Merkel cell polyomavirus-specific CD8⁺ and CD4⁺ T-cell responses identified in Merkel cell carcinomas and blood

Clin Cancer Res. 2011 Nov 1;17(21):6671-80. doi: 10.1158/1078-0432.CCR-11-1513. Epub 2011 Sep 9.

Abstract

Purpose: Merkel cell polyomavirus (MCPyV) is prevalent in the general population, integrates into most Merkel cell carcinomas (MCC), and encodes oncoproteins required for MCC tumor growth. We sought to characterize T-cell responses directed against viral proteins that drive this cancer as a step toward immunotherapy.

Experimental design: Intracellular cytokine cytometry, IFN-γ enzyme-linked immunospot (ELISPOT) assay, and a novel HLA-A*2402-restricted MCPyV tetramer were used to identify and characterize T-cell responses against MCPyV oncoproteins in tumors and blood of MCC patients and control subjects.

Results: We isolated virus-reactive CD8 or CD4 T cells from MCPyV-positive MCC tumors (2 of 6) but not from virus-negative tumors (0 of 4). MCPyV-specific T-cell responses were also detected in the blood of MCC patients (14 of 27) and control subjects (5 of 13). These T cells recognized a broad range of peptides derived from capsid proteins (2 epitopes) and oncoproteins (24 epitopes). HLA-A*2402-restricted MCPyV oncoprotein processing and presentation by mammalian cells led to CD8-mediated cytotoxicity. Virus-specific CD8 T cells were markedly enriched among tumor infiltrating lymphocytes as compared with blood, implying intact T-cell trafficking into the tumor. Although tetramer-positive CD8 T cells were detected in the blood of 2 of 5 HLA-matched MCC patients, these cells failed to produce IFN-γ when challenged ex vivo with peptide.

Conclusions: Our findings suggest that MCC tumors often develop despite the presence of T cells specific for MCPyV T-Ag oncoproteins. The identified epitopes may be candidates for peptide-specific vaccines and tumor- or virus-specific adoptive immunotherapies to overcome immune evasion mechanisms in MCC patients.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Viral, Tumor / immunology
  • CD4-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / immunology*
  • COS Cells
  • Carcinoma, Merkel Cell / blood
  • Carcinoma, Merkel Cell / immunology*
  • Carcinoma, Merkel Cell / virology
  • Chlorocebus aethiops
  • Epitope Mapping
  • Epitopes, T-Lymphocyte / immunology
  • HLA-A24 Antigen / immunology
  • Humans
  • Interferon-gamma / biosynthesis
  • Interferon-gamma / immunology
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Merkel cell polyomavirus / immunology*
  • Peptides / immunology
  • Polyomavirus Infections / blood
  • Polyomavirus Infections / immunology*
  • Polyomavirus Infections / virology
  • Skin Neoplasms / blood
  • Skin Neoplasms / immunology*
  • Skin Neoplasms / virology
  • Tumor Virus Infections / blood
  • Tumor Virus Infections / immunology*
  • Tumor Virus Infections / virology

Substances

  • Antigens, Viral, Tumor
  • Epitopes, T-Lymphocyte
  • HLA-A*24:02 antigen
  • HLA-A24 Antigen
  • Peptides
  • Interferon-gamma