Zinc-dependent interaction between JAB1 and pre-S2 mutant large surface antigen of hepatitis B virus and its implications for viral hepatocarcinogenesis

J Virol. 2013 Dec;87(23):12675-84. doi: 10.1128/JVI.01497-13. Epub 2013 Sep 18.

Abstract

Chronic hepatitis B virus (HBV) infection is a major cause of hepatocellular carcinoma (HCC) worldwide. The pre-S2 mutant large HBV surface protein (Δ2 LHBS), which contains an in-frame deletion of approximately 17 amino acids in LHBS, is highly associated with risks and prognoses of HBV-induced HCC. It was previously reported that Δ2 LHBS interacts with the Jun activation domain-binding protein 1 (JAB1), a zinc metalloprotease. This promotes the degradation of the cell cycle regulator p27(Kip1) and is believed to be the major mechanism for Δ2 LHBS-induced HCC. In this study, it was found that the interaction between JAB1 and Δ2 LHBS is facilitated by divalent metal Zn(2+) ions. The binding of JAB1 to Δ2 LHBS requires the JAB1/CSN5 MPN metalloenzyme (JAMM) motif and residue H138 that binds to Zn(2+) ions in JAB1. Isothermal titration calorimetry showed that Δ2 LHBS binds directly to Zn(2+) ions in a two-site binding mode. Residues H71 and H116 in Δ2 LHBS, which also contact Zn(2+) ions, are also indispensable for Δ2 LHBS-mediated p27(Kip1) degradation in human HuH7 cells. These results suggest that developing drugs that interrupt interactions between Δ2 LHBS and JAB1 can be used to mitigate Δ2 LHBS-associated risks for HCC.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • COP9 Signalosome Complex
  • Carcinoma, Hepatocellular / enzymology*
  • Carcinoma, Hepatocellular / virology
  • Cell Line, Tumor
  • Hepatitis B Surface Antigens / genetics
  • Hepatitis B Surface Antigens / metabolism*
  • Hepatitis B virus / genetics
  • Hepatitis B virus / metabolism*
  • Hepatitis B, Chronic / enzymology*
  • Hepatitis B, Chronic / virology
  • Humans
  • Intracellular Signaling Peptides and Proteins / chemistry
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Liver Neoplasms / enzymology*
  • Liver Neoplasms / virology
  • Peptide Hydrolases / chemistry
  • Peptide Hydrolases / genetics
  • Peptide Hydrolases / metabolism*
  • Protein Binding
  • Protein Precursors / genetics
  • Protein Precursors / metabolism*
  • Zinc / metabolism*

Substances

  • Hepatitis B Surface Antigens
  • Intracellular Signaling Peptides and Proteins
  • Protein Precursors
  • presurface protein 2, hepatitis B surface antigen
  • Peptide Hydrolases
  • COPS5 protein, human
  • COP9 Signalosome Complex
  • Zinc