'Off-the-shelf' allogeneic antigen-specific adoptive T-cell therapy for the treatment of multiple EBV-associated malignancies

J Immunother Cancer. 2021 Feb;9(2):e001608. doi: 10.1136/jitc-2020-001608.

Abstract

Background: Epstein-Barr virus (EBV), an oncogenic human gammaherpesvirus, is associated with a wide range of human malignancies of epithelial and B-cell origin. Recent studies have demonstrated promising safety and clinical efficacy of allogeneic 'off-the-shelf' virus-specific T-cell therapies for post-transplant viral complications.

Methods: Taking a clue from these studies, we developed a highly efficient EBV-specific T-cell expansion process using a replication-deficient AdE1-LMPpoly vector that specifically targets EBV-encoded nuclear antigen 1 (EBNA1) and latent membrane proteins 1 and 2 (LMP1 and LMP2), expressed in latency II malignancies.

Results: These allogeneic EBV-specific T cells efficiently recognized human leukocyte antigen (HLA)-matched EBNA1-expressing and/or LMP1 and LMP2-expressing malignant cells and demonstrated therapeutic potential in a number of in vivo models, including EBV lymphomas that emerged spontaneously in humanized mice following EBV infection. Interestingly, we were able to override resistance to T-cell therapy in vivo using a 'restriction-switching' approach, through sequential infusion of two different allogeneic T-cell therapies restricted through different HLA alleles. Furthermore, we have shown that inhibition of the programmed cell death protein-1/programmed death-ligand 1 axis in combination with EBV-specific T-cell therapy significantly improved overall survival of tumor-bearing mice when compared with monotherapy.

Conclusion: These findings suggest that restriction switching by sequential infusion of allogeneic T-cell therapies that target EBV through distinct HLA alleles may improve clinical response.

Keywords: adoptive; cellular; immunity; immunotherapy; lymphocytes; t-lymphocytes; tumor-infiltrating.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Epstein-Barr Virus Infections / immunology
  • Epstein-Barr Virus Infections / therapy*
  • Epstein-Barr Virus Nuclear Antigens / immunology*
  • Female
  • HLA Antigens
  • Herpesvirus 4, Human / immunology*
  • Humans
  • Immune Checkpoint Inhibitors / administration & dosage*
  • Immune Checkpoint Inhibitors / pharmacology
  • Lymphoma / immunology
  • Lymphoma / therapy
  • Lymphoma / virology*
  • Mice
  • T-Lymphocytes / immunology
  • T-Lymphocytes / transplantation*
  • Transplantation, Homologous
  • Viral Matrix Proteins / immunology*
  • Xenograft Model Antitumor Assays

Substances

  • EBV-associated membrane antigen, Epstein-Barr virus
  • Epstein-Barr Virus Nuclear Antigens
  • HLA Antigens
  • Immune Checkpoint Inhibitors
  • Viral Matrix Proteins
  • EBV-encoded nuclear antigen 1