Increase of Tumor Infiltrating γδ T-cells in Pancreatic Ductal Adenocarcinoma Through Remodeling of the Extracellular Matrix by a Hyaluronan Synthesis Suppressor, 4-Methylumbelliferone

Pancreas. 2019 Feb;48(2):292-298. doi: 10.1097/MPA.0000000000001211.

Abstract

Objectives: Desmoplastic changes of extracellular matrix (ECM) containing large amounts of hyaluronan (HA) are of interest in chemo- and immunoresistance of pancreatic ductal adenocarcinoma (PDAC). The goal of this study was to evaluate the effects of 4-methylumbelliferone (MU), a selective inhibitor of HA, on ECM and to examine how MU affects adoptive immunotherapy.

Methods: The effect of MU on cell proliferation, HA synthesis and formation of ECM were investigated in four PDAC cell lines. In addition, the cytotoxicity of γδ T-cell-rich peripheral blood mononuclear cells (PBMCs) collected from healthy donors and stimulated with zoledronate and interleukin-2 was examined in the presence of MU. The amount of HA and tumor-infiltrating lymphocytes were also investigated in mice xenograft models.

Results: In vitro, 1.0 mM MU inhibited cell proliferation by 45-70% and HA synthesis by 55-80% in all four PDAC cell lines, and enhanced γδ T-cell-rich PBMC-mediated cytotoxicity against PDAC cells. In vivo, MU reduced intratumoral HA and promoted infiltration of inoculated γδ T-cells into tumor tissue, and consequently suppressed tumor growth.

Conclusions: 4-methylumbelliferone may be an effective immunosensitizer against PDAC through induction of structural changes in the ECM.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma, Pancreatic Ductal / drug therapy
  • Carcinoma, Pancreatic Ductal / immunology*
  • Carcinoma, Pancreatic Ductal / pathology
  • Cell Line, Tumor
  • Extracellular Matrix / drug effects
  • Extracellular Matrix / immunology
  • Extracellular Matrix / metabolism
  • Humans
  • Hyaluronic Acid / metabolism
  • Hymecromone / pharmacology
  • Interleukin-2 / pharmacology
  • Intraepithelial Lymphocytes / drug effects
  • Intraepithelial Lymphocytes / immunology*
  • Intraepithelial Lymphocytes / metabolism
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / immunology
  • Leukocytes, Mononuclear / metabolism
  • Lymphocytes, Tumor-Infiltrating / drug effects
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Lymphocytes, Tumor-Infiltrating / metabolism
  • Mice, Inbred NOD
  • Mice, SCID
  • Pancreatic Neoplasms / drug therapy
  • Pancreatic Neoplasms / immunology*
  • Pancreatic Neoplasms / pathology
  • Xenograft Model Antitumor Assays / methods
  • Zoledronic Acid / pharmacology

Substances

  • Interleukin-2
  • Hymecromone
  • Zoledronic Acid
  • Hyaluronic Acid