NF-κB-driven miR-34a impairs Treg/Th17 balance via targeting Foxp3

J Autoimmun. 2019 Aug:102:96-113. doi: 10.1016/j.jaut.2019.04.018. Epub 2019 May 23.

Abstract

The subset of regulatory T (Treg) cells, with its specific transcription Foxp3, is a unique cell type for the maintenance of immune homeostasis by controlling effector T (Teff) cell responses. Although it is common that a defect in Treg cells with Treg/Teff disorder causes autoimmune diseases; however, the precise mechanisms are not thoroughly revealed. Here, we report that miR-34a could attenuate human and murine Foxp3 gene expression via targeting their 3' untranslated regions (3' UTR). The human miR-34a, increased in peripheral blood mononuclear cells (PBMCs) and CD4+ T cells from rheumatoid arthritis (RA) or systemic lupus erythematosus (SLE) patients, displayed a positive correlation with some serum markers of inflammation including rheumatoid factor (RF), anti-streptolysin antibody (ASO), erythrocyte sedimentation rate (ESR) and C-reactive protein (CRP) as well as Th17 signature gene RORγt, but inversely correlated with the mRNA expression levels of FOXP3. In addition, murine miR-34a levels were downregulated in TGF-β-induced Treg cells but upregulated in Th17 cells induced in vitro compared to activated CD4+ T cells. It has also been demonstrated that elevated miR-34a disrupting Treg/Th17 balance in vivo contributed to the progress of pathogenesis of collagen induced arthritis (CIA) mice. Furthermore, IL-6 and TNF-α were responsible for the upregulation of miR-34a and downregulation of Foxp3, which was reverted by the addition of NF-κB/p65 inhibitor BAY11-7082, thus indicating that NF-κB/p65 inhibited Foxp3 expression in an miR-34a-dependent manner. Finally, IL-6 or TNF-α-activated p65 could bind to the miR-34a promotor and enhance its activity, resulting in upregulation of its transcription. Taken together, we show that NF-κB activated by inflammatory cytokines, such as IL-6 and TNF-α, ameliorates Foxp3 levels via regulating miR-34a expression, which provides a new mechanistic and therapeutic insight into the ongoing of autoimmune diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions / genetics
  • Adult
  • Aged
  • Animals
  • Antistreptolysin / blood
  • Arthritis, Rheumatoid / immunology*
  • Blood Sedimentation
  • C-Reactive Protein / analysis
  • Cell Line
  • Female
  • Forkhead Transcription Factors / metabolism*
  • HEK293 Cells
  • Humans
  • Interleukin-6 / immunology*
  • Leukocytes, Mononuclear / immunology
  • Lupus Erythematosus, Systemic / immunology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / genetics*
  • Middle Aged
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / blood
  • Promoter Regions, Genetic
  • Rheumatoid Factor / blood
  • T-Lymphocytes, Regulatory / cytology
  • T-Lymphocytes, Regulatory / immunology
  • Th17 Cells / cytology
  • Th17 Cells / immunology
  • Transcription Factor RelA / antagonists & inhibitors
  • Transcription Factor RelA / metabolism*
  • Tumor Necrosis Factor-alpha / immunology*

Substances

  • 3' Untranslated Regions
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • IL6 protein, human
  • Interleukin-6
  • MIRN34 microRNA, human
  • MicroRNAs
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • RELA protein, human
  • RORC protein, human
  • TNF protein, human
  • Transcription Factor RelA
  • Tumor Necrosis Factor-alpha
  • Antistreptolysin
  • C-Reactive Protein
  • Rheumatoid Factor