T cells specific for different latent and lytic viral proteins efficiently control Epstein-Barr virus-transformed B cells

Cytotherapy. 2015 Sep;17(9):1280-91. doi: 10.1016/j.jcyt.2015.06.003.

Abstract

Background aims: Epstein-Barr virus (EBV)-associated post-transplant lymphoproliferative disorders (PTLD) belong to the most dreaded complications of immunosuppression. The efficacy of EBV-specific T-cell transfer for PTLD has been previously shown, yet the optimal choice of EBV-derived antigens inducing polyclonal CD4(+) and CD8(+) T cells that cover a wide range of human leukocyte antigen types and efficiently control PTLD remains unclear.

Methods: A pool of 125 T-cell epitopes from seven latent and nine lytic EBV-derived proteins (EBVmix) and peptide pools of EBNA1, EBNA3c, LMP2a and BZLF1 were used to determine T-cell frequencies and to isolate T cells through the use of the interferon (IFN)-γ cytokine capture system. We further evaluated the phenotype and functionality of the generated T-cell lines in vitro.

Results: EBVmix induced significantly higher T-cell frequencies and allowed selecting more CD4(+)IFN-γ(+) and CD8(+)IFN-γ(+) cells than single peptide pools. T cells of all specificities expanded similarly in vitro, recognized cognate antigen, and, to a lower extent, EBV-infected cells, exerted moderate cytotoxicity and showed reduced alloreactivity. However, EBVmix-specific cells most efficiently controlled EBV-infected lymphoblastoid cell lines (LCLs). This control was mainly mediated by EBV-specific CD8(+) cells with an oligoclonal epitope signature covering both latent and lytic viral proteins. Notably, EBV-specific CD4(+) cells unable to control LCLs produced significantly less perforin and granzyme B, probably because of limited LCL epitope presentation.

Conclusions: EBVmix induces a broader T-cell response, probably because of its coverage of latent and lytic EBV-derived proteins that may be important to control EBV-transformed B cells and might offer an improvement of T-cell therapies.

Keywords: Epstein-Barr virus; IFN-γ selection; PTLD; T-cell transfer; immunotherapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • B-Lymphocytes / immunology
  • B-Lymphocytes / virology*
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / transplantation
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / transplantation
  • Cell Transformation, Viral / immunology*
  • Cells, Cultured
  • Epitopes, T-Lymphocyte / immunology
  • Epstein-Barr Virus Infections / therapy*
  • Epstein-Barr Virus Nuclear Antigens / immunology
  • Granzymes / metabolism
  • Herpesvirus 4, Human / immunology*
  • Humans
  • Interferon-gamma / immunology
  • Perforin / biosynthesis
  • Trans-Activators / immunology
  • Viral Matrix Proteins / immunology

Substances

  • BZLF1 protein, Herpesvirus 4, Human
  • EBNA-3C, epstein-barr virus
  • EBV-associated membrane antigen, Epstein-Barr virus
  • Epitopes, T-Lymphocyte
  • Epstein-Barr Virus Nuclear Antigens
  • Trans-Activators
  • Viral Matrix Proteins
  • Perforin
  • Interferon-gamma
  • Granzymes
  • EBV-encoded nuclear antigen 1