Synthetic lethal CRISPR screen identifies a cancer cell-intrinsic role of PD-L1 in regulation of vulnerability to ferroptosis

Cell Rep. 2024 Jul 23;43(7):114477. doi: 10.1016/j.celrep.2024.114477. Epub 2024 Jul 11.

Abstract

Despite the success of programmed cell death 1 (PD-1)/programmed death ligand 1 (PD-L1) inhibition in tumor therapy, many patients do not benefit. This failure may be attributed to the intrinsic functions of PD-L1. We perform a genome-wide CRISPR synthetic lethality screen to systematically explore the intrinsic functions of PD-L1 in head and neck squamous cell carcinoma (HNSCC) cells, identifying ferroptosis-related genes as essential for the viability of PD-L1-deficient cells. Genetic and pharmacological induction of ferroptosis accelerates cell death in PD-L1 knockout cells, which are also more susceptible to immunogenic ferroptosis. Mechanistically, nuclear PD-L1 transcriptionally activates SOD2 to maintain redox homeostasis. Lower reactive oxygen species (ROS) and ferroptosis are observed in patients with HNSCC who have higher PD-L1 expression. Our study illustrates that PD-L1 confers ferroptosis resistance in HNSCC cells by activating the SOD2-mediated antioxidant pathway, suggesting that targeting the intrinsic functions of PD-L1 could enhance therapeutic efficacy.

Keywords: CP: Cancer; PD-L1; ROS; SOD2; cell death; ferroptosis; genome-wide CRISPR synthetic lethality screen; immunotherapy; intrinsic function of PD-L1; reactive oxygen species; redox homeostasis.

MeSH terms

  • Animals
  • B7-H1 Antigen* / genetics
  • B7-H1 Antigen* / metabolism
  • CRISPR-Cas Systems
  • Cell Line, Tumor
  • Clustered Regularly Interspaced Short Palindromic Repeats
  • Ferroptosis*
  • Gene Expression Regulation, Neoplastic
  • Head and Neck Neoplasms / genetics
  • Head and Neck Neoplasms / metabolism
  • Head and Neck Neoplasms / pathology
  • Humans
  • Mice
  • Reactive Oxygen Species / metabolism
  • Squamous Cell Carcinoma of Head and Neck / genetics
  • Squamous Cell Carcinoma of Head and Neck / metabolism
  • Squamous Cell Carcinoma of Head and Neck / pathology
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase / metabolism
  • Synthetic Lethal Mutations

Substances

  • B7-H1 Antigen
  • CD274 protein, human
  • Reactive Oxygen Species
  • Superoxide Dismutase
  • superoxide dismutase 2