Zoledronate sensitizes neuroblastoma-derived tumor-initiating cells to cytolysis mediated by human γδ T cells

J Immunother. 2012 Oct;35(8):598-606. doi: 10.1097/CJI.0b013e31826a745a.

Abstract

Neuroblastoma is the most common extracranial solid tumor in children that is refractory to intensive multimodal therapy. In particular, tumor-initiating cells (TICs) derived from neuroblastoma are believed responsible for tumor formation and resistance to the conventional therapy; an optimal strategy therefore should target this population. Technically, TICs can be enriched from neuroblastoma-derived spheres when the tumor cells are cultured in a serum-free medium supplemented with certain growth factors. Recently, a line of evidence has suggested antitumor potential of Vγ9Vδ2 T cells (γδ T cells), a T-cell population that recognizes and kills target cells independent of surface HLA expressions. Furthermore, a mevalonate pathway inhibitor, zoledronate, has been reported to enhance cytolytic activity of γδ T cells. On the basis of these findings, we hypothesized that zoledronate would sensitize neuroblastoma TICs to γδ T-cell-mediated cytolysis and promote therapeutic efficacy against neuroblastoma. In the current study, we show that zoledronate efficiently sensitizes both neuroblastoma-derived adherent cells and sphere-forming cells to γδ T-cell-mediated cytolysis. Subsequently, in vitro colony formation inhibition assay and in vivo animal studies reveal that the presence of γδ T cells decelerates outgrowth of neuroblastoma TICs. We finally show that addition of interleukin-15 and/or interleukin-18 in culture enhances the cytolytic activity of γδ T cells. On the basis of these data, we conclude that ex vivo expanded γδ T cells are a promising tool for antineuroblastoma immunotherapy with options for further improvement.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Antineoplastic Agents / administration & dosage*
  • Bone Marrow Neoplasms / immunology
  • Bone Marrow Neoplasms / pathology
  • Bone Marrow Neoplasms / therapy*
  • Cell Line, Tumor
  • Child
  • Cytotoxicity, Immunologic / drug effects
  • Diphosphonates / administration & dosage*
  • Drug Synergism
  • Female
  • Growth Inhibitors / administration & dosage*
  • Humans
  • Imidazoles / administration & dosage*
  • Immunotherapy, Adoptive / methods*
  • Interleukin-15 / pharmacology
  • Interleukin-18 / pharmacology
  • Male
  • Mice
  • Mice, SCID
  • Neoplastic Stem Cells / drug effects*
  • Neoplastic Stem Cells / immunology
  • Neoplastic Stem Cells / pathology
  • Neuroblastoma / immunology
  • Neuroblastoma / pathology
  • Neuroblastoma / therapy*
  • Receptors, Antigen, T-Cell, gamma-delta / immunology
  • T-Lymphocytes / drug effects*
  • T-Lymphocytes / immunology
  • T-Lymphocytes / transplantation
  • Xenograft Model Antitumor Assays
  • Young Adult
  • Zoledronic Acid

Substances

  • Antineoplastic Agents
  • Diphosphonates
  • Growth Inhibitors
  • Imidazoles
  • Interleukin-15
  • Interleukin-18
  • Receptors, Antigen, T-Cell, gamma-delta
  • T-cell receptor Vdelta2, human
  • T-cell receptor Vgamma9, human
  • Zoledronic Acid