Radiation with STAT3 Blockade Triggers Dendritic Cell-T cell Interactions in the Glioma Microenvironment and Therapeutic Efficacy

Clin Cancer Res. 2020 Sep 15;26(18):4983-4994. doi: 10.1158/1078-0432.CCR-19-4092. Epub 2020 Jun 30.

Abstract

Purpose: Patients with central nervous system (CNS) tumors are typically treated with radiotherapy, but this is not curative and results in the upregulation of phosphorylated STAT3 (p-STAT3), which drives invasion, angiogenesis, and immune suppression. Therefore, we investigated the combined effect of an inhibitor of STAT3 and whole-brain radiotherapy (WBRT) in a murine model of glioma.

Experimental design: C57BL/6 mice underwent intracerebral implantation of GL261 glioma cells, WBRT, and treatment with WP1066, a blood-brain barrier-penetrant inhibitor of the STAT3 pathway, or the two in combination. The role of the immune system was evaluated using tumor rechallenge strategies, immune-incompetent backgrounds, immunofluorescence, immune phenotyping of tumor-infiltrating immune cells (via flow cytometry), and NanoString gene expression analysis of 770 immune-related genes from immune cells, including those directly isolated from the tumor microenvironment.

Results: The combination of WP1066 and WBRT resulted in long-term survivors and enhanced median survival time relative to monotherapy in the GL261 glioma model (combination vs. control P < 0.0001). Immunologic memory appeared to be induced, because mice were protected during subsequent tumor rechallenge. The therapeutic effect of the combination was completely lost in immune-incompetent animals. NanoString analysis and immunofluorescence revealed immunologic reprograming in the CNS tumor microenvironment specifically affecting dendritic cell antigen presentation and T-cell effector functions.

Conclusions: This study indicates that the combination of STAT3 inhibition and WBRT enhances the therapeutic effect against gliomas in the CNS by inducing dendritic cell and T-cell interactions in the CNS tumor.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigen Presentation / drug effects
  • Antigen Presentation / radiation effects
  • Brain Neoplasms / immunology
  • Brain Neoplasms / pathology
  • Brain Neoplasms / therapy*
  • Cell Communication / drug effects
  • Cell Communication / immunology*
  • Cell Communication / radiation effects
  • Cell Line, Tumor / ultrastructure
  • Chemoradiotherapy / methods*
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology
  • Dendritic Cells / radiation effects
  • Disease Models, Animal
  • Glioma / immunology
  • Glioma / pathology
  • Glioma / therapy*
  • Humans
  • Immunologic Memory / drug effects
  • Mice
  • Pyridines / administration & dosage
  • STAT3 Transcription Factor / antagonists & inhibitors*
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology
  • T-Lymphocytes / radiation effects
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / immunology
  • Tumor Microenvironment / radiation effects
  • Tyrphostins / administration & dosage

Substances

  • Pyridines
  • STAT3 Transcription Factor
  • Stat3 protein, mouse
  • Tyrphostins
  • WP1066