A STAT3-STING-IFN axis controls the metastatic spread of small cell lung cancer

Nat Immunol. 2024 Dec;25(12):2259-2269. doi: 10.1038/s41590-024-02014-5. Epub 2024 Nov 21.

Abstract

Small cell lung cancer (SCLC) is an aggressive neuroendocrine tumor characterized by a high metastatic potential with an overall survival rate of ~5%. The transcription factor signal transducer and activator of transcription 3 (STAT3) is overexpressed by >50% of tumors, including SCLC, but its role in SCLC development and metastasis is unclear. Here, we show that, while STAT3 deletion restricts primary tumor growth, it paradoxically enhances metastatic spread by promoting immune evasion. This occurs because STAT3 is crucial for maintaining the immune sensor stimulator of interferon (IFN) genes (STING). Without STAT3, the cyclic adenosine monophosphate-guanosine monophosphate synthase-STING pathway is inactive, resulting in decreased type I IFN secretion and an IFN gene signature. Importantly, restoration of IFN signaling through re-expression of endogenous STING, enforced expression of IFN response factor 7 or administration of recombinant type I IFN re-established antitumor immunity, inhibiting metastatic SCLC in vivo. These data show the potential of augmenting the innate immune response to block metastatic SCLC.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Humans
  • Immunity, Innate
  • Interferon Type I / metabolism
  • Lung Neoplasms* / genetics
  • Lung Neoplasms* / immunology
  • Lung Neoplasms* / pathology
  • Lung Neoplasms* / secondary
  • Membrane Proteins* / genetics
  • Membrane Proteins* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasm Metastasis
  • STAT3 Transcription Factor* / genetics
  • STAT3 Transcription Factor* / metabolism
  • Signal Transduction*
  • Small Cell Lung Carcinoma* / genetics
  • Small Cell Lung Carcinoma* / immunology
  • Small Cell Lung Carcinoma* / metabolism
  • Small Cell Lung Carcinoma* / pathology
  • Tumor Escape

Substances

  • STAT3 Transcription Factor
  • Membrane Proteins
  • Interferon Type I
  • Sting1 protein, mouse
  • Stat3 protein, mouse