BCL-6 suppresses miR-142-3p/5p expression in SLE CD4+ T cells by modulating histone methylation and acetylation of the miR-142 promoter

Cell Mol Immunol. 2020 May;17(5):474-482. doi: 10.1038/s41423-019-0268-3. Epub 2019 Aug 20.

Abstract

The reduced expression of miR-142-3p/5p in CD4+ T cells of SLE patients caused T cell hyperactivity and B cell hyperstimulation. This study aimed to investigate the mechanisms of regulating miR-142-3p/5p expression in SLE CD4+ T cells. The BCL-6 expression was significantly increased in SLE CD4+ T cells compared with normal controls, and the BCL-6 expression was inversely correlated with miR-142-3p/5p expression. BCL-6 suppresses the expression of miR-142-3p/5p by increasing H3K27me3 level and reducing H3K9/K14ac levels in SLE CD4+ T cells. BCL-6 regulates histone modifications in miR-142 promoter by recruiting EZH2 and HDAC5. Furthermore, we observed significantly decreased CD40L, ICOS, and IL-21 expression levels in SLE CD4+ T cells with BCL-6 interference, and obviously reduced autoantibody IgG production in autologous B cells co-cultured with BCL-6 inhibited SLE CD4+ T cells. Our study found that increased BCL-6 up-regulates H3K27me3 and down-regulates H3K9/14ac at miR-142 promoter in SLE CD4+ T cells. These factors induce a declination in miR-142-3p/5p expression, consequently resulting in CD4+ T cell hyperactivity.

Keywords: BCL-6; EZH2; HDAC5; SLE; miR-142-3p/5p.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Adolescent
  • Adult
  • CD4-Positive T-Lymphocytes / immunology*
  • Case-Control Studies
  • Enhancer of Zeste Homolog 2 Protein / metabolism
  • Female
  • Histone Deacetylases / metabolism
  • Histones / metabolism*
  • Humans
  • Lupus Erythematosus, Systemic / genetics*
  • Lupus Erythematosus, Systemic / immunology*
  • Methylation
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Middle Aged
  • Promoter Regions, Genetic*
  • Protein Binding
  • Proto-Oncogene Proteins c-bcl-6 / genetics
  • Proto-Oncogene Proteins c-bcl-6 / metabolism*
  • Up-Regulation / genetics
  • Young Adult

Substances

  • BCL6 protein, human
  • Histones
  • MIRN142 microRNA, human
  • MicroRNAs
  • Proto-Oncogene Proteins c-bcl-6
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • HDAC5 protein, human
  • Histone Deacetylases