The hepatitis B virus X protein promotes pancreatic cancer through modulation of the PI3K/AKT signaling pathway

Cancer Lett. 2016 Sep 28;380(1):98-105. doi: 10.1016/j.canlet.2016.06.011. Epub 2016 Jun 21.

Abstract

Pancreatic ductal adenocarcinoma (PDAC) is an aggressive and lethal cancer, with poor outcomes. Infection with the hepatitis B virus (HBV) may be associated as a worse prognosis for PDAC patients; however, the mechanisms involved in this process are unclear. We evaluated whether HBV infection leads to PDAC with a more aggressive phenotype, and attempted to elucidate the mechanisms involved. Clinicopathological data and outcomes from 64 patients with PDAC were collected and compared between serum HBsAg+ and HBsAg- patients. Furthermore, we examined the effects of the HBV X protein (HBx) on proliferation and migration of the pancreatic cancer cell lines PANC-1 and SW1990. We investigated expression changes of over 500 proteins by protein array analysis and identified several HBV- and PDAC-related candidates, which were further validated by immunoblotting and enzyme-linked immunosorbent assay. No differences in clinicopathological features were observed between HBsAg+ and HBsAg- patients; however, HBsAg+ patients had a shorter median survival time (8 vs. 13 months), although the differences were not significant. HBV DNA was detected in clinical specimens, even in PDAC patients considered "HBV-free", potentially due to occult infection. HBx expression significantly enhanced cellular proliferation and migration and induced an epithelial-mesenchymal transition phenotype. Expression of ErbB4 and TGF-α was increased in parallel with HBx expression, and several downstream pathways including PI3K/AKT, MAPK, and ERK were upregulated. Inhibition of the PI3K/AKT pathway reversed the effects of HBx in PDAC cell lines. HBx may, therefore, contribute to the progression of PDAC through modulation of these pathways.

Keywords: HBx; Migration; PI3K/AKT signaling; Risk factor; Survival.

MeSH terms

  • Carcinoma, Pancreatic Ductal / enzymology*
  • Carcinoma, Pancreatic Ductal / pathology
  • Carcinoma, Pancreatic Ductal / surgery
  • Carcinoma, Pancreatic Ductal / virology
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • Cell Transformation, Viral*
  • Epithelial-Mesenchymal Transition
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Hepatitis B / complications
  • Hepatitis B / metabolism*
  • Hepatitis B / virology
  • Hepatitis B Surface Antigens / blood
  • Hepatitis B virus / genetics
  • Hepatitis B virus / metabolism*
  • Hepatitis B virus / pathogenicity
  • Humans
  • Kaplan-Meier Estimate
  • Pancreatic Neoplasms / enzymology*
  • Pancreatic Neoplasms / pathology
  • Pancreatic Neoplasms / surgery
  • Pancreatic Neoplasms / virology
  • Phenotype
  • Phosphatidylinositol 3-Kinase / metabolism*
  • Phosphoinositide-3 Kinase Inhibitors
  • Protein Kinase Inhibitors / pharmacology
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Receptor, ErbB-4 / metabolism
  • Signal Transduction* / drug effects
  • Time Factors
  • Trans-Activators / genetics
  • Trans-Activators / metabolism*
  • Transfection
  • Tumor Necrosis Factor-alpha / metabolism
  • Viral Regulatory and Accessory Proteins

Substances

  • Hepatitis B Surface Antigens
  • Phosphoinositide-3 Kinase Inhibitors
  • Protein Kinase Inhibitors
  • Trans-Activators
  • Tumor Necrosis Factor-alpha
  • Viral Regulatory and Accessory Proteins
  • hepatitis B virus X protein
  • Phosphatidylinositol 3-Kinase
  • ERBB4 protein, human
  • Receptor, ErbB-4
  • Proto-Oncogene Proteins c-akt
  • Extracellular Signal-Regulated MAP Kinases