Immunosensitization of melanoma tumor cells to non-MHC Fas-mediated killing by MART-1-specific CTL cultures

J Immunol. 2001 Mar 1;166(5):3564-73. doi: 10.4049/jimmunol.166.5.3564.

Abstract

The discovery of human melanoma rejection Ags has allowed the rational design of immunotherapeutic strategies. One such Ag, MART-1, is expressed on >90% of human melanomas, and CTL generated against MART-1(27-35) kill most HLA A2.1(+) melanoma cells. However, variant tumor cells, which do not express MART-1, down-regulate MHC, or become resistant to apoptosis, will escape killing. Cytotoxic lymphocytes kill by two main mechanisms, the perforin/granzyme degranulation pathway and the TNF/Fas/TNF-related apoptosis-inducing ligand superfamily of apoptosis-inducing ligands. In this study, we examined whether cis-diaminedichloroplatinum (II) cisplatin (CDDP) sensitizes MART-1/HLA A2.1(+) melanoma and melanoma variant tumor cells to non-MHC-restricted, Fas ligand (FasL)-mediated killing by CTL. MART-1(27-35)-specific bulk CTL cultures were generated by pulsing normal PBL with MART-1(27-35) peptide. These CTL cultures specifically kill M202 melanoma cells (MART-1(+), HLA A2.1(+), FasR(-)), and MART-1(27-35) peptide-pulsed T2 cells (FasR(+)), but not M207 melanoma cells (MART-1(+), HLA A2.1(-), FasR(-)), FLU(58-66) peptide-pulsed T2 cells, or DU145 and PC-3 prostate cells (MART-1(-), HLA A2.1(-), FasR(+)). CDDP (0.1-10 microg/ml) sensitized non-MART-1(27-35) peptide-pulsed T2 to the CD8(+) subset of bulk MART-1-specific CTL, and killing was abolished by neutralizing anti-Fas Ab. Furthermore, CDDP up-regulated FasR expression and FasL-mediated killing of M202, and sensitized PC-3 and DU145 to killing by bulk MART-1-specific CTL cultures. These findings demonstrate that drug-mediated sensitization can potentiate FasL-mediated killing by MHC-restricted CTL cell lines, independent of MHC and MART-1 expression on tumor cells. This represents a novel approach for potentially controlling tumor cell variants found in primary heterogeneous melanoma tumor cell populations that would normally escape killing by MART-1-specific immunotherapy.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adjuvants, Immunologic / pharmacology
  • Animals
  • Antigens, Neoplasm
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects
  • Apoptosis / immunology*
  • Cells, Cultured
  • Cisplatin / pharmacology
  • Cytotoxicity Tests, Immunologic
  • Cytotoxicity, Immunologic* / drug effects
  • Drug Resistance, Neoplasm
  • Epitopes / metabolism
  • Epitopes, T-Lymphocyte / immunology*
  • Fas Ligand Protein
  • Humans
  • Hybridomas
  • Immunization
  • MART-1 Antigen
  • Major Histocompatibility Complex / immunology
  • Male
  • Melanoma / drug therapy
  • Melanoma / immunology*
  • Melanoma / metabolism
  • Melanoma / pathology*
  • Membrane Glycoproteins / biosynthesis
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / physiology
  • Mice
  • Mice, Inbred BALB C
  • Neoplasm Proteins / immunology*
  • Neoplasm Proteins / metabolism
  • Perforin
  • Pore Forming Cytotoxic Proteins
  • Prostatic Neoplasms / drug therapy
  • Prostatic Neoplasms / immunology
  • Prostatic Neoplasms / pathology
  • RNA, Messenger / biosynthesis
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocytes, Cytotoxic / drug effects
  • T-Lymphocytes, Cytotoxic / immunology*
  • Tumor Cells, Cultured
  • Up-Regulation / drug effects
  • Up-Regulation / immunology
  • fas Receptor / metabolism
  • fas Receptor / physiology*

Substances

  • Adjuvants, Immunologic
  • Antigens, Neoplasm
  • Antineoplastic Agents
  • Epitopes
  • Epitopes, T-Lymphocyte
  • FASLG protein, human
  • Fas Ligand Protein
  • Fasl protein, mouse
  • MART-1 Antigen
  • MART-1-Melan-A(27-35) epitope
  • MLANA protein, human
  • Membrane Glycoproteins
  • Mlana protein, mouse
  • Neoplasm Proteins
  • Pore Forming Cytotoxic Proteins
  • RNA, Messenger
  • fas Receptor
  • Perforin
  • Cisplatin