Immune Escape After Adoptive T-cell Therapy for Malignant Gliomas

Clin Cancer Res. 2020 Nov 1;26(21):5689-5700. doi: 10.1158/1078-0432.CCR-20-1065. Epub 2020 Aug 11.

Abstract

Purpose: Immunotherapy has been demonstrably effective against multiple cancers, yet tumor escape is common. It remains unclear how brain tumors escape immunotherapy and how to overcome this immune escape.

Experimental design: We studied KR158B-luc glioma-bearing mice during treatment with adoptive cellular therapy (ACT) with polyclonal tumor-specific T cells. We tested the immunogenicity of primary and escaped tumors using T-cell restimulation assays. We used flow cytometry and RNA profiling of whole tumors to further define escape mechanisms. To treat immune-escaped tumors, we generated escape variant-specific T cells through the use of escape variant total tumor RNA and administered these cells as ACT. In addition, programmed cell death protein-1 (PD-1) checkpoint blockade was studied in combination with ACT.

Results: Escape mechanisms included a shift in immunogenic tumor antigens, downregulation of MHC class I, and upregulation of checkpoint molecules. Polyclonal T cells specific for escape variants displayed greater recognition of escaped tumors than primary tumors. When administered as ACT, these T cells prolonged median survival of escape variant-bearing mice by 60%. The rational combination of ACT with PD-1 blockade prolonged median survival of escape variant glioma-bearing mice by 110% and was dependent upon natural killer cells and T cells.

Conclusions: These findings suggest that the immune landscape of brain tumors are markedly different postimmunotherapy yet can still be targeted with immunotherapy.

Publication types

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

MeSH terms

  • Animals
  • Antibodies, Monoclonal / immunology
  • Antibodies, Monoclonal / pharmacology
  • Antigens, Neoplasm / immunology
  • Cell Line, Tumor
  • Glioma / genetics
  • Glioma / immunology
  • Glioma / pathology
  • Glioma / therapy*
  • Heterografts
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immunotherapy, Adoptive / adverse effects
  • Killer Cells, Natural / drug effects
  • Killer Cells, Natural / immunology
  • Mice
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor / immunology*
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology*
  • Tumor Escape / drug effects*
  • Tumor Escape / immunology
  • Tumor Microenvironment / drug effects

Substances

  • Antibodies, Monoclonal
  • Antigens, Neoplasm
  • Immune Checkpoint Inhibitors
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor