Caspase-1-dependent spatiality in triple-negative breast cancer and response to immunotherapy

Nat Commun. 2024 Oct 1;15(1):8514. doi: 10.1038/s41467-024-52553-6.

Abstract

Tumor immune microenvironment (TIME) spatial organization predicts outcome and therapy response in triple-negative breast cancer (TNBC). An immunosuppressive TIME containing elevated tumor-associated macrophages (TAM) and scarce CD8+ T cells is associated with poor outcome, but the regulatory mechanisms are poorly understood. Here we show that ETS1-driven caspase-1 expression, required for IL1β processing and TAM recruitment, is negatively regulated by estrogen receptors alpha (ERα) and a defining feature of TNBC. Elevated tumoral caspase-1 is associated with a distinct TIME characterized by increased pro-tumoral TAMs and CD8+ T cell exclusion from tumor nests. Mouse models prove the functional importance of ERα, ETS1, caspase-1 and IL1β in TIME conformation. Caspase-1 inhibition induces an immunoreactive TIME and reverses resistance to immune checkpoint blockade, identifying a therapeutically targetable mechanism that governs TNBC spatial organization.

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Caspase 1* / metabolism
  • Cell Line, Tumor
  • Estrogen Receptor alpha / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Immunotherapy* / methods
  • Interleukin-1beta / metabolism
  • Mice
  • Proto-Oncogene Protein c-ets-1 / genetics
  • Proto-Oncogene Protein c-ets-1 / metabolism
  • Triple Negative Breast Neoplasms* / genetics
  • Triple Negative Breast Neoplasms* / immunology
  • Triple Negative Breast Neoplasms* / metabolism
  • Triple Negative Breast Neoplasms* / therapy
  • Tumor Microenvironment / immunology
  • Tumor-Associated Macrophages* / immunology
  • Tumor-Associated Macrophages* / metabolism

Substances

  • Caspase 1
  • ESR1 protein, human
  • Estrogen Receptor alpha
  • ETS1 protein, human
  • Immune Checkpoint Inhibitors
  • Interleukin-1beta
  • Proto-Oncogene Protein c-ets-1