Predictors of ribociclib-mediated antitumour effects in native and sorafenib-resistant human hepatocellular carcinoma cells

Cell Oncol (Dordr). 2019 Oct;42(5):705-715. doi: 10.1007/s13402-019-00458-8. Epub 2019 Jun 27.

Abstract

Purpose: The cyclin-dependent kinases (CDKs) CDK4 and CDK6 are important regulators of the cell cycle and represent promising targets in cancer treatment. We aimed to investigate the relevance of CDK4/6 in the development of hepatocellular carcinoma (HCC) and the potential of ribociclib, a novel orally available CDK4/6 inhibitor, as a treatment for HCC.

Methods: The effect of ribociclib was assessed in native and sorafenib-resistant HCC cell lines using viability assays, colony formation assays and FACS-based analyses. The expression of potential biomarkers of ribociclib response was assessed in cell lines and primary human hepatocytes using Western blotting. In addition, the prognostic relevance of the cyclin D-CDK4/6-retinoblastoma protein (Rb) pathway was assessed by analysing mRNA expression data from The Cancer Genome Atlas (TCGA).

Results: We found that ribociclib downregulated Rb and caused a profound loss of cell viability by inducing G1 cell cycle arrest in HCC cell lines exhibiting Rb-high/p16-low protein expression profiles, but not in Rb-low/p16-high cells, regardless their sensitivity to sorafenib. siRNA-based Rb silencing decreased cell proliferation, but did not diminish the sensitivity of HCC cells to ribociclib. Furthermore, we found that ribociclib synergized with sorafenib to cause cell death. mRNA analysis of primary human HCC specimens showed that CDK4 expression was correlated with patient survival and that the expression of Rb and the p16-encoding CDKN2A gene were inversely correlated.

Conclusions: From our data we conclude that impairment of the cyclin D-CDK4/6-Rb pathway is a frequent feature of HCC and that it is associated with a unfavourable prognosis. We also found that ribociclib exhibits a preferential antineoplastic activity in Rb-high HCC cells. Our results warrant further investigation of Rb and p16 expression as markers of HCC sensitivity to ribociclib.

Keywords: CDK inhibition; Hepatocellular carcinoma; Retinoblastoma protein; Ribociclib; Sorafenib; Targeted tumour therapy.

MeSH terms

  • Aminopyridines / pharmacology*
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Biomarkers, Tumor
  • Carcinoma, Hepatocellular / metabolism*
  • Carcinoma, Hepatocellular / mortality
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Cyclin-Dependent Kinase 4 / antagonists & inhibitors
  • Cyclin-Dependent Kinase 4 / metabolism*
  • Cyclin-Dependent Kinase 6 / antagonists & inhibitors
  • Cyclin-Dependent Kinase 6 / metabolism*
  • Cyclin-Dependent Kinase Inhibitor p16 / metabolism
  • Drug Resistance, Neoplasm
  • G1 Phase Cell Cycle Checkpoints / drug effects
  • Hepatocytes / drug effects
  • Humans
  • Liver Neoplasms / metabolism*
  • Liver Neoplasms / mortality
  • Purines / pharmacology*
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Retinoblastoma Protein / antagonists & inhibitors
  • Retinoblastoma Protein / genetics
  • Retinoblastoma Protein / metabolism*
  • Sorafenib / pharmacology

Substances

  • Aminopyridines
  • Antineoplastic Agents
  • Biomarkers, Tumor
  • Cyclin-Dependent Kinase Inhibitor p16
  • Purines
  • RNA, Small Interfering
  • Retinoblastoma Protein
  • Sorafenib
  • CDK6 protein, human
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6
  • ribociclib