The RNA helicase DDX39B activates FOXP3 RNA splicing to control T regulatory cell fate

Elife. 2023 Jun 1:12:e76927. doi: 10.7554/eLife.76927.

Abstract

Genes associated with increased susceptibility to multiple sclerosis (MS) have been identified, but their functions are incompletely understood. One of these genes codes for the RNA helicase DExD/H-Box Polypeptide 39B (DDX39B), which shows genetic and functional epistasis with interleukin-7 receptor-α gene (IL7R) in MS-risk. Based on evolutionary and functional arguments, we postulated that DDX39B enhances immune tolerance thereby decreasing MS risk. Consistent with such a role we show that DDX39B controls the expression of many MS susceptibility genes and important immune-related genes. Among these we identified Forkhead Box P3 (FOXP3), which codes for the master transcriptional factor in CD4+/CD25+ T regulatory cells. DDX39B knockdown led to loss of immune-regulatory and gain of immune-effector expression signatures. Splicing of FOXP3 introns, which belong to a previously unrecognized type of introns with C-rich polypyrimidine tracts, was exquisitely sensitive to DDX39B levels. Given the importance of FOXP3 in autoimmunity, this work cements DDX39B as an important guardian of immune tolerance.

Keywords: DDX39B; FOXP3; RNA helicase; RNA splicing; autoimmunity; biochemistry; chemical biology; human; immunology; inflammation; multiple sclerosis.

Publication types

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

MeSH terms

  • DEAD-box RNA Helicases / genetics
  • DEAD-box RNA Helicases / metabolism
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / metabolism
  • Gene Expression Regulation
  • Humans
  • Multiple Sclerosis* / genetics
  • RNA Splicing
  • T-Lymphocytes, Regulatory*

Substances

  • DEAD-box RNA Helicases
  • Forkhead Transcription Factors
  • DDX39B protein, human
  • FOXP3 protein, human

Associated data

  • GEO/GSE145773