Merkel polyomavirus-specific T cells fluctuate with merkel cell carcinoma burden and express therapeutically targetable PD-1 and Tim-3 exhaustion markers

Clin Cancer Res. 2013 Oct 1;19(19):5351-60. doi: 10.1158/1078-0432.CCR-13-0035. Epub 2013 Aug 6.

Abstract

Purpose: The persistent expression of Merkel cell polyomavirus (MCPyV) oncoproteins in Merkel cell carcinoma (MCC) provides a unique opportunity to characterize immune evasion mechanisms in human cancer. We isolated MCPyV-specific T cells and determined their frequency and functional status.

Experimental design: Multiparameter flow cytometry panels and HLA/peptide tetramers were used to identify and characterize T cells from tumors (n = 7) and blood (n = 18) of patients with MCC and control subjects (n = 10). PD-1 ligand (PD-L1) and CD8 expression within tumors were determined using mRNA profiling (n = 35) and immunohistochemistry (n = 13).

Results: MCPyV-specific CD8 T cells were detected directly ex vivo from the blood samples of 7 out of 11 (64%) patients with MCPyV-positive tumors. In contrast, 0 of 10 control subjects had detectable levels of these cells in their blood (P < 0.01). MCPyV-specific T cells in serial blood specimens increased with MCC disease progression and decreased with effective therapy. MCPyV-specific CD8 T cells and MCC-infiltrating lymphocytes expressed higher levels of therapeutically targetable PD-1 and Tim-3 inhibitory receptors compared with T cells specific to other human viruses (P < 0.01). PD-L1 was present in 9 of 13 (69%) MCCs and its expression was correlated with CD8-lymphocyte infiltration.

Conclusions: MCC-targeting T cells expand with tumor burden and express high levels of immune checkpoint receptors PD-1 and Tim-3. Reversal of these inhibitory pathways is therefore a promising therapeutic approach for this virus-driven cancer.

Publication types

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

MeSH terms

  • Antibodies, Viral / immunology
  • Antigens, Viral / immunology
  • Antigens, Viral / metabolism
  • Biomarkers / metabolism
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Carcinoma, Merkel Cell / immunology*
  • Carcinoma, Merkel Cell / metabolism*
  • Carcinoma, Merkel Cell / pathology
  • Carcinoma, Merkel Cell / virology
  • Case-Control Studies
  • Hepatitis A Virus Cellular Receptor 2
  • Immunohistochemistry
  • Immunophenotyping
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Lymphocytes, Tumor-Infiltrating / metabolism
  • Membrane Proteins / metabolism*
  • Merkel cell polyomavirus / immunology*
  • Oncogene Proteins, Viral / immunology
  • Oncogene Proteins, Viral / metabolism
  • Programmed Cell Death 1 Receptor / metabolism*
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / metabolism
  • Tumor Burden / immunology

Substances

  • Antibodies, Viral
  • Antigens, Viral
  • Biomarkers
  • HAVCR2 protein, human
  • Hepatitis A Virus Cellular Receptor 2
  • Membrane Proteins
  • Oncogene Proteins, Viral
  • Programmed Cell Death 1 Receptor