Altered peptide ligands revisited: vaccine design through chemically modified HLA-A2-restricted T cell epitopes

J Immunol. 2014 Nov 15;193(10):4803-13. doi: 10.4049/jimmunol.1400800. Epub 2014 Oct 13.

Abstract

Virus or tumor Ag-derived peptides that are displayed by MHC class I molecules are attractive starting points for vaccine development because they induce strong protective and therapeutic cytotoxic T cell responses. In thus study, we show that the MHC binding and consequent T cell reactivity against several HLA-A*02 restricted epitopes can be further improved through the incorporation of nonproteogenic amino acids at primary and secondary anchor positions. We screened more than 90 nonproteogenic, synthetic amino acids through a range of epitopes and tested more than 3000 chemically enhanced altered peptide ligands (CPLs) for binding affinity to HLA-A*0201. With this approach, we designed CPLs of viral epitopes, of melanoma-associated Ags, and of the minor histocompatibility Ag UTA2-1, which is currently being evaluated for its antileukemic activity in clinical dendritic cell vaccination trials. The crystal structure of one of the CPLs in complex with HLA-A*0201 revealed the molecular interactions likely responsible for improved binding. The best CPLs displayed enhanced affinity for MHC, increasing MHC stability and prolonging recognition by Ag-specific T cells and, most importantly, they induced accelerated expansion of antitumor T cell frequencies in vitro and in vivo as compared with the native epitope. Eventually, we were able to construct a toolbox of preferred nonproteogenic residues with which practically any given HLA-A*02 restricted epitope can be readily optimized. These CPLs could improve the therapeutic outcome of vaccination strategies or can be used for ex vivo enrichment and faster expansion of Ag-specific T cells for transfer into patients.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Antigens, Neoplasm / chemistry
  • Antigens, Neoplasm / genetics
  • Antigens, Neoplasm / immunology*
  • B-Lymphocytes
  • Cancer Vaccines / administration & dosage
  • Cancer Vaccines / chemistry
  • Cancer Vaccines / immunology*
  • Crystallography, X-Ray
  • Epitopes
  • Gene Expression
  • HLA-A2 Antigen / chemistry
  • HLA-A2 Antigen / genetics
  • HLA-A2 Antigen / immunology*
  • Humans
  • Immunization
  • Mice
  • Mice, Transgenic
  • Minor Histocompatibility Antigens / chemistry
  • Minor Histocompatibility Antigens / genetics
  • Minor Histocompatibility Antigens / immunology
  • Models, Molecular
  • Molecular Sequence Data
  • Neoplasms / immunology
  • Neoplasms / prevention & control*
  • Peptides / administration & dosage
  • Peptides / chemistry
  • Peptides / genetics
  • Peptides / immunology*
  • Protein Binding
  • Recombinant Proteins / genetics
  • Recombinant Proteins / immunology
  • T-Lymphocytes, Cytotoxic / cytology
  • T-Lymphocytes, Cytotoxic / immunology
  • T-Lymphocytes, Cytotoxic / metabolism

Substances

  • Antigens, Neoplasm
  • Cancer Vaccines
  • Epitopes
  • HLA-A*02:01 antigen
  • HLA-A2 Antigen
  • Minor Histocompatibility Antigens
  • Peptides
  • Recombinant Proteins

Associated data

  • PDB/4WJ5