IL-23 production of liver inflammatory macrophages to damaged hepatocytes promotes hepatocellular carcinoma development after chronic hepatitis B virus infection

Biochim Biophys Acta Mol Basis Dis. 2018 Dec;1864(12):3759-3770. doi: 10.1016/j.bbadis.2018.10.004. Epub 2018 Oct 4.

Abstract

Liver inflammation after chronic hepatitis B virus (HBV) infection is essential for hepatocellular carcinoma (HCC) development. We did a nested case-control study based on QBC chronic HBV infection cohort to identify HCC-related inflammatory cytokines. Serum levels of distinct Th-cell representative cytokines at varied periods before HCC diagnosis were determined in 50 HCC cases and 150 age- and gender-matched controls who did not develop HCC in 8-10 years. The individuals with HCC outcome had statistically higher serum levels of IL-23 than controls (P < 0.01). Further analysis in HCC tissues showed that CD14+ inflammatory macrophages were the major IL-23 producers. Monocytes-derived macrophages generated more amount of IL-23 after being stimulated with cell-associated HBV core antigen from damaged HBV-infected hepatocytes than the cells being stimulated with HBV-S and HBV e antigen, which are secreted from infected hepatocytes. IL-23 upregulated IL-23 receptor expressions on macrophages, enhanced macrophage-mediated angiogenesis. In HBV-transgenic (Alb1HBV) mice, administration of diethylnitrosamine induced more liver tumors than in wild-type mice. The livers of Alb1HBV mice had higher concentrations of IL-23 and vascular endothelial growth factor (VEGF) than the wild-type mice. Neutralizing IL-23 activity, diethylnitrosamine-treated Alb1HBV mice developed significantly less tumors and produced less VEGF, tumor angiogenesis was inhibited with dramatically decreased CD31+ cells within tumor mass (all P < 0.01). CONCLUSION: Persistent IL-23 generation of liver inflammatory macrophages responding to damaged hepatocytes after chronic HBV infection altered macrophage function for HCC promotion. Blocking IL-23 activity might be helpful for the intervention in chronic hepatitis B patients who had high risk to HCC.

Keywords: Hepatitis B virus proteins; Hepatocellular carcinoma; Interleukin 23; Liver macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular / blood
  • Carcinoma, Hepatocellular / etiology*
  • Carcinoma, Hepatocellular / immunology
  • Carcinoma, Hepatocellular / pathology
  • Cell Line, Tumor
  • Female
  • Hepatitis B, Chronic / blood
  • Hepatitis B, Chronic / complications*
  • Hepatitis B, Chronic / immunology
  • Hepatitis B, Chronic / pathology
  • Hepatocytes / immunology*
  • Hepatocytes / pathology
  • Humans
  • Inflammation / blood
  • Inflammation / etiology*
  • Inflammation / immunology
  • Inflammation / pathology
  • Interleukin-23 / blood
  • Interleukin-23 / immunology*
  • Liver / immunology
  • Liver / pathology
  • Liver Neoplasms / blood
  • Liver Neoplasms / etiology*
  • Liver Neoplasms / immunology
  • Liver Neoplasms / pathology
  • Macrophages / immunology*
  • Macrophages / pathology
  • Male
  • Mice, Inbred C57BL
  • Neovascularization, Pathologic / blood
  • Neovascularization, Pathologic / etiology
  • Neovascularization, Pathologic / immunology
  • Neovascularization, Pathologic / pathology

Substances

  • Interleukin-23