Efficient cross-presentation by heat shock protein 90-peptide complex-loaded dendritic cells via an endosomal pathway

J Immunol. 2007 Aug 1;179(3):1803-13. doi: 10.4049/jimmunol.179.3.1803.

Abstract

It is well-established that heat shock proteins (HSPs)-peptides complexes elicit antitumor responses in prophylactic and therapeutic immunization protocols. HSPs such as gp96 and Hsp70 have been demonstrated to undergo receptor-mediated uptake by APCs with subsequent representation of the HSP-associated peptides to MHC class I molecules on APCs, facilitating efficient cross-presentation. On the contrary, despite its abundant expression among HSPs in the cytosol, the role of Hsp90 for the cross-presentation remains unknown. We show here that exogenous Hsp90-peptide complexes can gain access to the MHC class I presentation pathway and cause cross-presentation by bone marrow-derived dendritic cells. Interestingly, this presentation is TAP independent, and followed chloroquine, leupeptin-sensitive, as well as cathepsin S-dependent endosomal pathways. In addition, we show that Hsp90-chaperoned precursor peptides are processed and transferred onto MHC class I molecules in the endosomal compartment. Furthermore, we demonstrate that immunization with Hsp90-peptide complexes induce Ag-specific CD8(+) T cell responses and strong antitumor immunity in vivo. These findings have significant implications for the design of T cell-based cancer immunotherapy.

MeSH terms

  • Animals
  • Bone Marrow Cells / immunology
  • Bone Marrow Cells / metabolism
  • Cancer Vaccines / administration & dosage
  • Cancer Vaccines / immunology
  • Cancer Vaccines / metabolism
  • Cell Line, Tumor
  • Clone Cells
  • Cross-Priming / immunology*
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Endosomes / immunology*
  • Endosomes / metabolism
  • HSP90 Heat-Shock Proteins / administration & dosage
  • HSP90 Heat-Shock Proteins / immunology*
  • HSP90 Heat-Shock Proteins / metabolism
  • HeLa Cells
  • Histocompatibility Antigens Class I / immunology
  • Histocompatibility Antigens Class I / metabolism
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Peptide Fragments / immunology*
  • Peptide Fragments / metabolism
  • Protein Transport / immunology
  • Signal Transduction / immunology*
  • T-Lymphocytes, Cytotoxic / immunology
  • Thymoma / immunology
  • Thymoma / metabolism
  • Thymoma / prevention & control

Substances

  • Cancer Vaccines
  • HSP90 Heat-Shock Proteins
  • Histocompatibility Antigens Class I
  • Peptide Fragments