Hepatitis B virus X protein enhances transcriptional activity of hypoxia-inducible factor-1alpha through activation of mitogen-activated protein kinase pathway

J Biol Chem. 2003 Oct 3;278(40):39076-84. doi: 10.1074/jbc.M305101200. Epub 2003 Jul 10.

Abstract

Hepatitis B virus X protein (HBx) of the hepatitis B virus was strongly implicated in angiogenesis and metastasis during hepatocarcinogenesis. Here, we explored the possibility of cross-talk between HBx and hypoxia-inducible factor-1alpha (HIF-1alpha), a potent transcriptional inducer of angiogenic factors. First, we showed that stability of HIF-1alpha protein was increased by HBx in HBx-inducible Chang liver cells as well as in transient HBx expression system of non-hepatic cells. Immunofluorescence studies revealed that the HBx-induced HIF-1alpha was partially translocated into the nucleus in majority of cells while additional CoCl2-induced hypoxic condition caused complete nuclear translocation. Second, HBx induced both phosphorylation of HIF-1alpha and activation of p42/p44 mitogen-activated protein kinases (MAPKs), which were synergistically enhanced in the presence of CoCl2. Furthermore, HBx enhanced transcriptional activity of HIF-1alpha in the reporter genes encoding hypoxia response element or VEGF promoter. Either treatment of MEK inhibitor PD98059 or coexpression of dominant-negative MAPK mutants abolished the HBx-induced transcriptional activity and protein stability as well as nuclear translocation of HIF-1alpha, suggesting that HBx activates HIF-1alpha through MAPK pathway. Third, the association of HIF-1alpha with von Hippel-Lindau was decreased but the association with CREB-binding protein was enhanced in the presence of HBx, suggesting the molecular mechanism by which HBx enhances the protein stability and transactivation function of HIF-1alpha. Finally, we demonstrated that expression of HIF-1alpha and vascular endothelial growth factor was increased in the liver of HBx-transgenic mice, suggesting that the cross-talk between HIF-1alpha and HBx may lead to transcriptional activation of HIF-1alpha target genes, which play a critical role in hepatocarcinogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Androstadienes / pharmacology
  • Animals
  • Blotting, Western
  • Cell Line
  • Cell Nucleus / metabolism
  • Cobalt / pharmacology
  • Endothelial Growth Factors / metabolism
  • Enzyme Inhibitors / pharmacology
  • Flavonoids / pharmacology
  • Flow Cytometry
  • Genes, Reporter
  • HeLa Cells
  • Humans
  • Hypoxia
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Immunohistochemistry
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Ligases / metabolism
  • Lymphokines / metabolism
  • MAP Kinase Signaling System*
  • Mice
  • Mice, Transgenic
  • Microscopy, Fluorescence
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases / metabolism
  • Phosphorylation
  • Plasmids / metabolism
  • Precipitin Tests
  • Promoter Regions, Genetic
  • Protein Transport
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction
  • Time Factors
  • Trans-Activators / metabolism
  • Trans-Activators / physiology*
  • Transcription Factors / metabolism*
  • Transcription, Genetic*
  • Transcriptional Activation
  • Transfection
  • Tumor Cells, Cultured
  • Tumor Suppressor Proteins*
  • Ubiquitin-Protein Ligases*
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors
  • Viral Regulatory and Accessory Proteins
  • Von Hippel-Lindau Tumor Suppressor Protein
  • Wortmannin

Substances

  • Androstadienes
  • Endothelial Growth Factors
  • Enzyme Inhibitors
  • Flavonoids
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Intercellular Signaling Peptides and Proteins
  • Lymphokines
  • Trans-Activators
  • Transcription Factors
  • Tumor Suppressor Proteins
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors
  • Viral Regulatory and Accessory Proteins
  • hepatitis B virus X protein
  • Cobalt
  • Ubiquitin-Protein Ligases
  • Von Hippel-Lindau Tumor Suppressor Protein
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases
  • Ligases
  • VHL protein, human
  • cobaltous chloride
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one
  • Wortmannin