Intermittent MEK Inhibition with GITR Costimulation Rescues T-cell Function for Increased Efficacy with CTLA-4 Blockade in Solid Tumor Models

Cancer Immunol Res. 2024 Oct 1;12(10):1392-1408. doi: 10.1158/2326-6066.CIR-23-0729.

Abstract

MEK inhibitors (MEKi) have shown limited success as a treatment for MAPK/ERK pathway-dependent cancers due to various resistance mechanisms tumor cells can employ. CH5126766 (CKI27) is an inhibitor that binds to MEK and prevents release of RAF, reducing the relief of negative feedback commonly observed with other MEKis. We observed that CKI27 increased MHC expression in tumor cells and improved T cell-mediated killing. Yet, CKI27 also decreased T-cell proliferation, activation, and cytolytic activity by inhibiting the MAPK/ERK pathway that is activated downstream of T-cell receptor signaling. Therefore, we aimed to balance the positive and negative immunomodulatory effects of MEKis for optimal combination with immunotherapy. Intermittent administration of CKI27 allowed T cells to partially recover and costimulation via GITR and OX-40 agonist antibodies completely alleviated inhibition of function. In Kras mutant lung and colon tumor mouse models, intermittent CKI27 and anti-GITR significantly decreased tumor growth and prolonged survival when further combined with CTLA-4 immune checkpoint blockade. Moreover, this triple combination increased CD8+ and CD4+ T-cell proliferation, activation, and effector/memory subsets in the tumor-draining lymph nodes and tumors and led to intratumoral regulatory T-cell destabilization. These data, collectively, will allow for more informed decisions when optimizing combination regimens by overcoming resistance, reducing toxicity, and generating long-term immune responses.

MeSH terms

  • Animals
  • CTLA-4 Antigen* / antagonists & inhibitors
  • Cell Line, Tumor
  • Colonic Neoplasms / drug therapy
  • Colonic Neoplasms / immunology
  • Colonic Neoplasms / pathology
  • Colonic Neoplasms / therapy
  • Disease Models, Animal
  • Female
  • Glucocorticoid-Induced TNFR-Related Protein* / antagonists & inhibitors
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Neoplasms / drug therapy
  • Neoplasms / immunology
  • Neoplasms / therapy
  • Protein Kinase Inhibitors / pharmacology
  • Protein Kinase Inhibitors / therapeutic use
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism

Substances

  • Glucocorticoid-Induced TNFR-Related Protein
  • CTLA-4 Antigen
  • Protein Kinase Inhibitors
  • Tnfrsf18 protein, mouse
  • Immune Checkpoint Inhibitors