Cytotoxicity of 5-Aza-2'-deoxycytidine against gastric cancer involves DNA damage in an ATM-P53 dependent signaling pathway and demethylation of P16(INK4A)

Biomed Pharmacother. 2013 Feb;67(1):78-87. doi: 10.1016/j.biopha.2012.10.015. Epub 2012 Nov 19.

Abstract

The DNA methylation inhibitor 5-Aza-2'-deoxycytidine (5-Aza-CdR) has increasingly attracted worldwide attention for its antineoplastic potential. The cytotoxitic mechanisms, however, especially, the relative contribution of silenced genes reactivation by demethylation and enzyme-DNA adduct formation to the efficacy of 5-Aza-CdR is still a crucial unresolved question. In this investigation, we demonstrated that 5-Aza-CdR treatment resulted in growth suppression in a concentration and time-dependent manner and G2 phrase arrest - hallmarks of a DNA damage response in gastric cancer AGS cells. Formation of DNA double-strand breaks, as monitored by comet assay was examined in an ATM (ataxia-telangiectasia mutated)-dependent manner based on the fact that PI3K inhibitor Wortmannin abolished the action of cytotoxicity of 5-Aza-CdR. Upon treatment with 5-Aza-CdR, ATM activation was clearly associated with P53 phosphorylation at Ser(15), which was directly responsible for 5-Aza-CdR modified P21(Waf1/Cip1) expression. Further exploration revealed that demethylation of P16(INK4A) correlated with the strikingly down-regulated expressions of DNA methyltransferase 3A as well as 3B was, at least in part, attributed to the cytotoxicity of 5-Aza-CdR in AGS cells. Conclusively, these results greatly enhance our understanding of the mechanisms of cytotoxicity of 5-Aza-CdR and strongly provide the preclinical rationale for an assessment of 5-Aza-CdR to ameliorate patient outcome with gastric cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Androstadienes / pharmacology
  • Antimetabolites, Antineoplastic / administration & dosage
  • Antimetabolites, Antineoplastic / pharmacology*
  • Ataxia Telangiectasia Mutated Proteins
  • Azacitidine / administration & dosage
  • Azacitidine / analogs & derivatives*
  • Azacitidine / pharmacology
  • Cell Cycle Proteins / metabolism
  • Cell Line, Tumor
  • Comet Assay
  • DNA (Cytosine-5-)-Methyltransferases / genetics
  • DNA Breaks, Double-Stranded / drug effects
  • DNA Damage / drug effects*
  • DNA Methyltransferase 3A
  • DNA Methyltransferase 3B
  • DNA-Binding Proteins / metabolism
  • Decitabine
  • Dose-Response Relationship, Drug
  • Down-Regulation
  • G2 Phase Cell Cycle Checkpoints / drug effects
  • Humans
  • Protein Serine-Threonine Kinases / metabolism
  • Signal Transduction / drug effects
  • Stomach Neoplasms / drug therapy*
  • Stomach Neoplasms / pathology
  • Time Factors
  • Tumor Suppressor Protein p53 / metabolism
  • Tumor Suppressor Proteins / metabolism
  • Wortmannin

Substances

  • Androstadienes
  • Antimetabolites, Antineoplastic
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • DNMT3A protein, human
  • Tumor Suppressor Protein p53
  • Tumor Suppressor Proteins
  • Decitabine
  • DNA (Cytosine-5-)-Methyltransferases
  • DNA Methyltransferase 3A
  • ATM protein, human
  • Ataxia Telangiectasia Mutated Proteins
  • Protein Serine-Threonine Kinases
  • Azacitidine
  • Wortmannin