The DNA methylation signature of human TCRαβ+CD4-CD8- double negative T cells reveals CG demethylation and a unique epigenetic architecture permissive to a broad stimulatory immune response

Clin Immunol. 2015 Jan;156(1):19-27. doi: 10.1016/j.clim.2014.10.007. Epub 2014 Oct 29.

Abstract

T cell receptor (TCR) αβ+CD4-CD8- double negative T cells represent a rare T cell subset implicated in the pathogenesis of several autoimmune diseases. We investigated the DNA methylation signature of double negative T cells to gain insight into the epigenetic architecture of peripheral blood primary human double negative T cells compared to autologous CD4+ and CD8+ T cells. We identified 2984 CG sites across the genome with unique loss of DNA methylation in double negative T cells, and showed significant reduction in mRNA expression of DNA methyltransferases DNMT1, DNMT3A, and DNMT3B. DNA methylation was increased in CD8A/CD8B and CD4 consistent with epigenetic repression of both the CD8 and CD4 genetic loci in double negative T cells. We show a consistent increase in non-CG methylation in double negative T cells, a finding suggestive of pluripotency. Network analyses indicate a strong relationship between double negative T cells and functions related to cell-cell interaction, cell adhesion, and cell activation pathways. Our data also suggest a robust pro-inflammatory epigenetic signature in double negative T cells, consistent with a transcriptional permissiveness in key inflammatory cytokines including IFNγ, IL-17F, IL-12B, IL-5, IL-18, TNFSF11 (RANKL), and TNFSF13B (BLYS or BAFF). These findings highlight an epigenetic basis for a role of double negative T cells in autoimmunity.

Keywords: DNA methylation; Double negative; Epigenome; Methylome; T cell.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • CD4-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Computational Biology
  • Cytosine / chemistry
  • DNA (Cytosine-5-)-Methyltransferases / genetics
  • DNA (Cytosine-5-)-Methyltransferases / metabolism
  • DNA Methylation*
  • DNA Methyltransferase 3A
  • DNA Methyltransferase 3B
  • Down-Regulation
  • Epigenesis, Genetic / immunology*
  • Female
  • Flow Cytometry
  • Guanine / chemistry
  • Humans
  • Middle Aged
  • Receptors, Antigen, T-Cell, alpha-beta / metabolism*
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • T-Lymphocytes / immunology*

Substances

  • DMAP1 protein, human
  • DNMT3A protein, human
  • Receptors, Antigen, T-Cell, alpha-beta
  • Repressor Proteins
  • Guanine
  • Cytosine
  • DNA (Cytosine-5-)-Methyltransferases
  • DNA Methyltransferase 3A