Oncogenic KRAS drives immunosuppression of colorectal cancer by impairing DDX60-mediated dsRNA accumulation and viral mimicry

Sci Immunol. 2024 Oct 4;9(100):eado8758. doi: 10.1126/sciimmunol.ado8758. Epub 2024 Oct 4.

Abstract

The interferon (IFN) response is vital for the effectiveness of immune checkpoint inhibition (ICI) therapy. Our previous research showed that KRAS (Kirsten rat sarcoma viral) mutation impairs the IFN response in colorectal cancer (CRC), with an unclear mechanism. Here, we demonstrate that KRAS accelerates double-stranded RNA (dsRNA) degradation, impairing dsRNA sensing and IFN response by down-regulating DExD/H-box helicase 6 (DDX60). DDX60 was identified as a KRAS target here and could bind to dsRNAs to protect against RNA-induced silencing complex (RISC)-mediated degradation. Overexpressing DDX60 induced dsRNA accumulation, reactivated IFN signaling, and increased CRC sensitivity to ICI therapy. Mechanistically, KRAS engaged the AKT (also known as protein kinase B)-GSK3β (glycogen synthase kinase-3 beta) pathway to suppress STAT3 phosphorylation, thereby inhibiting STAT3-driven DDX60 transcription. Our findings reveal a role for KRAS in dsRNA homeostasis, suggesting potential strategies to convert "cold" tumors to "hot" and to overcome ICI resistance in CRC with KRAS mutations.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Colorectal Neoplasms* / genetics
  • Colorectal Neoplasms* / immunology
  • DEAD-box RNA Helicases* / genetics
  • DEAD-box RNA Helicases* / metabolism
  • Female
  • Humans
  • Mice
  • Proto-Oncogene Proteins p21(ras)* / genetics
  • Proto-Oncogene Proteins p21(ras)* / immunology
  • RNA, Double-Stranded* / immunology

Substances

  • DEAD-box RNA Helicases
  • KRAS protein, human
  • Proto-Oncogene Proteins p21(ras)
  • RNA, Double-Stranded
  • DDX60 protein, human