Activating Immune Recognition in Pancreatic Ductal Adenocarcinoma via Autophagy Inhibition, MEK Blockade, and CD40 Agonism

Gastroenterology. 2022 Feb;162(2):590-603.e14. doi: 10.1053/j.gastro.2021.09.066. Epub 2021 Oct 8.

Abstract

Background and aims: Patients with pancreatic ductal adenocarcinoma (PDA) have not yet benefitted from the revolution in cancer immunotherapy due in large part to a dominantly immunosuppressive tumor microenvironment. MEK inhibition combined with autophagy inhibition leads to transient tumor responses in some patients with PDA. We examined the functional effects of combined MEK and autophagy inhibition on the PDA immune microenvironment and the synergy of combined inhibition of MEK and autophagy with CD40 agonism (aCD40) against PDA using immunocompetent model systems.

Methods: We implanted immunologically "cold" murine PDA cells orthotopically in wide type C57BL/6J mice. We administered combinations of inhibitors of MEK1/2, inhibitors of autophagy, and aCD40 and measured anticancer efficacy and immune sequelae using mass cytometry and multiplexed immunofluorescence imaging analysis to characterize the tumor microenvironment. We also used human and mouse PDA cell lines and human macrophages in vitro to perform functional assays to elucidate the cellular effects induced by the treatments.

Results: We find that coinhibition of MEK (using cobimetinib) and autophagy (using mefloquine), but not either treatment alone, activates the STING/type I interferon pathway in tumor cells that in turn activates paracrine tumor associated macrophages toward an immunogenic M1-like phenotype. This switch is further augmented by aCD40. Triple therapy (cobimetinib + mefloquine + aCD40) achieved cytotoxic T-cell activation in an immunologically "cold" mouse PDA model, leading to enhanced antitumor immunity.

Conclusions: MEK and autophagy coinhibition coupled with aCD40 invokes immune repolarization and is an attractive therapeutic approach for PDA immunotherapy development.

Keywords: Autophagy; CD40 Agonism; MAPK Pathway; Macrophage Polarization; Pancreatic Ductal Adenocarcinoma.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy / drug effects
  • Autophagy / immunology*
  • Azetidines / pharmacology*
  • CD40 Antigens / agonists*
  • Carcinoma, Pancreatic Ductal / immunology*
  • Cell Line, Tumor
  • Drug Synergism
  • Humans
  • Hydroxychloroquine / pharmacology
  • Immunotherapy
  • Interferon Type I / drug effects
  • Interferon Type I / immunology
  • MAP Kinase Kinase 1 / antagonists & inhibitors
  • MAP Kinase Kinase 2 / antagonists & inhibitors
  • Macrophages
  • Mefloquine / pharmacology*
  • Membrane Proteins / drug effects
  • Membrane Proteins / immunology
  • Mice
  • Pancreatic Neoplasms / immunology*
  • Paracrine Communication / drug effects
  • Paracrine Communication / immunology
  • Piperidines / pharmacology*
  • Protein Kinase Inhibitors / pharmacology*
  • Tumor Escape
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / immunology*
  • Tumor-Associated Macrophages / drug effects
  • Tumor-Associated Macrophages / immunology*

Substances

  • Azetidines
  • CD40 Antigens
  • Interferon Type I
  • Membrane Proteins
  • Piperidines
  • Protein Kinase Inhibitors
  • STING1 protein, human
  • Sting1 protein, mouse
  • Hydroxychloroquine
  • MAP Kinase Kinase 1
  • MAP Kinase Kinase 2
  • cobimetinib
  • Mefloquine