Comparison of vaccine-induced effector CD8 T cell responses directed against self- and non-self-tumor antigens: implications for cancer immunotherapy

J Immunol. 2013 Oct 1;191(7):3955-67. doi: 10.4049/jimmunol.1300555. Epub 2013 Sep 9.

Abstract

It is generally accepted that CD8 T cells play a major role in tumor control, yet vaccination aimed at eliciting potent CD8 T cell responses are rarely efficient in clinical trials. To try and understand why this is so, we have generated potent adenoviral vectors encoding the endogenous tumor Ags (TA) tyrosinase-related protein-2 (TRP-2) and glycoprotein 100 (GP100) tethered to the invariant chain (Ii). Using these vectors, we sought to characterize the self-TA-specific CD8 T cell response and compare it to that induced against non-self-Ags expressed from a similar vector platform. Prophylactic vaccination with adenoviral vectors expressing either TRP-2 (Ad-Ii-TRP-2) or GP100 (Ad-Ii-GP100) had little or no effect on the growth of s.c. B16 melanomas, and only Ad-Ii-TRP-2 was able to induce a marginal reduction of B16 lung metastasis. In contrast, vaccination with a similar vector construct expressing a foreign (viral) TA induced efficient tumor control. Analyzing the self-TA-specific CD8 T cells, we observed that these could be activated to produce IFN-γ and TNF-α. In addition, surface expression of phenotypic markers and inhibitory receptors, as well as in vivo cytotoxicity and degranulation capacity matched that of non-self-Ag-specific CD8 T cells. However, the CD8 T cells specific for self-TAs had a lower functional avidity, and this impacted on their in vivo performance. On the basis of these results and a low expression of the targeted TA epitopes on the tumor cells, we suggest that low avidity of the self-TA-specific CD8 T cells may represent a major obstacle for efficient immunotherapy of cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoviridae / genetics
  • Animals
  • Antigens, Neoplasm / immunology*
  • Autoantigens / immunology
  • CD8-Positive T-Lymphocytes / immunology*
  • Cancer Vaccines / immunology*
  • Cell Degranulation / immunology
  • Cell Line, Tumor
  • Cytotoxicity, Immunologic
  • Epitopes, T-Lymphocyte / immunology
  • Epitopes, T-Lymphocyte / metabolism
  • Female
  • Genetic Vectors / genetics
  • Immunotherapy
  • Interferon-gamma / biosynthesis
  • Intramolecular Oxidoreductases / immunology
  • Intramolecular Oxidoreductases / metabolism
  • Lung Neoplasms / immunology
  • Lung Neoplasms / secondary
  • Lung Neoplasms / therapy
  • Melanocytes / immunology
  • Mice
  • Neoplasms / immunology*
  • Neoplasms / therapy
  • Phenotype
  • Protein Binding / immunology
  • Receptors, Antigen, T-Cell / immunology
  • Receptors, Antigen, T-Cell / metabolism
  • T-Lymphocytes, Regulatory / immunology
  • Transduction, Genetic
  • gp100 Melanoma Antigen / immunology
  • gp100 Melanoma Antigen / metabolism

Substances

  • Antigens, Neoplasm
  • Autoantigens
  • Cancer Vaccines
  • Epitopes, T-Lymphocyte
  • Receptors, Antigen, T-Cell
  • gp100 Melanoma Antigen
  • Interferon-gamma
  • Intramolecular Oxidoreductases
  • dopachrome isomerase