Rapid high efficiency sensitization of CD8+ T cells to tumor antigens by dendritic cells leads to enhanced functional avidity and direct tumor recognition through an IL-12-dependent mechanism

J Immunol. 2003 Sep 1;171(5):2251-61. doi: 10.4049/jimmunol.171.5.2251.

Abstract

Myeloid-origin dendritic cells (DCs) can develop into IL-12-secreting DC1 or non-IL-12-secreting DC2 depending on signals received during maturation. Through rapid culture techniques that prepared either mature, CD83+ DC1 or DC2 from CD14+ monocytes in only 2 days followed by a single 6-7 day DC-T cell coculture, we sensitized normal donor CD8+ T cells to tumor Ags (HER-2/neu, MART-1, and gp100) such that peptide Ag-specific lymphocytes constituted up to 16% of the total CD8+ population. Both DC1 and DC2 could sensitize CD8+ T cells that recognized peptide-pulsed target cells. However, with DC2, a general decoupling was observed between recognition of peptide-pulsed T2 target cells and recognition of Ag-expressing tumor cells, with peptide-sensitized T cells responding to tumor only about 15% of the time. In contrast, direct recognition of tumor by T cells was dramatically increased (to 85%) when DC1 were used for sensitization. Enhanced tumor recognition was accompanied by 10- to 100-fold increases in peptide sensitivity and elevated expression of CD8beta, characteristic of high functional avidity T cells. Both of these properties were IL-12-dependent. These results demonstrate the utility of rapid DC culture methods for high efficiency in vitro T cell sensitization that achieves robust priming and expansion of Ag-specific populations in 6 days. They also demonstrate a novel function of IL-12, which is enhancement of CD8+ T cell functional avidity. A new approach to DC-based vaccines that emphasizes IL-12 secretion to enhance functional avidity and concomitant tumor recognition by CD8+ T cells is indicated.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adjuvants, Immunologic / physiology
  • Adult
  • Antigen Presentation
  • Antigens, Neoplasm / immunology*
  • Antigens, Neoplasm / metabolism
  • CD8 Antigens / biosynthesis
  • CD8-Positive T-Lymphocytes / cytology
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • Cell Adhesion / immunology
  • Cell Differentiation / immunology
  • Cell Line, Tumor
  • Cells, Cultured
  • Culture Media, Conditioned / pharmacology
  • Cytotoxicity, Immunologic / immunology
  • Dendritic Cells / classification
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology*
  • Epitopes, T-Lymphocyte / immunology
  • Female
  • Humans
  • Immunization* / methods
  • Interleukin-12 / physiology*
  • Lymphocyte Activation / immunology
  • MART-1 Antigen
  • Male
  • Melanoma / immunology*
  • Melanoma / metabolism
  • Membrane Glycoproteins / immunology
  • Membrane Glycoproteins / metabolism
  • Neoplasm Proteins / immunology
  • Neoplasm Proteins / metabolism
  • Peptide Fragments / immunology
  • Peptide Fragments / metabolism
  • Receptor, ErbB-2 / immunology
  • Receptor, ErbB-2 / metabolism
  • T-Lymphocyte Subsets / cytology
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • gp100 Melanoma Antigen

Substances

  • Adjuvants, Immunologic
  • Antigens, Neoplasm
  • CD8 Antigens
  • CD8beta antigen
  • Culture Media, Conditioned
  • Epitopes, T-Lymphocyte
  • MART-1 Antigen
  • MLANA protein, human
  • Membrane Glycoproteins
  • Neoplasm Proteins
  • PMEL protein, human
  • Peptide Fragments
  • gp100 Melanoma Antigen
  • Interleukin-12
  • Receptor, ErbB-2