Therapeutic targeting of ATR yields durable regressions in small cell lung cancers with high replication stress

Cancer Cell. 2021 Apr 12;39(4):566-579.e7. doi: 10.1016/j.ccell.2021.02.014.

Abstract

Small cell neuroendocrine cancers (SCNCs) are recalcitrant cancers arising from diverse primary sites that lack effective treatments. Using chemical genetic screens, we identified inhibition of ataxia telangiectasia and rad3 related (ATR), the primary activator of the replication stress response, and topoisomerase I (TOP1), nuclear enzyme that suppresses genomic instability, as synergistically cytotoxic in small cell lung cancer (SCLC). In a proof-of-concept study, we combined M6620 (berzosertib), first-in-class ATR inhibitor, and TOP1 inhibitor topotecan in patients with relapsed SCNCs. Objective response rate among patients with SCLC was 36% (9/25), achieving the primary efficacy endpoint. Durable tumor regressions were observed in patients with platinum-resistant SCNCs, typically fatal within weeks of recurrence. SCNCs with high neuroendocrine differentiation, characterized by enhanced replication stress, were more likely to respond. These findings highlight replication stress as a potentially transformative vulnerability of SCNCs, paving the way for rational patient selection in these cancers, now treated as a single disease.

Keywords: DNA damage response; DNA topoisomerases; SCLC; ataxia telangiectasia mutated and rad3 related; cell-cycle checkpoints; replication stress; small cell neuroendocrine cancers; translational research.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Aged
  • Antineoplastic Agents / pharmacology
  • Ataxia Telangiectasia Mutated Proteins / genetics
  • Ataxia Telangiectasia Mutated Proteins / metabolism*
  • DNA Replication / drug effects
  • DNA Topoisomerases, Type I / genetics
  • Genomic Instability / genetics
  • Humans
  • Isoxazoles / pharmacology*
  • Lung Neoplasms / drug therapy*
  • Lung Neoplasms / metabolism
  • Middle Aged
  • Neoplasm Recurrence, Local / drug therapy*
  • Neoplasm Recurrence, Local / metabolism
  • Protein Kinase Inhibitors / pharmacology
  • Pyrazines / pharmacology*
  • Signal Transduction / drug effects
  • Small Cell Lung Carcinoma / drug therapy*
  • Small Cell Lung Carcinoma / metabolism

Substances

  • Antineoplastic Agents
  • Isoxazoles
  • Protein Kinase Inhibitors
  • Pyrazines
  • ATR protein, human
  • Ataxia Telangiectasia Mutated Proteins
  • DNA Topoisomerases, Type I
  • berzosertib