Small-molecule GSDMD agonism in tumors stimulates antitumor immunity without toxicity

Cell. 2024 Oct 31;187(22):6165-6181.e22. doi: 10.1016/j.cell.2024.08.007. Epub 2024 Sep 6.

Abstract

Gasdermin-mediated inflammatory cell death (pyroptosis) can activate protective immunity in immunologically cold tumors. Here, we performed a high-throughput screen for compounds that could activate gasdermin D (GSDMD), which is expressed widely in tumors. We identified 6,7-dichloro-2-methylsulfonyl-3-N-tert-butylaminoquinoxaline (DMB) as a direct and selective GSDMD agonist that activates GSDMD pore formation and pyroptosis without cleaving GSDMD. In mouse tumor models, pulsed and low-level pyroptosis induced by DMB suppresses tumor growth without harming GSDMD-expressing immune cells. Protection is immune-mediated and abrogated in mice lacking lymphocytes. Vaccination with DMB-treated cancer cells protects mice from secondary tumor challenge, indicating that immunogenic cell death is induced. DMB treatment synergizes with anti-PD-1. DMB treatment does not alter circulating proinflammatory cytokine or leukocyte numbers or cause weight loss. Thus, our studies reveal a strategy that relies on a low level of tumor cell pyroptosis to induce antitumor immunity and raise the possibility of exploiting pyroptosis without causing overt toxicity.

Keywords: GSDMD; GSDMD agonist; antitumor immunity; cancer; checkpoint blockade; gasdermin; immunogenic cell death; immunotherapy; pyroptosis; tumor.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Female
  • Gasdermins
  • Humans
  • Intracellular Signaling Peptides and Proteins* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Neoplasms / drug therapy
  • Neoplasms / immunology
  • Phosphate-Binding Proteins* / metabolism
  • Programmed Cell Death 1 Receptor / metabolism
  • Pyroptosis* / drug effects
  • Quinoxalines / pharmacology
  • Quinoxalines / therapeutic use
  • Small Molecule Libraries / pharmacology

Substances

  • Phosphate-Binding Proteins
  • Intracellular Signaling Peptides and Proteins
  • Gsdmd protein, mouse
  • GSDMD protein, human
  • Quinoxalines
  • Programmed Cell Death 1 Receptor
  • Small Molecule Libraries
  • Gasdermins