Constitutive gp130 activation rapidly accelerates the transformation of human hepatocytes via an impaired oxidative stress response

Oncotarget. 2016 Aug 23;7(34):55639-55648. doi: 10.18632/oncotarget.10956.

Abstract

Pro-inflammatory signaling pathways, especially interleukin 6 (IL-6), and reactive oxygen species (ROS) promote carcinogenesis in the liver. In order to elucidate the underlying oncogenic mechanism, we activated the IL-6 signal transducer glycoprotein 130 (gp130) via stable expression of a constitutively active gp130 construct (L-gp130) in untransformed telomerase-immortalized human fetal hepatocytes (FH-hTERT). As known from hepatocellular adenomas, forced gp130 activation alone was not sufficient to induce malignant transformation. However, additional challenge of FH-hTERT L-gp130 clones with oxidative stress resulted in 2- to 3-fold higher ROS levels and up to 6-fold more DNA-double strand breaks (DSB). Despite increased DNA damage, ROS-challenged FH-hTERT L-gp130 clones displayed an enhanced proliferation and rapidly developed colony growth capabilities in soft agar. As driving gp130-mediated oncogenic mechanism, we detected a decreased expression of antioxidant genes, in particular glutathione peroxidase 3 and apolipoprotein E, and an absence of P21 upregulation following ROS-conferred induction of DSB. In summary, an impaired oxidative stress response in hepatocytes with gp130 gain-of-function mutations, as detected in dysplastic intrahepatic nodules and hepatocellular adenomas, is one of the central oncogenic mechanisms in chronic liver inflammation.

Keywords: glycoprotein 130; hepatocyte transformation; interleukin 6; oxidative stress response; reactive oxygen species.

MeSH terms

  • Animals
  • Cell Transformation, Neoplastic*
  • Cytokine Receptor gp130 / physiology*
  • DNA Breaks, Double-Stranded
  • Female
  • Hep G2 Cells
  • Hepatocytes / pathology*
  • Humans
  • Liver Neoplasms / etiology*
  • Mice
  • Oxidative Stress*
  • Reactive Oxygen Species / metabolism
  • Signal Transduction / physiology
  • Telomerase / genetics

Substances

  • Reactive Oxygen Species
  • Cytokine Receptor gp130
  • TERT protein, human
  • Telomerase