. 2013 Feb;34(2):475-85. doi: 10.1093/carcin/bgs365. Epub 2012 Nov 21.

Abstract

Chronic hepatitis B virus (HBV) infection is the major cause of hepatocellular carcinoma (HCC). The pre-S(2) mutant large HBV surface antigen (LHBS) in type II ground glass hepatocytes (GGHs) has been recognized as an emerging viral oncoprotein; it directly interacts with the c-Jun activation domain-binding protein 1 (JAB1) and subsequently causes hyperphosphorylation of the tumor-suppressor retinoblastoma and, consequently, leads to disturbed cell cycle progression. The interaction of the pre-S(2) mutant LHBS with JAB1 could provide a potential target for chemoprevention. In this study, we found that the preneoplastic type II GGHs showed a significant decrease of the cyclin-dependent kinase inhibitor p27(Kip1), which serves as a marker for pre-S(2) mutant-JAB1 complex formation. The histone deacetylase (HDAC) inhibitor suberoylanilide hydroxamic acid (SAHA) elevated expression of the tumor-suppressor thioredoxin-binding protein 2 (TBP2), which subsequently enhanced the JAB1-TBP2 interaction and abolished the pre-S(2) mutant LHBS-induced degradation of p27(Kip1), which, in turn, recovered the normal cell cycle checkpoint. The pre-S(2) mutant LHBS-induced pro-oncogenic effects: increased cell proliferation, nuclear/cytoplasmic ratio and proliferating cell nuclear antigen expression, were all greatly ameliorated after SAHA treatments, which suggested SAHA as a promising chemopreventive agent for the pre-S(2) mutant oncoprotein-induced HCC. In conclusion, this study provides the mechanism of histone deacetylase (HDAC) inhibitor in preventing the pre-S(2) mutant-induced oncogenic phenotype. The HDAC inhibitor SAHA is therefore a potential chemopreventive agent for high-risk chronic HBV patients who may develop HCC.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Blotting, Western
  • COP9 Signalosome Complex
  • Carcinoma, Hepatocellular / etiology
  • Carcinoma, Hepatocellular / metabolism
  • Carcinoma, Hepatocellular / prevention & control*
  • Cell Cycle / drug effects
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Cell Proliferation / drug effects*
  • Cyclin-Dependent Kinase Inhibitor p27 / genetics
  • Cyclin-Dependent Kinase Inhibitor p27 / metabolism
  • Cytoplasm / drug effects
  • Cytoplasm / metabolism
  • Female
  • Fluorescent Antibody Technique
  • Hepatitis B Surface Antigens / genetics
  • Hepatitis B Surface Antigens / metabolism*
  • Hepatitis B virus / drug effects
  • Hepatitis B, Chronic / complications
  • Hepatitis B, Chronic / prevention & control*
  • Hepatitis B, Chronic / virology
  • Hepatocytes / cytology
  • Hepatocytes / drug effects
  • Hepatocytes / metabolism
  • Histone Deacetylase Inhibitors / pharmacology
  • Humans
  • Hydroxamic Acids / pharmacology*
  • Immunoenzyme Techniques
  • Immunoprecipitation
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Liver Neoplasms / etiology
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / prevention & control*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism
  • Mutation / genetics*
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Peptide Hydrolases / genetics
  • Peptide Hydrolases / metabolism
  • Protein Precursors / genetics
  • Protein Precursors / metabolism*
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • TATA Box Binding Protein-Like Proteins / genetics
  • TATA Box Binding Protein-Like Proteins / metabolism
  • Two-Hybrid System Techniques
  • Vorinostat

Substances

  • Hepatitis B Surface Antigens
  • Histone Deacetylase Inhibitors
  • Hydroxamic Acids
  • Intracellular Signaling Peptides and Proteins
  • Mutant Proteins
  • Nuclear Proteins
  • Protein Precursors
  • RNA, Messenger
  • TATA Box Binding Protein-Like Proteins
  • TBPL2 protein, human
  • presurface protein 2, hepatitis B surface antigen
  • Cyclin-Dependent Kinase Inhibitor p27
  • Vorinostat
  • Peptide Hydrolases
  • COPS5 protein, human
  • COP9 Signalosome Complex