Noncovalent association with stress protein facilitates cross-priming of CD8+ T cells to tumor cell antigens by dendritic cells

J Immunol. 2002 Jan 1;168(1):108-17. doi: 10.4049/jimmunol.168.1.108.

Abstract

A viral oncogene carrying well-defined K(b)/D(b)-restricted epitopes was expressed in a heat shock protein (hsp)-associated or nonassociated form in the murine tumor cells P815 and Meth-A. Wild-type SV40 large T-Ag (wtT-Ag) is expressed without stable hsp association; mutant (cytoplasmic cT-Ag) or chimeric (cT272-green fluorescent fusion protein) T-Ag is expressed in stable association with the constitutively expressed, cytosolic hsp73 (hsc70) protein. In vitro, remnants from apoptotic wtT-Ag- or cT-Ag-expressing tumor cells are taken up and processed by immature dendritic cells (DC), and the K(b)/D(b)-binding epitopes T1, T2/3, and T4 of the T-Ag are cross-presented to CTL in a TAP-independent way. DC pulsed with remnants of transfected, apoptotic tumor cells cross-presented the three T-Ag epitopes more efficiently when they processed ATP-sensitive hsp73/cT-Ag complexes than when they processed hsp-nonassociated (native) T-Ag. In vivo, more IFN-gamma-producing CD8+ T cells were elicited by a DNA vaccine that encoded hsp73-binding mutant T-Ag than by a DNA vaccine that encoded native, non-hsp-binding T-Ag. Three- to 5-fold higher numbers of T-Ag (T1-, T2/3-, or T4-) specific, D(b)/K(b)-restricted IFN-gamma-producing CD8+ T cells were primed during the growth of transfected H-2(d) Meth-A/cT tumors than during the growth of transfected Meth-A/T tumors in F(1)(b x d) hosts. Hence, the association of an oncogene with constitutively expressed, cytosolic hsp73 facilitates cross-priming in vitro and in vivo of CTL by DC that process material from apoptotic cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigen Presentation*
  • Antigens, Polyomavirus Transforming / genetics
  • Antigens, Polyomavirus Transforming / immunology*
  • Antigens, Polyomavirus Transforming / metabolism
  • Cancer Vaccines
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cells, Cultured
  • Dendritic Cells / immunology*
  • Endocytosis
  • Epitopes, T-Lymphocyte / immunology
  • HSC70 Heat-Shock Proteins
  • HSP70 Heat-Shock Proteins*
  • Interferon-gamma / biosynthesis
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mutation
  • Neoplasms / immunology*
  • Neoplasms / therapy
  • T-Lymphocytes, Cytotoxic / immunology*
  • Tumor Cells, Cultured
  • Vaccines, DNA

Substances

  • Antigens, Polyomavirus Transforming
  • Cancer Vaccines
  • Carrier Proteins
  • Epitopes, T-Lymphocyte
  • HSC70 Heat-Shock Proteins
  • HSP70 Heat-Shock Proteins
  • Hspa8 protein, mouse
  • Vaccines, DNA
  • Interferon-gamma