Essential role of the voltage-dependent anion channel (VDAC) in mitochondrial permeability transition pore opening and cytochrome c release induced by arsenic trioxide

Oncogene. 2004 Feb 12;23(6):1239-47. doi: 10.1038/sj.onc.1207205.

Abstract

The precise molecular mechanism underlying arsenic trioxide (As(2)O(3))-induced apoptosis is a subject of extensive study. Here, we show that clinically relevant doses of As(2)O(3) can induce typical apoptosis in IM-9, a multiple myeloma cell line, in a Bcl-2 inhibitable manner. We confirmed that As(2)O(3) directly induced cytochrome c (cyto c) release from isolated mouse liver mitochondria via the mitochondrial permeability transition pore, and we further identified the voltage-dependent anion channel (VDAC) as a biological target of As(2)O(3) responsible for eliciting cyto c release in apoptosis. First, pretreatment of the isolated mitochondria with an anti-VDAC antibody specifically prevented As(2)O(3)-induced cyto c release. Second, in proteoliposome experiments, VDAC by itself was sufficient to mediate As(2)O(3)-induced cyto c release, which could be specifically inhibited by Bcl-X(L). Third, As(2)O(3) induced mitochondria membrane potential (DeltaPsim) reduction and cyto c release only in the VDAC-expressing, but not in the VDAC-deficient yeast strain. Finally, we found that As(2)O(3) induced the increased expression and homodimerization of VDAC in IM-9 cells, but not in Bcl-2 overexpressing cells, suggesting that VDAC homodimerization could potentially determine its gating capacity to cyto c, and Bcl-2 blockage of VDAC homodimerization represents a novel mechanism for its inhibition of apoptosis.

Publication types

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

MeSH terms

  • Animals
  • Annexin A5 / analysis
  • Arsenic Trioxide
  • Arsenicals / pharmacology*
  • Cytochromes c / analysis*
  • Flow Cytometry
  • Humans
  • Intracellular Membranes / physiology*
  • Ion Channel Gating / drug effects*
  • Ion Channel Gating / physiology
  • Membrane Potentials / physiology
  • Mice
  • Mice, Inbred BALB C
  • Mitochondria / physiology*
  • Mitochondria, Liver / physiology
  • Multiple Myeloma
  • Oxides / pharmacology*
  • Permeability
  • Porins / physiology*
  • Proteolipids / metabolism
  • Tumor Cells, Cultured
  • Voltage-Dependent Anion Channels

Substances

  • Annexin A5
  • Arsenicals
  • Oxides
  • Porins
  • Proteolipids
  • Voltage-Dependent Anion Channels
  • proteoliposomes
  • Cytochromes c
  • Arsenic Trioxide