Galectin-3 Shapes Antitumor Immune Responses by Suppressing CD8+ T Cells via LAG-3 and Inhibiting Expansion of Plasmacytoid Dendritic Cells

Cancer Immunol Res. 2015 Apr;3(4):412-23. doi: 10.1158/2326-6066.CIR-14-0150. Epub 2015 Feb 17.

Abstract

Galectin-3 is a 31-kDa lectin that modulates T-cell responses through several mechanisms, including apoptosis, T-cell receptor (TCR) cross-linking, and TCR downregulation. We found that patients with pancreatic ductal adenocarcinoma (PDA) who responded to a granulocyte-macrophage colony-stimulating factor-secreting allogeneic PDA vaccine developed neutralizing antibodies to galectin-3 after immunization. We show that galectin-3 binds activated antigen-committed CD8(+) T cells only in the tumor microenvironment. Galectin-3-deficient mice exhibit improved CD8(+) T-cell effector function and increased expression of several inflammatory genes. Galectin-3 binds to LAG-3, and LAG-3 expression is necessary for galectin-3-mediated suppression of CD8(+) T cells in vitro. Lastly, galectin-3-deficient mice have elevated levels of circulating plasmacytoid dendritic cells, which are superior to conventional dendritic cells in activating CD8(+) T cells. Thus, inhibiting galectin-3 in conjunction with CD8(+) T-cell-directed immunotherapies should enhance the tumor-specific immune response.

Publication types

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

MeSH terms

  • Animals
  • Antigens, CD / immunology*
  • CD8-Positive T-Lymphocytes / immunology*
  • Cancer Vaccines / immunology
  • Cancer Vaccines / therapeutic use
  • Carcinoma, Pancreatic Ductal / immunology
  • Carcinoma, Pancreatic Ductal / therapy*
  • Cell Differentiation / immunology
  • Dendritic Cells / immunology*
  • Female
  • Galectin 3 / deficiency
  • Galectin 3 / genetics
  • Galectin 3 / immunology*
  • Humans
  • Immune Tolerance
  • Immunophenotyping
  • Interferon-gamma / biosynthesis
  • Lymphocyte Activation / immunology
  • Lymphocyte Activation Gene 3 Protein
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Mice, Knockout
  • Pancreatic Neoplasms / immunology
  • Pancreatic Neoplasms / therapy*

Substances

  • Antigens, CD
  • Cancer Vaccines
  • Galectin 3
  • Interferon-gamma
  • Lymphocyte Activation Gene 3 Protein