The p53-cathepsin axis cooperates with ROS to activate programmed necrotic death upon DNA damage

Proc Natl Acad Sci U S A. 2009 Jan 27;106(4):1093-8. doi: 10.1073/pnas.0808173106. Epub 2009 Jan 14.

Abstract

Three forms of cell death have been described: apoptosis, autophagic cell death, and necrosis. Although genetic and biochemical studies have formulated a detailed blueprint concerning the apoptotic network, necrosis is generally perceived as a passive cellular demise resulted from unmanageable physical damages. Here, we conclude an active de novo genetic program underlying DNA damage-induced necrosis, thus assigning necrotic cell death as a form of "programmed cell death." Cells deficient of the essential mitochondrial apoptotic effectors, BAX and BAK, ultimately succumbed to DNA damage, exhibiting signature necrotic characteristics. Importantly, this genotoxic stress-triggered necrosis was abrogated when either transcription or translation was inhibited. We pinpointed the p53-cathepsin axis as the quintessential framework underlying necrotic cell death. p53 induces cathepsin Q that cooperates with reactive oxygen species (ROS) to execute necrosis. Moreover, we presented the in vivo evidence of p53-activated necrosis in tumor allografts. Current study lays the foundation for future experimental and therapeutic discoveries aimed at "programmed necrotic death."

Publication types

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

MeSH terms

  • Animals
  • Cathepsins / genetics
  • Cathepsins / metabolism*
  • Cell Line, Tumor
  • Cysteine Endopeptidases / genetics
  • Cysteine Endopeptidases / metabolism*
  • DNA Damage*
  • Fibroblasts / pathology
  • Fibroblasts / ultrastructure
  • Humans
  • Mice
  • Necrosis / pathology*
  • Neoplasm Transplantation
  • Neoplasms / pathology
  • Neoplasms / ultrastructure
  • Reactive Oxygen Species / metabolism*
  • Transcriptional Activation / genetics
  • Transplantation, Homologous
  • Tumor Suppressor Protein p53 / metabolism*
  • bcl-2 Homologous Antagonist-Killer Protein / deficiency
  • bcl-2 Homologous Antagonist-Killer Protein / metabolism
  • bcl-2-Associated X Protein / deficiency
  • bcl-2-Associated X Protein / metabolism

Substances

  • Bak1 protein, mouse
  • Bax protein, mouse
  • Reactive Oxygen Species
  • Tumor Suppressor Protein p53
  • bcl-2 Homologous Antagonist-Killer Protein
  • bcl-2-Associated X Protein
  • Cathepsins
  • Cysteine Endopeptidases
  • cathepsin Q