SMARCAL1 is a dual regulator of innate immune signaling and PD-L1 expression that promotes tumor immune evasion

Cell. 2024 Feb 15;187(4):861-881.e32. doi: 10.1016/j.cell.2024.01.008. Epub 2024 Jan 31.

Abstract

Genomic instability can trigger cancer-intrinsic innate immune responses that promote tumor rejection. However, cancer cells often evade these responses by overexpressing immune checkpoint regulators, such as PD-L1. Here, we identify the SNF2-family DNA translocase SMARCAL1 as a factor that favors tumor immune evasion by a dual mechanism involving both the suppression of innate immune signaling and the induction of PD-L1-mediated immune checkpoint responses. Mechanistically, SMARCAL1 limits endogenous DNA damage, thereby suppressing cGAS-STING-dependent signaling during cancer cell growth. Simultaneously, it cooperates with the AP-1 family member JUN to maintain chromatin accessibility at a PD-L1 transcriptional regulatory element, thereby promoting PD-L1 expression in cancer cells. SMARCAL1 loss hinders the ability of tumor cells to induce PD-L1 in response to genomic instability, enhances anti-tumor immune responses and sensitizes tumors to immune checkpoint blockade in a mouse melanoma model. Collectively, these studies uncover SMARCAL1 as a promising target for cancer immunotherapy.

Keywords: AP-1; CRISPR-Cas9 screens; DNA damage response; JUN; PD-L1 regulation; SMARCAL1; cGAS-STING pathway; cancer immunotherapy; cancer-intrinsic innate immunity.

MeSH terms

  • Animals
  • B7-H1 Antigen* / metabolism
  • DNA Helicases* / metabolism
  • Genomic Instability
  • Immunity, Innate*
  • Melanoma* / immunology
  • Melanoma* / metabolism
  • Mice
  • Tumor Escape*

Substances

  • B7-H1 Antigen
  • Smarcal1 protein, mouse
  • DNA Helicases