Targeting DNA Damage Response in Prostate Cancer by Inhibiting Androgen Receptor-CDC6-ATR-Chk1 Signaling

Cell Rep. 2017 Feb 21;18(8):1970-1981. doi: 10.1016/j.celrep.2017.01.072.

Abstract

Cell division cycle 6 (CDC6), an androgen receptor (AR) target gene, is implicated in regulating DNA replication and checkpoint mechanisms. CDC6 expression is increased during prostate cancer (PCa) progression and positively correlates with AR in PCa tissues. AR or CDC6 knockdown, together with AZD7762, a Chk1/2 inhibitor, results in decreased TopBP1-ATR-Chk1 signaling and markedly increased ataxia-telangiectasia-mutated (ATM) phosphorylation, a biomarker of DNA damage, and synergistically increases treatment efficacy. Combination treatment with the AR signaling inhibitor enzalutamide (ENZ) and the Chk1/2 inhibitor AZD7762 demonstrates synergy with regard to inhibition of AR-CDC6-ATR-Chk1 signaling, ATM phosphorylation induction, and apoptosis in VCaP (mutant p53) and LNCaP-C4-2b (wild-type p53) cells. CDC6 overexpression significantly reduced ENZ- and AZD7762-induced apoptosis. Additive or synergistic therapeutic activities are demonstrated in AR-positive animal xenograft models. These findings have important clinical implications, since they introduce a therapeutic strategy for AR-positive, metastatic, castration-resistant PCa, regardless of p53 status, through targeting AR-CDC6-ATR-Chk1 signaling.

Keywords: ATR; AZD7762; CDC6; Chk1; DNA damage; TOPBP1; androgen receptor; enzalutamide; prostate cancer.

Publication types

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

MeSH terms

  • Androgen Receptor Antagonists / pharmacology*
  • Animals
  • Apoptosis / drug effects
  • Ataxia Telangiectasia Mutated Proteins / metabolism
  • Biomarkers / metabolism
  • Cell Cycle Checkpoints / drug effects
  • Cell Cycle Proteins / metabolism*
  • Cell Line, Tumor
  • Checkpoint Kinase 1 / metabolism*
  • DNA Damage / drug effects
  • DNA Damage / physiology*
  • DNA Replication / drug effects
  • DNA-Binding Proteins / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Nude
  • Nuclear Proteins / metabolism*
  • Phosphorylation / drug effects
  • Prostatic Neoplasms / drug therapy
  • Prostatic Neoplasms / metabolism*
  • Receptors, Androgen / metabolism*
  • Signal Transduction / drug effects
  • Thiophenes / pharmacology
  • Urea / analogs & derivatives
  • Urea / pharmacology

Substances

  • 3-(carbamoylamino)-5-(3-fluorophenyl)-N-(3-piperidyl)thiophene-2-carboxamide
  • AR protein, human
  • Androgen Receptor Antagonists
  • Biomarkers
  • CDC6 protein, human
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Nuclear Proteins
  • Receptors, Androgen
  • Thiophenes
  • Urea
  • ATR protein, human
  • Ataxia Telangiectasia Mutated Proteins
  • CHEK1 protein, human
  • Checkpoint Kinase 1