Bortezomib-induced apoptosis in cultured pancreatic cancer cells is associated with ceramide production

Cancer Chemother Pharmacol. 2014 Jan;73(1):69-77. doi: 10.1007/s00280-013-2318-3. Epub 2013 Nov 5.

Abstract

Purpose: The proteasome inhibitor bortezomib (PS-341) has displayed significant efficiency against pancreatic cancer cells. However, the underlying mechanisms are not fully understood. Here, we tested if ceramide production was involved in the bortezomib's effect.

Methods: Two transformed pancreatic cancer cell lines (PANC-1 and Mia) and the primary pancreatic cancer cells were used. Cell death was analyzed by MTT viability assay and trypan blue staining. Cell apoptosis was analyzed by Histone DNA-ELISA assay and Annexin V FACS. Western blots were used to test signal protein changes. The cellular ceramide level after bortezomib treatment was also determined.

Results: In cultured pancreatic cancer cells, bortezomib increased cellular ceramide production to promote cell apoptosis. The ceramide de novo synthase inhibitor fumonisin B1 (F-B1) suppressed bortezomib-induced ceramide production and apoptosis, while exogenously added C6-ceramide facilitated bortezomib-induced pancreatic cancer cell death. Meanwhile, 1-phenyl-2-decanoylamino-3-morpholino-1-propanol (PDMP), the inhibitor of glucosylceramide synthetase as well as the sphingosine kinase 1 inhibitors (SKI-II and SKI-IV), facilitated bortezomib-induced ceramide production and subsequent cell apoptosis. Further, bortezomib-induced pro-apoptotic c-Jun N-terminal kinase (JNK) activation was also associated with ceramide production. JNK activation by bortezomib was suppressed by F-B1, but was enhanced by SKI-II and PDMP in pancreatic cancer cells. Finally, C6-ceramide, SKI-II, and PDMP dramatically enhanced bortezomib-induced cytotoxicity in primary cultured pancreatic cancer cells.

Conclusions: We found that bortezomib-induced apoptosis was associated with ceramide production in primary and transformed pancreatic cancer cells.

MeSH terms

  • Antineoplastic Agents / therapeutic use*
  • Apoptosis / drug effects*
  • Boronic Acids / pharmacology*
  • Bortezomib
  • Cell Line, Tumor
  • Ceramides / biosynthesis*
  • Humans
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • MAP Kinase Kinase Kinase 5 / physiology
  • Morpholines / pharmacology
  • Pancreatic Neoplasms / drug therapy*
  • Pancreatic Neoplasms / metabolism
  • Pancreatic Neoplasms / pathology
  • Phosphotransferases (Alcohol Group Acceptor) / antagonists & inhibitors
  • Pyrazines / pharmacology*

Substances

  • Antineoplastic Agents
  • Boronic Acids
  • Ceramides
  • Morpholines
  • Pyrazines
  • Bortezomib
  • RV 538
  • Phosphotransferases (Alcohol Group Acceptor)
  • sphingosine kinase
  • JNK Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase Kinase 5
  • MAP3K5 protein, human