Tumor-specific T cells in human Merkel cell carcinomas: a possible role for Tregs and T-cell exhaustion in reducing T-cell responses

J Invest Dermatol. 2013 Jul;133(7):1879-89. doi: 10.1038/jid.2013.75. Epub 2013 Feb 18.

Abstract

Merkel cell carcinomas (MCCs) are rare but highly malignant skin cancers associated with a recently described polyomavirus. MCC tumors were infiltrated by T cells, including effector, central memory, and regulatory T cells. Infiltrating T cells showed markedly reduced activation as evidenced by reduced expression of CD69 and CD25. Treatment of MCC tumors in vitro with IL-2 and IL-15 led to T-cell activation, proliferation, enhanced cytokine production, and loss of viable tumor cells from cultures. Expanded tumor-infiltrating lymphocytes showed TCR repertoire skewing and upregulation of CD137. MCC tumors implanted into immunodeficient mice failed to grow unless human T cells in the tumor grafts were depleted with denileukin diftitox, suggesting that tumor-specific T cells capable of controlling tumor growth were present in MCC. Both CD4(+) and CD8(+) FOXP3(+) regulatory T cells were frequent in MCC. Fifty percent of nonactivated T cells in MCC-expressed PD-1, a marker of T-cell exhaustion, and PD-L1 and PD-L2 were expressed by a subset of tumor dendritic cells and macrophages. In summary, we observed tumor-specific T cells with suppressed activity in MCC tumors. Agents that stimulate T-cell activity, block regulatory T cell function, or inhibit PD-1 signaling may be effective in the treatment of this highly malignant skin cancer.

Publication types

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

MeSH terms

  • Animals
  • Antigens, CD / metabolism
  • Antigens, Differentiation, T-Lymphocyte / metabolism
  • CD8 Antigens / metabolism
  • Carcinoma, Merkel Cell / metabolism
  • Carcinoma, Merkel Cell / pathology*
  • Carcinoma, Squamous Cell / metabolism
  • Carcinoma, Squamous Cell / pathology
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Cytokines / metabolism
  • Forkhead Transcription Factors / metabolism
  • Humans
  • In Vitro Techniques
  • Interleukin-15 / pharmacology
  • Interleukin-2 / pharmacology
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Lectins, C-Type / metabolism
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Programmed Cell Death 1 Receptor / metabolism*
  • Signal Transduction / physiology
  • Skin / metabolism
  • Skin / pathology
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / pathology*
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / metabolism*
  • T-Lymphocytes / pathology*
  • T-Lymphocytes, Regulatory / metabolism*
  • T-Lymphocytes, Regulatory / pathology*
  • Transplantation, Heterologous

Substances

  • Antigens, CD
  • Antigens, Differentiation, T-Lymphocyte
  • CD69 antigen
  • CD8 Antigens
  • Cytokines
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Interleukin-15
  • Interleukin-2
  • Interleukin-2 Receptor alpha Subunit
  • Lectins, C-Type
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor