Somatic BRCA1/2 Recovery as a Resistance Mechanism After Exceptional Response to Poly (ADP-ribose) Polymerase Inhibition

J Clin Oncol. 2017 Apr 10;35(11):1240-1249. doi: 10.1200/JCO.2016.71.3677. Epub 2017 Feb 21.

Abstract

Purpose Durable and long-term responses to the poly (ADP-ribose) polymerase inhibitor olaparib are observed in patients without BRCA1/2 mutations. However, beyond BRCA1/2 mutations, there are no approved biomarkers for olaparib in high-grade serous ovarian cancer (HGSOC). To determine mechanisms of durable response and resistance to olaparib therapy, we performed an analysis of HGSOC tumors from three patients without germline BRCA1/2 mutations who experienced exceptional responses to olaparib. Patients and Methods We performed integrated exome, low-pass genome, and RNA sequence analysis of tumors at diagnosis and upon relapse from patients with platinum-sensitive HGSOC recurrence who were treated > 5 years with olaparib therapy as a single agent. Results We observed somatic disruption of BRCA1/2 in all three patients at diagnosis, followed by subsequent BRCA recovery upon progression by copy number gain and/or upregulation of the remaining functional allele in two patients. The third patient with ongoing response (> 7 years) had a tumor at diagnosis with biallelic somatic deletion and loss-of-function mutation, thereby lacking a functional allele for recovery of BRCA1 activity and indicating a potential cure. Conclusion Olaparib has durable benefit for patients with ovarian cancer beyond germline BRCA1/2 carriers. These data suggest that biallelic loss of BRCA1/2 in cancer cells may be a potential marker of long-term response to poly (ADP-ribose) polymerase inhibition and that restoration of homologous repair function may be a mechanism of disease resistance.

Publication types

  • Case Reports

MeSH terms

  • Aged
  • Alleles
  • Antineoplastic Agents / therapeutic use*
  • DNA Mutational Analysis
  • Drug Resistance, Neoplasm / genetics*
  • Exome
  • Female
  • Gene Dosage
  • Gene Expression
  • Genes, BRCA1*
  • Genes, BRCA2*
  • Humans
  • Middle Aged
  • Neoplasm Grading
  • Ovarian Neoplasms / chemistry
  • Ovarian Neoplasms / drug therapy*
  • Ovarian Neoplasms / genetics*
  • Ovarian Neoplasms / pathology
  • Phthalazines / therapeutic use*
  • Piperazines / therapeutic use*
  • Poly(ADP-ribose) Polymerase Inhibitors / therapeutic use*
  • Recombinational DNA Repair
  • Sequence Analysis, RNA
  • Treatment Outcome
  • Up-Regulation

Substances

  • Antineoplastic Agents
  • Phthalazines
  • Piperazines
  • Poly(ADP-ribose) Polymerase Inhibitors
  • olaparib