Tumors with microsatellite instability upregulate TREX1 to escape antitumor immunity

J Exp Med. 2025 Dec 1;222(12):e20250265. doi: 10.1084/jem.20250265. Epub 2025 Oct 7.

Abstract

Currently, it remains largely unclear how MSI-H/dMMR tumors, despite heightened immune pathway activation and antigenic mutation accumulation, evade immune elimination and promote tumorigenesis. Our study showed that dMMR tumors accumulate cytosolic double-stranded DNA, activating the cGAS-IFN pathway and upregulating DNA-digesting enzyme TREX1. In immunocompetent mice, Trex1 depletion in MSI-H/dMMR tumors abolished tumor formation in a CD8+ T cell-dependent manner, suggesting its critical role in enabling these tumors to evade immune attack. Mechanistically, Trex1 loss amplified tumor-intrinsic cGAS-STING signaling, promoted the activation of CD8+ T cells, and triggered systemic antitumor immunity. Critically, ablating cGAS-STING signaling in MSI-H/dMMR tumors abolished the immune boost from TREX1 deletion, revealing the critical role MSI-H/dMMR tumor-intrinsic cGAS-STING pathway. Furthermore, Trex1 inhibition specifically reduced MSI-H/dMMR tumors growth in vivo, highlighting its clinical potential. Together, we identify the cGAS-STING-TREX1 loop as a key immune escape mechanism in MSI-H/dMMR cancers, suggesting TREX1 inhibition could enhance immunotherapy for these patients.

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Line, Tumor
  • Cyclic Guanosine Monophosphate-Adenosine Monophosphate Synthase
  • Exodeoxyribonucleases* / genetics
  • Exodeoxyribonucleases* / metabolism
  • Humans
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Microsatellite Instability*
  • Neoplasms* / genetics
  • Neoplasms* / immunology
  • Neoplasms* / pathology
  • Nucleotidyltransferases / metabolism
  • Phosphoproteins* / genetics
  • Phosphoproteins* / metabolism
  • Signal Transduction
  • Tumor Escape* / genetics
  • Tumor Escape* / immunology
  • Up-Regulation*

Substances

  • Exodeoxyribonucleases
  • Phosphoproteins
  • Nucleotidyltransferases
  • Membrane Proteins
  • three prime repair exonuclease 1
  • cGAS protein, mouse
  • Cyclic Guanosine Monophosphate-Adenosine Monophosphate Synthase