COX2/mPGES1/PGE2 pathway regulates PD-L1 expression in tumor-associated macrophages and myeloid-derived suppressor cells

Proc Natl Acad Sci U S A. 2017 Jan 31;114(5):1117-1122. doi: 10.1073/pnas.1612920114. Epub 2017 Jan 17.

Abstract

In recent years, it has been established that programmed cell death protein ligand 1 (PD-L1)-mediated inhibition of activated PD-1+ T lymphocytes plays a major role in tumor escape from immune system during cancer progression. Lately, the anti-PD-L1 and -PD-1 immune therapies have become an important tool for treatment of advanced human cancers, including bladder cancer. However, the underlying mechanisms of PD-L1 expression in cancer are not fully understood. We found that coculture of murine bone marrow cells with bladder tumor cells promoted strong expression of PD-L1 in bone marrow-derived myeloid cells. Tumor-induced expression of PD-L1 was limited to F4/80+ macrophages and Ly-6C+ myeloid-derived suppressor cells. These PD-L1-expressing cells were immunosuppressive and were capable of eliminating CD8 T cells in vitro. Tumor-infiltrating PD-L1+ cells isolated from tumor-bearing mice also exerted morphology of tumor-associated macrophages and expressed high levels of prostaglandin E2 (PGE2)-forming enzymes microsomal PGE2 synthase 1 (mPGES1) and COX2. Inhibition of PGE2 formation, using pharmacologic mPGES1 and COX2 inhibitors or genetic overexpression of PGE2-degrading enzyme 15-hydroxyprostaglandin dehydrogenase (15-PGDH), resulted in reduced PD-L1 expression. Together, our study demonstrates that the COX2/mPGES1/PGE2 pathway involved in the regulation of PD-L1 expression in tumor-infiltrating myeloid cells and, therefore, reprogramming of PGE2 metabolism in tumor microenvironment provides an opportunity to reduce immune suppression in tumor host.

Keywords: PD-L1; PGE2 metabolism; bone marrow; myeloid cells; tumor-associated macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B7-H1 Antigen / biosynthesis*
  • B7-H1 Antigen / genetics
  • Bone Marrow Cells / metabolism*
  • Cell Communication
  • Cell Line, Tumor
  • Coculture Techniques
  • Cyclooxygenase 2 / physiology*
  • Dinoprostone / physiology*
  • Gene Expression Regulation, Neoplastic
  • Heterografts
  • Humans
  • Hydroxyprostaglandin Dehydrogenases / biosynthesis
  • Hydroxyprostaglandin Dehydrogenases / genetics
  • Macrophages / metabolism*
  • Mice
  • Mice, Inbred C3H
  • Mice, Inbred NOD
  • Mice, SCID
  • Myeloid-Derived Suppressor Cells / metabolism*
  • Prostaglandin Antagonists / pharmacology
  • Prostaglandin-E Synthases / physiology*
  • Urinary Bladder Neoplasms / immunology
  • Urinary Bladder Neoplasms / pathology

Substances

  • B7-H1 Antigen
  • Cd274 protein, mouse
  • Prostaglandin Antagonists
  • Hydroxyprostaglandin Dehydrogenases
  • 15-hydroxyprostaglandin dehydrogenase
  • Ptgs2 protein, mouse
  • Cyclooxygenase 2
  • Prostaglandin-E Synthases
  • Dinoprostone