Lack of effector cell function and altered tetramer binding of tumor-infiltrating lymphocytes

J Immunol. 2002 Nov 15;169(10):5522-30. doi: 10.4049/jimmunol.169.10.5522.

Abstract

Tumor-specific CD8 T cell responses to MCA102 fibrosarcoma cells expressing the cytotoxic T cell epitope gp33 from lymphocytic choriomeningitis virus were studied. MCA102(gp33) tumors grew progressively in C57BL/6 mice, despite induction of peripheral gp33-tetramer(+) T cells that were capable of mediating antiviral protection, specific cell rejection, and concomitant tumor immunity. MCA102(gp33) tumors were infiltrated with a high number ( approximately 20%) of CD11b(+)CD11c(-) macrophage-phenotype cells that were able to cross-present the gp33 epitope to T cells. Tumor-infiltrating CD8 T cells exhibited a highly activated phenotype but lacked effector cell function. Strikingly, a significant portion of tumor-infiltrating lymphocytes expressed TCRs specific for gp33 but bound MHC tetramers only after cell purification and a 24-h resting period in vitro. The phenomenon of "tetramer-negative T cells" was not restricted to tumor-infiltrating lymphocytes from MCA102(gp33) tumors, but was also observed when Ag-specific T cells derived from an environment with high Ag load were analyzed ex vivo. Thus, using a novel tumor model, allowing us to trace tumor-specific T cells at the single cell level in vivo, we demonstrate that the tumor microenvironment is able to alter the functional activity of T cells infiltrating the tumor mass.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigen Presentation / genetics
  • Antigens, Viral / biosynthesis
  • Antigens, Viral / immunology
  • Antigens, Viral / metabolism*
  • CD11b Antigen / biosynthesis
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism*
  • Cell Division / genetics
  • Cell Division / immunology
  • Cell Separation
  • Cells, Cultured
  • Cytotoxicity, Immunologic* / genetics
  • Epitopes, T-Lymphocyte / biosynthesis
  • Epitopes, T-Lymphocyte / immunology
  • Female
  • Fibrosarcoma / immunology*
  • Fibrosarcoma / metabolism
  • Fibrosarcoma / pathology
  • Glycoproteins / biosynthesis
  • Glycoproteins / immunology
  • Glycoproteins / metabolism*
  • Histocompatibility Antigens Class I / metabolism*
  • Immunity, Innate / genetics
  • Lymphocyte Count
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Lymphocytes, Tumor-Infiltrating / metabolism*
  • Lymphocytes, Tumor-Infiltrating / pathology
  • Lymphocytic choriomeningitis virus / immunology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neoplasm Transplantation
  • Peptide Fragments / biosynthesis
  • Peptide Fragments / immunology
  • Peptide Fragments / metabolism*
  • Protein Binding / genetics
  • Protein Binding / immunology
  • Receptors, Antigen, T-Cell / biosynthesis
  • Tumor Cells, Cultured
  • Viral Proteins / biosynthesis
  • Viral Proteins / immunology
  • Viral Proteins / metabolism*

Substances

  • Antigens, Viral
  • CD11b Antigen
  • Epitopes, T-Lymphocyte
  • Glycoproteins
  • Histocompatibility Antigens Class I
  • Peptide Fragments
  • Receptors, Antigen, T-Cell
  • Viral Proteins
  • glycoprotein peptide 33-41, Lymphocytic choriomeningitis virus