Human Leukocyte Antigen (HLA) A*1101-Restricted Epstein-Barr Virus-Specific T-cell Receptor Gene Transfer to Target Nasopharyngeal Carcinoma

Cancer Immunol Res. 2015 Oct;3(10):1138-47. doi: 10.1158/2326-6066.CIR-14-0203-T. Epub 2015 Feb 24.

Abstract

Infusing virus-specific T cells is effective treatment for rare Epstein-Barr virus (EBV)-associated posttransplant lymphomas, and more limited success has been reported using this approach to treat a far more common EBV-associated malignancy, nasopharyngeal carcinoma (NPC). However, current approaches using EBV-transformed lymphoblastoid cell lines to reactivate EBV-specific T cells for infusion take 2 to 3 months of in vitro culture and favor outgrowth of T cells targeting viral antigens expressed within EBV(+) lymphomas, but not in NPC. Here, we explore T-cell receptor (TCR) gene transfer to rapidly and reliably generate T cells specific for the NPC-associated viral protein LMP2. We cloned a human leukocyte antigen (HLA) A*1101-restricted TCR, which would be widely applicable because 40% of NPC patients carry this HLA allele. Studying both the wild-type and modified forms, we have optimized expression of the TCR and demonstrated high-avidity antigen-specific function (proliferation, cytotoxicity, and cytokine release) in both CD8(+) and CD4(+) T cells. The engineered T cells also inhibited LMP2(+) epithelial tumor growth in a mouse model. Furthermore, transduced T cells from patients with advanced NPC lysed LMP2-expressing NPC cell lines. Using this approach, within a few days large numbers of high-avidity LMP2-specific T cells can be generated reliably to treat NPC, thus providing an ideal clinical setting to test TCR gene transfer without the risk of autoimmunity through targeting self-antigens.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Carcinoma
  • Cell Line, Tumor
  • Cytokines / biosynthesis
  • Cytotoxicity, Immunologic
  • Disease Models, Animal
  • Epitopes, T-Lymphocyte / immunology
  • Epstein-Barr Virus Infections / complications*
  • Epstein-Barr Virus Infections / immunology*
  • Female
  • Gene Expression
  • Gene Transfer Techniques
  • HLA-A Antigens / immunology*
  • Herpesvirus 4, Human / immunology*
  • Humans
  • Immunotherapy
  • Interferon-gamma / biosynthesis
  • Mice
  • Molecular Sequence Data
  • Nasopharyngeal Carcinoma
  • Nasopharyngeal Neoplasms / etiology*
  • Nasopharyngeal Neoplasms / therapy
  • Receptors, Antigen, T-Cell / genetics*
  • Transduction, Genetic
  • Tumor Burden
  • Viral Matrix Proteins / immunology
  • Xenograft Model Antitumor Assays

Substances

  • Cytokines
  • EBV-associated membrane antigen, Epstein-Barr virus
  • Epitopes, T-Lymphocyte
  • HLA-A Antigens
  • Receptors, Antigen, T-Cell
  • Viral Matrix Proteins
  • Interferon-gamma

Associated data

  • GENBANK/KU163590