In vivo vulnerabilities to GPX4 and HDAC inhibitors in drug-persistent versus drug-resistant BRAFV600E lung adenocarcinoma

Cell Rep Med. 2024 Aug 20;5(8):101663. doi: 10.1016/j.xcrm.2024.101663. Epub 2024 Aug 1.

Abstract

The current targeted therapy for BRAFV600E-mutant lung cancer consists of a dual blockade of RAF/MEK kinases often combining dabrafenib/trametinib (D/T). This regimen extends survival when compared to single-agent treatments, but disease progression is unavoidable. By using whole-genome CRISPR screening and RNA sequencing, we characterize the vulnerabilities of both persister and D/T-resistant cellular models. Oxidative stress together with concomitant induction of antioxidant responses is boosted by D/T treatment. However, the nature of the oxidative damage, the choice of redox detoxification systems, and the resulting therapeutic vulnerabilities display stage-specific differences. Persister cells suffer from lipid peroxidation and are sensitive to ferroptosis upon GPX4 inhibition in vivo. Biomarkers of lipid peroxidation are detected in clinical samples following D/T treatment. Acquired alterations leading to mitogen-activated protein kinase (MAPK) reactivation enhance cystine transport to boost GPX4-independent antioxidant responses. Similarly to BRAFV600E-mutant melanoma, histone deacetylase (HDAC) inhibitors decrease D/T-resistant cell viability and extend therapeutic response in vivo.

Keywords: BRAF oncogene; GPX4 inhibition; HDAC inhibition; ferroptosis; lung adenocarcinoma; persister cells; targeted therapy.

MeSH terms

  • Adenocarcinoma of Lung* / drug therapy
  • Adenocarcinoma of Lung* / genetics
  • Adenocarcinoma of Lung* / metabolism
  • Adenocarcinoma of Lung* / pathology
  • Animals
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm* / drug effects
  • Drug Resistance, Neoplasm* / genetics
  • Ferroptosis / drug effects
  • Ferroptosis / genetics
  • Histone Deacetylase Inhibitors* / pharmacology
  • Humans
  • Imidazoles / pharmacology
  • Lipid Peroxidation / drug effects
  • Lung Neoplasms* / drug therapy
  • Lung Neoplasms* / genetics
  • Lung Neoplasms* / metabolism
  • Lung Neoplasms* / pathology
  • Mice
  • Mutation / genetics
  • Oxidative Stress / drug effects
  • Oximes / pharmacology
  • Phospholipid Hydroperoxide Glutathione Peroxidase* / genetics
  • Phospholipid Hydroperoxide Glutathione Peroxidase* / metabolism
  • Proto-Oncogene Proteins B-raf* / antagonists & inhibitors
  • Proto-Oncogene Proteins B-raf* / genetics
  • Proto-Oncogene Proteins B-raf* / metabolism
  • Pyridones / pharmacology
  • Pyrimidinones / pharmacology
  • Xenograft Model Antitumor Assays

Substances

  • Proto-Oncogene Proteins B-raf
  • Phospholipid Hydroperoxide Glutathione Peroxidase
  • Histone Deacetylase Inhibitors
  • Oximes
  • Imidazoles
  • dabrafenib
  • Pyridones
  • trametinib
  • BRAF protein, human
  • Pyrimidinones