Tumor cell-intrinsic EPHA2 suppresses anti-tumor immunity by regulating PTGS2 (COX-2)

J Clin Invest. 2019 Jun 4;129(9):3594-3609. doi: 10.1172/JCI127755.

Abstract

Resistance to immunotherapy is one of the biggest problems of current oncotherapeutics. WhileT cell abundance is essential for tumor responsiveness to immunotherapy, factors that define the T cell inflamed tumor microenvironment are not fully understood. We conducted an unbiased approach to identify tumor-intrinsic mechanisms shaping the immune tumor microenvironment(TME), focusing on pancreatic adenocarcinoma because it is refractory to immunotherapy and excludes T cells from the TME. From human tumors, we identified EPHA2 as a candidate tumor intrinsic driver of immunosuppression. Epha2 deletion reversed T cell exclusion and sensitized tumors to immunotherapy. We found that PTGS2, the gene encoding cyclooxygenase-2, lies downstream of EPHA2 signaling through TGFβ and is associated with poor patient survival. Ptgs2 deletion reversed T cell exclusion and sensitized tumors to immunotherapy; pharmacological inhibition of PTGS2 was similarly effective. Thus, EPHA2-PTGS2 signaling in tumor cells regulates tumor immune phenotypes; blockade may represent a novel therapeutic avenue for immunotherapy-refractory cancers. Our findings warrant clinical trials testing the effectiveness of therapies combining EPHA2-TGFβ-PTGS2 pathway inhibitors with anti-tumor immunotherapy, and may change the treatment of notoriously therapy-resistant pancreatic adenocarcinoma.

Keywords: Immunology; Oncology; Pharmacology.

Publication types

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

MeSH terms

  • Adenocarcinoma / immunology
  • Adenocarcinoma / therapy
  • Animals
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Line
  • Cyclooxygenase 2 / metabolism*
  • Ephrin-A2 / metabolism*
  • Female
  • Gene Deletion
  • Humans
  • Immunosuppression Therapy
  • Immunotherapy
  • Inflammation
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Pancreatic Neoplasms / immunology*
  • Pancreatic Neoplasms / therapy
  • Receptor, EphA2
  • Transforming Growth Factor beta / metabolism*

Substances

  • EPHA2 protein, human
  • Ephrin-A2
  • Transforming Growth Factor beta
  • Ptgs2 protein, mouse
  • Cyclooxygenase 2
  • PTGS2 protein, human
  • Receptor, EphA2