Preclinical development of T-cell receptor-engineered T-cell therapy targeting the 5T4 tumor antigen on renal cell carcinoma

Cancer Immunol Immunother. 2019 Dec;68(12):1979-1993. doi: 10.1007/s00262-019-02419-4. Epub 2019 Nov 4.

Abstract

5T4 (trophoblast glycoprotein, TPBG) is a transmembrane tumor antigen expressed on more than 90% of primary renal cell carcinomas (RCC) and a wide range of human carcinomas but not on most somatic adult tissues. The favorable expression pattern has encouraged the development and clinical testing of 5T4-targeted antibody and vaccine therapies. 5T4 also represents a compelling and unexplored target for T-cell receptor (TCR)-engineered T-cell therapy. Our group has previously isolated high-avidity CD8+ T-cell clones specific for an HLA-A2-restricted 5T4 epitope (residues 17-25; 5T4p17). In this report, targeted single-cell RNA sequencing was performed on 5T4p17-specific T-cell clones to sequence the highly variable complementarity-determining region 3 (CDR3) of T-cell receptor α chain (TRA) and β chain (TRB) genes. Full-length TRA and TRB sequences were cloned into lentiviral vectors and transduced into CD8+ T-cells from healthy donors. Redirected effector T-cell function against 5T4p17 was measured by cytotoxicity and cytokine release assays. Seven unique TRA-TRB pairs were identified. All seven TCRs exhibited high expression on CD8+ T-cells with transduction efficiencies from 59 to 89%. TCR-transduced CD8+ T-cells demonstrated redirected cytotoxicity and cytokine release in response to 5T4p17 on target-cells and killed 5T4+/HLA-A2+ kidney-, breast-, and colorectal-tumor cell lines as well as primary RCC tumor cells in vitro. TCR-transduced CD8+ T-cells also detected presentation of 5T4p17 in TAP1/2-deficient T2 target-cells. TCR-transduced T-cells redirected to recognize the 5T4p17 epitope from a broadly shared tumor antigen are of interest for future testing as a cellular immunotherapy strategy for HLA-A2+ subjects with 5T4+ tumors.

Keywords: 5T4; Adoptive cell therapy; Antigen processing; Renal cell carcinoma; T-cell receptor; Trophoblast glycoprotein.

MeSH terms

  • CD8-Positive T-Lymphocytes / physiology*
  • CD8-Positive T-Lymphocytes / transplantation
  • Cancer Vaccines / immunology*
  • Carcinoma, Renal Cell / immunology
  • Carcinoma, Renal Cell / therapy*
  • Clone Cells
  • Cytotoxicity, Immunologic
  • Epitopes, T-Lymphocyte / immunology
  • Epitopes, T-Lymphocyte / metabolism*
  • HLA-A2 Antigen / metabolism
  • Humans
  • Immunotherapy, Adoptive / methods*
  • Kidney Neoplasms / immunology
  • Kidney Neoplasms / therapy*
  • Membrane Glycoproteins / immunology
  • Membrane Glycoproteins / metabolism*
  • Receptors, Antigen, T-Cell, alpha-beta / genetics

Substances

  • Cancer Vaccines
  • Epitopes, T-Lymphocyte
  • HLA-A2 Antigen
  • Membrane Glycoproteins
  • Receptors, Antigen, T-Cell, alpha-beta
  • trophoblastic glycoprotein 5T4, human