Modulation of the poly (ADP-ribose) polymerase inhibitor response and DNA recombination in breast cancer cells by drugs affecting endogenous wild-type p53

Carcinogenesis. 2014 Oct;35(10):2273-82. doi: 10.1093/carcin/bgu160. Epub 2014 Aug 1.

Abstract

Synthetic lethal interactions between poly (ADP-ribose) polymerase (PARP) and homologous recombination (HR) repair pathways have been exploited for the development of novel mono- and combination cancer therapies. The tumor suppressor p53 was demonstrated to exhibit indirect and direct regulatory activities in DNA repair, particularly in DNA double-strand break (DSB)-induced and replication-associated HR. In this study, we tested a potential influence of the p53 status on the response to PARP inhibition, which is known to cause replication stress. Silencing endogenous or inducibly expressing p53 we found a protective effect of p53 on PARP inhibitor (PARPi)-mediated cytotoxicities. This effect was specific for wild-type versus mutant p53 and observed in cancer but not in non-transformed cell lines. Enhanced cytotoxicities after treatment with the p53-inhibitory drug Pifithrinα further supported p53-mediated resistance to PARP inhibition. Surprisingly, we equally observed increased PARPi sensitivity in the presence of the p53-activating compound Nutlin-3. As a common denominator, both drug responses correlated with decreased HR activities: Pifithrinα downregulated spontaneous HR resulting in damage accumulation. Nutlin-3 induced a decrease of DSB-induced HR, which was accompanied by a severe drop in RAD51 protein levels. Thus, we revealed a novel link between PARPi responsiveness and p53-controlled HR activities. These data expand the concept of cell and stress type-dependent healer and killer functions of wild-type p53 in response to cancer therapeutic treatment. Our findings have implications for the individualized design of cancer therapies using PARPi and the potentially combined use of p53-modulatory drugs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Benzothiazoles / pharmacology
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / genetics*
  • Cell Line, Tumor / drug effects
  • Enzyme Inhibitors / pharmacology*
  • Female
  • Gene Knockdown Techniques
  • Genes, p53*
  • Humans
  • Imidazoles / pharmacology
  • Isoquinolines / pharmacology
  • Molecular Weight
  • Piperazines / pharmacology
  • Poly(ADP-ribose) Polymerase Inhibitors*
  • Poly(ADP-ribose) Polymerases / genetics
  • Poly(ADP-ribose) Polymerases / metabolism
  • RNA, Small Interfering
  • Recombinational DNA Repair / drug effects*
  • Toluene / analogs & derivatives
  • Toluene / pharmacology

Substances

  • Benzothiazoles
  • Enzyme Inhibitors
  • Imidazoles
  • Isoquinolines
  • Piperazines
  • Poly(ADP-ribose) Polymerase Inhibitors
  • RNA, Small Interfering
  • Toluene
  • 1,5-dihydroxyisoquinoline
  • nutlin 3
  • pifithrin
  • Poly(ADP-ribose) Polymerases