Synthetic lethality in ATM-deficient RAD50-mutant tumors underlies outlier response to cancer therapy

Cancer Discov. 2014 Sep;4(9):1014-21. doi: 10.1158/2159-8290.CD-14-0380. Epub 2014 Jun 16.

Abstract

Metastatic solid tumors are almost invariably fatal. Patients with disseminated small-cell cancers have a particularly unfavorable prognosis, with most succumbing to their disease within two years. Here, we report on the genetic and functional analysis of an outlier curative response of a patient with metastatic small-cell cancer to combined checkpoint kinase 1 (CHK1) inhibition and DNA-damaging chemotherapy. Whole-genome sequencing revealed a clonal hemizygous mutation in the Mre11 complex gene RAD50 that attenuated ATM signaling which in the context of CHK1 inhibition contributed, via synthetic lethality, to extreme sensitivity to irinotecan. As Mre11 mutations occur in a diversity of human tumors, the results suggest a tumor-specific combination therapy strategy in which checkpoint inhibition in combination with DNA-damaging chemotherapy is synthetically lethal in tumor cells but not normal cells with somatic mutations that impair Mre11 complex function.

Significance: Strategies to effect deep and lasting responses to cancer therapy in patients with metastatic disease have remained difficult to attain, especially in early-phase clinical trials. Here, we present an in-depth genomic and functional genetic analysis identifying RAD50 hypomorphism as a contributing factor to a curative response to systemic combination therapy in a patient with recurrent, metastatic small-cell cancer.

Publication types

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

MeSH terms

  • Acid Anhydride Hydrolases
  • Amino Acid Sequence
  • Ataxia Telangiectasia Mutated Proteins / deficiency*
  • Ataxia Telangiectasia Mutated Proteins / genetics
  • DNA Copy Number Variations
  • DNA Damage
  • DNA Repair Enzymes / chemistry
  • DNA Repair Enzymes / genetics*
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / genetics*
  • Enzyme Activation
  • Genomics
  • Humans
  • Models, Molecular
  • Molecular Sequence Data
  • Mutation*
  • Neoplasm Metastasis
  • Neoplasms / genetics*
  • Neoplasms / metabolism
  • Neoplasms / pathology
  • Neoplasms / therapy
  • Phosphorylation
  • Protein Conformation
  • Sequence Alignment
  • Treatment Outcome

Substances

  • DNA-Binding Proteins
  • Ataxia Telangiectasia Mutated Proteins
  • Acid Anhydride Hydrolases
  • RAD50 protein, human
  • DNA Repair Enzymes