Possible mechanisms of the crosstalk between Langerhans cells and regulatory T cells in extramammary Paget disease by receptor activator of nuclear factor kappa B (RANK) ligand/RANK pathways

Br J Dermatol. 2017 Feb;176(2):387-394. doi: 10.1111/bjd.14864. Epub 2016 Dec 22.

Abstract

Background: Extramammary Paget disease (EMPD) is a skin adenocarcinoma of apocrine gland origin, in which Paget cells express receptor activator of nuclear factor kappa B (RANK) ligand (RANKL) and matrix metalloproteinase (MMP)-7, and release soluble (s)RANKL into the tumour microenvironment. We previously reported that about 60% of the RANK+ cells among the stromal cells are M2 macrophages, but the identity of the remaining population of RANK+ cells is still unknown.

Objectives: To investigate the unknown subpopulation of RANK-expressing cells in EMPD.

Methods: The main population of RANK-expressing cells in the epidermis was composed of epidermal Langerhans cells (LCs). To explore the effects of RANKL on LCs, we stimulated LCs generated from human CD34+ hematopoietic progenitor cells with graded concentrations of sRANKL. To further examine the correlation between LCs and regulatory T cells (Tregs) in EMPD, we employed immunohistochemical staining.

Results: sRANKL stimulation was shown to augment the production of C-C motif chemokine ligand 17 (CCL17) from LCs. We additionally demonstrated CCL17 expression by CD1a+ LCs in EMPD in an immunofluorescence study. Spearman's rank correlation test confirmed a correlation between the number of LCs and the number of Foxp3+ Tregs in the lesional skin of invasive EMPD. In addition, the numbers of Foxp3+ Tregs in the sentinel lymph nodes of metastatic EMPD were significantly higher than those of metastatic melanoma, which did not express RANKL.

Conclusions: The findings suggest that the RANKL/RANK pathway in EMPD might contribute to the recruitment of Tregs and to maintenance of the tumour microenvironment.

MeSH terms

  • Chemokine CCL17 / metabolism
  • Forkhead Transcription Factors / metabolism
  • Humans
  • Langerhans Cells / physiology*
  • Lymphatic Metastasis
  • NF-kappa B / metabolism*
  • Paget Disease, Extramammary / metabolism*
  • RANK Ligand / metabolism*
  • Receptor Cross-Talk / physiology
  • Skin Neoplasms / metabolism*
  • T-Lymphocytes, Regulatory / physiology*
  • Tumor Cells, Cultured

Substances

  • Chemokine CCL17
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • NF-kappa B
  • RANK Ligand