Disrupting the phase separation of KAT8-IRF1 diminishes PD-L1 expression and promotes antitumor immunity

Nat Cancer. 2023 Mar;4(3):382-400. doi: 10.1038/s43018-023-00522-1. Epub 2023 Mar 9.

Abstract

Immunotherapies targeting the PD-1/PD-L1 axis have become first-line treatments in multiple cancers. However, only a limited subset of individuals achieves durable benefits because of the elusive mechanisms regulating PD-1/PD-L1. Here, we report that in cells exposed to interferon-γ (IFNγ), KAT8 undergoes phase separation with induced IRF1 and forms biomolecular condensates to upregulate PD-L1. Multivalency from both the specific and promiscuous interactions between IRF1 and KAT8 is required for condensate formation. KAT8-IRF1 condensation promotes IRF1 K78 acetylation and binding to the CD247 (PD-L1) promoter and further enriches the transcription apparatus to promote transcription of PD-L1 mRNA. Based on the mechanism of KAT8-IRF1 condensate formation, we identified the 2142-R8 blocking peptide, which disrupts KAT8-IRF1 condensate formation and consequently inhibits PD-L1 expression and enhances antitumor immunity in vitro and in vivo. Our findings reveal a key role of KAT8-IRF1 condensates in PD-L1 regulation and provide a competitive peptide to enhance antitumor immune responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • B7-H1 Antigen* / genetics
  • Cell Line, Tumor
  • Histone Acetyltransferases / metabolism
  • Humans
  • Immunotherapy
  • Interferon Regulatory Factor-1 / genetics
  • Interferon Regulatory Factor-1 / metabolism
  • Interferon-gamma / genetics
  • Interferon-gamma / pharmacology
  • Programmed Cell Death 1 Receptor* / metabolism

Substances

  • B7-H1 Antigen
  • Programmed Cell Death 1 Receptor
  • Interferon-gamma
  • KAT8 protein, human
  • Histone Acetyltransferases
  • IRF1 protein, human
  • Interferon Regulatory Factor-1