Strong and sustained effector function of memory- versus naïve-derived T cells upon T-cell receptor RNA transfer: implications for cellular therapy

Eur J Immunol. 2012 Dec;42(12):3442-53. doi: 10.1002/eji.201242666. Epub 2012 Oct 1.

Abstract

Current protocols used to select CMV-specific T cells for adoptive immunotherapy focus on virus-specific memory T cells from seropositive donors. However, this strategy is not feasible in patients undergoing allogeneic haematopoietic stem-cell transplantation (HSCT) from CMV-seronegative donors. Here, we redirected T cells of CMV-seronegative donors with a human genetically engineered TCR recognizing an HLA-A*0201-binding peptide epitope of CMVpp65. To facilitate clinical translation of this approach, we used a non-viral expression system based on in vitro transcribed RNA and electroporation. Although memory and naïve-derived T-cell subsets were both efficiently transfected by TCR-RNA, memory-derived T cells showed much stronger levels of HLA-A*0201-restricted cytolytic activity to CMV-infected fibroblasts and maintained acquired function for 5-10 days. In addition to redirection of CD8(+) cytotoxic T cells, TCR-RNA transfection was capable of redirecting CD4(+) T cells into potent Ag-specific Th cells that efficiently triggered maturation of DCs. Our data suggest that memory rather than naïve-derived T cells are the preferred subset for transient TCR expression by RNA electroporation, providing more efficient and sustained virus-specific CD4(+) and CD8(+) T-cell function. CMV TCR-RNA may represent a suitable therapeutic 'off-the-shelf' reagent to be used in severe CMV infections of HSCT patients when endogenous CMV-specific T-cell immunity is insufficient.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CD4-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / immunology*
  • Cell- and Tissue-Based Therapy*
  • Cytomegalovirus / genetics
  • Cytomegalovirus / immunology*
  • Cytomegalovirus Infections / genetics
  • Cytomegalovirus Infections / immunology
  • Cytomegalovirus Infections / therapy
  • Electroporation / methods
  • Fibroblasts / immunology
  • Gene Expression Regulation / genetics
  • Gene Expression Regulation / immunology
  • Graft vs Host Disease / genetics
  • Graft vs Host Disease / immunology
  • Graft vs Host Disease / therapy
  • HLA-A2 Antigen / genetics
  • HLA-A2 Antigen / immunology
  • Hematopoietic Stem Cell Transplantation
  • Humans
  • Immunologic Memory / drug effects*
  • Immunologic Memory / genetics
  • Phosphoproteins / genetics
  • Phosphoproteins / immunology*
  • RNA / genetics
  • RNA / immunology
  • RNA / pharmacology*
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology*
  • Transfection / methods
  • Transplantation, Homologous
  • Viral Matrix Proteins / genetics
  • Viral Matrix Proteins / immunology*

Substances

  • HLA-A*02:01 antigen
  • HLA-A2 Antigen
  • Phosphoproteins
  • Receptors, Antigen, T-Cell
  • Viral Matrix Proteins
  • cytomegalovirus matrix protein 65kDa
  • RNA