A hormone-DNA repair circuit governs the response to genotoxic insult

Cancer Discov. 2013 Nov;3(11):1254-71. doi: 10.1158/2159-8290.CD-13-0108. Epub 2013 Sep 11.

Abstract

Alterations in DNA repair promote tumor development, but the impact on tumor progression is poorly understood. Here, discovery of a biochemical circuit linking hormone signaling to DNA repair and therapeutic resistance is reported. Findings show that androgen receptor (AR) activity is induced by DNA damage and promotes expression and activation of a gene expression program governing DNA repair. Subsequent investigation revealed that activated AR promotes resolution of double-strand breaks and resistance to DNA damage both in vitro and in vivo. Mechanistically, DNA-dependent protein kinase catalytic subunit (DNAPKcs) was identified as a key target of AR after damage, controlling AR-mediated DNA repair and cell survival after genotoxic insult. Finally, DNAPKcs was shown to potentiate AR function, consistent with a dual role in both DNA repair and transcriptional regulation. Combined, these studies identify the AR-DNAPKcs circuit as a major effector of DNA repair and therapeutic resistance and establish a new node for therapeutic intervention in advanced disease.

Significance: The present study identifies for the fi rst time a positive feedback circuit linking hormone action to the DNA damage response and shows the significant impact of this process on tumor progression and therapeutic response. These provocative findings provide the foundation for development of novel nodes of therapeutic intervention for advanced disease.

Publication types

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

MeSH terms

  • Androgen Antagonists / pharmacology
  • Animals
  • Antineoplastic Agents, Hormonal / pharmacology
  • Cell Line, Tumor
  • Cell Survival / genetics
  • DNA Damage / genetics
  • DNA Damage / radiation effects*
  • DNA Repair* / drug effects
  • DNA-Activated Protein Kinase / genetics
  • DNA-Activated Protein Kinase / metabolism*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drug Resistance, Neoplasm / genetics*
  • Feedback, Physiological
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Male
  • Mice
  • Mice, Nude
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / pathology*
  • Prostatic Neoplasms / therapy
  • Receptors, Androgen / genetics
  • Receptors, Androgen / metabolism*
  • Signal Transduction / genetics
  • Xenograft Model Antitumor Assays

Substances

  • Androgen Antagonists
  • Antineoplastic Agents, Hormonal
  • DNA-Binding Proteins
  • Nuclear Proteins
  • Receptors, Androgen
  • DNA-Activated Protein Kinase
  • PRKDC protein, human
  • Prkdc protein, mouse