Sialic Acid-Dependent Inhibition of T Cells by Exosomal Ganglioside GD3 in Ovarian Tumor Microenvironments

J Immunol. 2018 Dec 15;201(12):3750-3758. doi: 10.4049/jimmunol.1801041. Epub 2018 Nov 16.

Abstract

The tumor microenvironment is rendered immunosuppressive by a variety of cellular and acellular factors that represent potential cancer therapeutic targets. Although exosomes isolated from ovarian tumor ascites fluids have been previously reported to induce a rapid and reversible T cell arrest, the factors present on or within exosomes that contribute to immunosuppression have not been fully defined. In this study, we establish that GD3, a ganglioside expressed on the surface of exosomes isolated from human ovarian tumor ascites fluids, is causally linked to the functional arrest of T cells activated through their TCR. This arrest is inhibited by Ab blockade of exosomal GD3 or by the removal of GD3+ exosomes. Empty liposomes expressing GD3 on the surface also inhibit the activation of T cells, establishing that GD3 contributes to the functional arrest of T cells independent of factors present in exosomes. Finally, we demonstrate that the GD3-mediated arrest of the TCR activation is dependent upon sialic acid groups, because their enzymatic removal from exosomes or liposomes results in a loss of inhibitory capacity. Collectively, these data define GD3 as a potential immunotherapeutic target.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Ascites
  • Ascitic Fluid / metabolism*
  • Cells, Cultured
  • Exosomes / metabolism*
  • Female
  • Gangliosides / metabolism*
  • Humans
  • Immune Tolerance
  • Immunotherapy / methods*
  • N-Acetylneuraminic Acid / metabolism*
  • NF-kappa B / metabolism
  • Neoplasm Staging
  • Ovarian Neoplasms / immunology
  • Ovarian Neoplasms / metabolism*
  • T-Lymphocytes / immunology*
  • Tumor Microenvironment

Substances

  • Gangliosides
  • NF-kappa B
  • ganglioside, GD3
  • N-Acetylneuraminic Acid