Redirected perforin-dependent lysis of colon carcinoma by ex vivo genetically engineered CTL

J Immunol. 2000 Apr 1;164(7):3705-12. doi: 10.4049/jimmunol.164.7.3705.

Abstract

The redirection of autologous lymphocytes to predefined tumor target Ags has considerable potential for the immunotherapeutic treatment of cancer; however, robust experimental systems for comparing various approaches have not been developed. Herein, we have generated a single chain variable domain anti-carcinoembryonic Ag (CEA) Fcepsilon receptor I gamma-chain fusion (scFv anti-CEA) receptor and demonstrated high-level expression of this chimeric receptor in naive mouse T lymphocytes by retroviral gene transduction. These gene-modified CTL were able to lyse CEA+ targets and secrete high levels of IFN-gamma following Ag stimulation. Depletion studies demonstrated that specific tumor cell cytotoxicity was mediated by gene-modified CD8+ T cells. Importantly, in increasingly stringent tests of efficacy in vivo, transduced CTL were sequentially shown to reject CEA+ colon carcinoma cells in a Winn assay and then reject established s.c. colon carcinoma in scid or syngeneic mice. Furthermore, using gene-targeted and scFv anti-CEA receptor-transduced donor CTL, perforin and IFN-gamma were demonstrated to be absolutely critical for the eradication of colon carcinoma in mice. In summary, we have developed a highly efficient gene transfer system for evaluating chimeric receptor expression in cytotoxic lymphocytes. This series of experiments has revealed the utility of scFv anti-CEA chimeras in providing mouse T cells the capacity to reject colon carcinoma in an Ag- and perforin-specific manner.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / genetics
  • Adenocarcinoma / immunology
  • Adenocarcinoma / prevention & control
  • Adoptive Transfer
  • Animals
  • Binding Sites / genetics
  • Binding Sites / immunology
  • Carcinoembryonic Antigen / metabolism
  • Carrier Proteins / genetics
  • Carrier Proteins / immunology
  • Cell Division / immunology
  • Colonic Neoplasms / genetics*
  • Colonic Neoplasms / immunology*
  • Colonic Neoplasms / pathology
  • Colonic Neoplasms / prevention & control
  • Cytokines / metabolism
  • Cytotoxicity, Immunologic / genetics*
  • Epitopes, T-Lymphocyte / immunology
  • Epitopes, T-Lymphocyte / metabolism
  • Humans
  • Immunoglobulin Fragments / biosynthesis
  • Immunoglobulin Fragments / genetics
  • Immunoglobulin Variable Region / genetics
  • Interferon-gamma / physiology
  • Lymphocyte Count
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / physiology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, SCID
  • Neoplasm Transplantation
  • Perforin
  • Pore Forming Cytotoxic Proteins
  • Receptors, Cell Surface*
  • Recombinant Fusion Proteins / biosynthesis
  • Recombinant Fusion Proteins / chemical synthesis
  • Recombinant Fusion Proteins / genetics
  • T-Lymphocytes, Cytotoxic / immunology*
  • T-Lymphocytes, Cytotoxic / metabolism
  • T-Lymphocytes, Cytotoxic / transplantation
  • Transduction, Genetic
  • Tumor Cells, Cultured

Substances

  • Carcinoembryonic Antigen
  • Carrier Proteins
  • Cytokines
  • Epitopes, T-Lymphocyte
  • Immunoglobulin Fragments
  • Immunoglobulin Variable Region
  • Membrane Glycoproteins
  • Pore Forming Cytotoxic Proteins
  • Receptors, Cell Surface
  • Recombinant Fusion Proteins
  • carcinoembryonic antigen binding protein, human
  • immunoglobulin Fv
  • Perforin
  • Interferon-gamma