3,3'-diindolylmethane enhances the efficacy of butyrate in colon cancer prevention through down-regulation of survivin

Cancer Prev Res (Phila). 2009 Jun;2(6):581-9. doi: 10.1158/1940-6207.CAPR-08-0142. Epub 2009 May 26.

Abstract

Butyrate is an inhibitor of histone deacetylase (HDAC) and has been extensively evaluated as a chemoprevention agent for colon cancer. We recently showed that mutations in the adenomatous polyposis coli (APC) gene confer resistance to HDAC inhibitor-induced apoptosis in colon cancers. Here, we show that APC mutation rendered colon cancer cells resistant to butyrate-induced apoptosis due to the failure of butyrate to down-regulate survivin in these cells. Another cancer-preventive agent, 3,3'-diindolylmethane (DIM), was identified to be able to down-regulate survivin in colon cancers expressing mutant APC. DIM inhibited survivin mRNA expression and promoted survivin protein degradation through inhibition of p34(cdc2)-cyclin B1-mediated survivin Thr(34) phosphorylation. Pretreatment with DIM enhanced butyrate-induced apoptosis in colon cancer cells expressing mutant APC. DIM/butyrate combination treatment induced the expression of proapoptotic Bax and Bak proteins, triggered Bax dimerization/activation, and caused release of cytochrome c and Smac proteins from mitochondria. Whereas overexpression of survivin blocked DIM/butyrate-induced apoptosis, knocking down of survivin by small interfering RNA increased butyrate-induced apoptosis in colon cancer cells. We further showed that DIM was able to down-regulate survivin and enhance the effects of butyrate in apoptosis induction and prevention of familial adenomatous polyposis in APC(min/+) mice. Thus, the combination of DIM and butyrate is potentially an effective strategy for the prevention of colon cancer.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenocarcinoma / genetics
  • Adenocarcinoma / metabolism
  • Adenocarcinoma / pathology
  • Adenocarcinoma / prevention & control*
  • Adenomatous Polyposis Coli / drug therapy
  • Adenomatous Polyposis Coli / pathology
  • Animals
  • Anticarcinogenic Agents / administration & dosage
  • Anticarcinogenic Agents / pharmacology*
  • Anticarcinogenic Agents / therapeutic use
  • Apoptosis / drug effects
  • Butyrates / administration & dosage
  • Butyrates / pharmacology*
  • Butyrates / therapeutic use
  • Cell Line, Tumor / drug effects
  • Cell Line, Tumor / metabolism
  • Colonic Neoplasms / genetics
  • Colonic Neoplasms / metabolism
  • Colonic Neoplasms / pathology
  • Colonic Neoplasms / prevention & control*
  • DNA, Complementary / genetics
  • Down-Regulation / drug effects
  • Drug Synergism
  • Gene Expression Regulation, Neoplastic / drug effects
  • Genes, APC
  • Histone Deacetylase Inhibitors
  • Humans
  • Indoles / administration & dosage
  • Indoles / pharmacology*
  • Indoles / therapeutic use
  • Inhibitor of Apoptosis Proteins
  • Mice
  • Mice, Mutant Strains
  • Microtubule-Associated Proteins / antagonists & inhibitors*
  • Microtubule-Associated Proteins / biosynthesis
  • Microtubule-Associated Proteins / genetics
  • Neoplasm Proteins / antagonists & inhibitors*
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Recombinant Fusion Proteins / antagonists & inhibitors
  • Survivin

Substances

  • Anticarcinogenic Agents
  • BIRC5 protein, human
  • Butyrates
  • DNA, Complementary
  • Histone Deacetylase Inhibitors
  • Indoles
  • Inhibitor of Apoptosis Proteins
  • Microtubule-Associated Proteins
  • Neoplasm Proteins
  • Recombinant Fusion Proteins
  • Survivin
  • 3,3'-diindolylmethane