Redirecting apoptosis to aponecrosis induces selective cytotoxicity to pancreatic cancer cells through increased ROS, decline in ATP levels, and VDAC

Mol Cancer Ther. 2013 Dec;12(12):2792-803. doi: 10.1158/1535-7163.MCT-13-0234. Epub 2013 Oct 14.

Abstract

Pancreatic cancer cell lines with mutated ras underwent an alternative form of cell death (aponecrosis) when treated concomitantly with clinically achievable concentrations of arsenic trioxide, ascorbic acid, and disulfiram (Antabuse; AAA). AAA's major effects are mediated through generation of intracellular reactive oxygen species (ROS) and more than 50% decline in intracellular ATP. N-acetyl cysteine and a superoxide dismutase mimetic prevented aponecrosis and restored intracellular ATP levels. DIDS (4,4'-diisothiocyanatostilbene-2, 2' disulfonic acid), the pan- Voltage-Dependent Anion Channel (VDAC), -1, 2, 3 inhibitor and short hairpin RNA (shRNA) to VDAC-1 blocked cell death and ROS accumulation. In vivo exposure of AAA led to a 62% reduction in mean tumor size and eliminated tumors in 30% of nude mice with PANC-1 xenografts. We concluded that early caspase-independent apoptosis was shifted to VDAC-mediated "targeted" aponecrosis by the addition of disulfiram to arsenic trioxide and ascorbic acid. Conceptually, this work represents a paradigm shift where switching from apoptosis to aponecrosis death pathways, also known as targeted aponecrosis, could be utilized to selectively kill pancreatic cancer cells resistant to apoptosis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Animals
  • Antineoplastic Agents / administration & dosage
  • Antineoplastic Agents / pharmacology
  • Apoptosis* / drug effects
  • Arsenic Trioxide
  • Arsenicals / administration & dosage
  • Arsenicals / pharmacology
  • Ascorbic Acid / administration & dosage
  • Ascorbic Acid / pharmacology
  • Cell Line, Tumor
  • Disease Models, Animal
  • Disulfiram / administration & dosage
  • Disulfiram / pharmacology
  • Dose-Response Relationship, Drug
  • Heterografts
  • Humans
  • Male
  • Mice
  • Necrosis / metabolism*
  • Oxides / administration & dosage
  • Oxides / pharmacology
  • Pancreatic Neoplasms / drug therapy
  • Pancreatic Neoplasms / metabolism*
  • Pancreatic Neoplasms / pathology*
  • Reactive Oxygen Species / metabolism*
  • Tumor Stem Cell Assay
  • Voltage-Dependent Anion Channels / metabolism*

Substances

  • Antineoplastic Agents
  • Arsenicals
  • Oxides
  • Reactive Oxygen Species
  • Voltage-Dependent Anion Channels
  • Adenosine Triphosphate
  • Ascorbic Acid
  • Arsenic Trioxide
  • Disulfiram