Bortezomib induces protective autophagy through AMP-activated protein kinase activation in cultured pancreatic and colorectal cancer cells

Cancer Chemother Pharmacol. 2014 Jul;74(1):167-76. doi: 10.1007/s00280-014-2451-7. Epub 2014 May 20.

Abstract

Background: Bortezomib, a selective and potent inhibitor of the proteasome, has demonstrated broad anti-tumor activities in many malignancies. In the current study, we aimed to understand the potential resistance factor of bortezomib in cultured pancreatic and colorectal cancer cells.

Results: We observed that bortezomib-induced protective autophagy in cultured PANC-1 pancreatic cancer cells and HT-29 colorectal cancer cells. Inhibition of autophagy by 3-methyladenine (3-MA) and chloroquine enhanced bortezomib-induced apoptosis and cytotoxicity in both PANC-1 and HT-29 cells. Activation of AMP-activated protein kinase (AMPK) was required for bortezomib-induced autophagy induction in PANC-1 and HT-29 cells, and AMPK inhibition by its inhibitor compound C (CC) or RNAi-depletion suppressed bortezomib-induced autophagy, while dramatically enhancing cancer cell apoptosis/cytotoxicity. Meanwhile, significant AMPK activation and autophagy induction were observed after bortezomib stimulation in primary cultured pancreatic cancer cells derived from a patient's tumor tissue. Both CC and 3-MA facilitated bortezomib-induced cytotoxicity in primary cultured pancreatic cancer cells.

Conclusions: In conclusion, our data here suggest that bortezomib induces protective autophagy in pancreatic and colorectal cancer cells through activating AMPK-Ulk1 signalings. AMPK or autophagy inhibitors could be developed as an adjunct or chemo-sensitizer for bortezomib.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / antagonists & inhibitors
  • AMP-Activated Protein Kinases / chemistry
  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / metabolism*
  • Adenine / analogs & derivatives
  • Adenine / pharmacology
  • Antineoplastic Agents / agonists
  • Antineoplastic Agents / antagonists & inhibitors
  • Antineoplastic Agents / pharmacology*
  • Autophagy / drug effects*
  • Boronic Acids / agonists
  • Boronic Acids / antagonists & inhibitors
  • Boronic Acids / pharmacology*
  • Bortezomib
  • Cell Survival / drug effects
  • Cells, Cultured
  • Chloroquine / pharmacology
  • Colorectal Neoplasms / drug therapy*
  • Colorectal Neoplasms / enzymology
  • Colorectal Neoplasms / metabolism
  • Drug Resistance, Neoplasm / drug effects
  • Drug Synergism
  • Enzyme Activation / drug effects
  • Humans
  • Neoplasm Proteins / agonists
  • Neoplasm Proteins / metabolism
  • Pancreatic Neoplasms / drug therapy*
  • Pancreatic Neoplasms / metabolism
  • Pancreatic Neoplasms / pathology
  • Proteasome Inhibitors / agonists
  • Proteasome Inhibitors / chemistry
  • Proteasome Inhibitors / pharmacology*
  • Protein Kinase Inhibitors
  • Pyrazines / agonists
  • Pyrazines / antagonists & inhibitors
  • Pyrazines / pharmacology*
  • RNA Interference
  • RNA, Small Interfering

Substances

  • Antineoplastic Agents
  • Boronic Acids
  • Neoplasm Proteins
  • Proteasome Inhibitors
  • Protein Kinase Inhibitors
  • Pyrazines
  • RNA, Small Interfering
  • 3-methyladenine
  • Bortezomib
  • Chloroquine
  • AMP-Activated Protein Kinases
  • Adenine