Ibulocydine sensitizes human hepatocellular carcinoma cells to TRAIL-induced apoptosis via calpain-mediated Bax cleavage

Int J Biochem Cell Biol. 2017 Feb:83:47-55. doi: 10.1016/j.biocel.2016.12.001. Epub 2016 Dec 5.

Abstract

Tumor necrosis factor-related apoptosis-induced ligand (TRAIL) induces apoptosis selectively in cancer cells without affecting the majority of normal human cells. However, hepatocellular carcinoma (HCC) cells often display resistance to TRAIL-induced apoptosis. Ibulocydine (IB) is an isobutyrate ester pro-drug of a novel synthetic Cdk inhibitor that targets Cdk7 and Cdk9. In this study, we show that treatment with subtoxic doses of IB in combination with TRAIL displays potent cytotoxicity in TRAIL-resistant human HCC cells. Combination of IB and TRAIL was found to synergistically induce apoptosis through activation of caspases, which was blocked by a pan-caspase inhibitor (zVAD). Although the expression of Mcl-1 and survivin were reduced by IB plus TRAIL, overexpression of Mcl-1 and survivin did not block the cell death induced by co-treatment. Moreover, overexpression of Bcl-xL did not significantly interfere with the cell death induced by co-treatment of IB and TRAIL. Interestingly, the combination treatment induced cleavage of Bax, which was translocated to mitochondria upon induction of apoptosis. Furthermore, down-regulation of Bax by small interfering RNA effectively reduced the cell death and loss of mitochondrial membrane potential (MMP) caused by co-treatment with IB and TRAIL. Finally, pre-treatment of HCC cells with a calpain inhibitor effectively blocked IB plus TRAIL-induced cleavage of Bax and apoptosis. Collectively, our results demonstrate that IB increases the sensitivity of human HCC cells to TRAIL via mitochondria signaling pathway mediated by calpain-induced cleavage of Bax, suggesting that combined treatment with IB and TRAIL may offer an effective therapeutic strategy for human HCC.

Keywords: Calpain; Caspase; Cleaved-Bax; Ibulocydine; Mitochondria.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / drug effects*
  • Apoptosis / physiology
  • Calpain / metabolism*
  • Carcinoma, Hepatocellular / drug therapy*
  • Carcinoma, Hepatocellular / metabolism
  • Carcinoma, Hepatocellular / pathology
  • Caspases / metabolism
  • Cell Line, Tumor
  • Drug Synergism
  • Humans
  • Liver Neoplasms / drug therapy*
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Prodrugs / administration & dosage
  • Prodrugs / pharmacology*
  • Pyrimidine Nucleosides / administration & dosage
  • Pyrimidine Nucleosides / pharmacology*
  • RNA, Small Interfering / genetics
  • Signal Transduction / drug effects
  • TNF-Related Apoptosis-Inducing Ligand / administration & dosage
  • TNF-Related Apoptosis-Inducing Ligand / metabolism*
  • Up-Regulation
  • bcl-2-Associated X Protein / antagonists & inhibitors
  • bcl-2-Associated X Protein / genetics
  • bcl-2-Associated X Protein / metabolism*
  • bcl-X Protein / genetics
  • bcl-X Protein / metabolism

Substances

  • (5-(4-amino-6-bromo-5-carbamoyl-1H-pyrrolo(2,3-d)pyrimidin-1-yl)-3,4-dihydroxytetrahydrofuran-2-yl)methyl isobutyrate
  • BAX protein, human
  • BCL2L1 protein, human
  • Prodrugs
  • Pyrimidine Nucleosides
  • RNA, Small Interfering
  • TNF-Related Apoptosis-Inducing Ligand
  • TNFSF10 protein, human
  • bcl-2-Associated X Protein
  • bcl-X Protein
  • Calpain
  • Caspases