IFIT1 Exerts Opposing Regulatory Effects on the Inflammatory and Interferon Gene Programs in LPS-Activated Human Macrophages

Cell Rep. 2018 Oct 2;25(1):95-106.e6. doi: 10.1016/j.celrep.2018.09.002.

Abstract

Activation of the TLR4 signaling pathway by lipopolysaccharide (LPS) leads to induction of both inflammatory and interferon-stimulated genes, but the mechanisms through which these coordinately activated transcriptional programs are balanced to promote an optimal innate immune response remain poorly understood. In a genome-wide small interfering RNA (siRNA) screen of the LPS-induced tumor necrosis factor α (TNF-α) response in macrophages, we identify the interferon-stimulated protein IFIT1 as a negative regulator of the inflammatory gene program. Transcriptional profiling further identifies a positive regulatory role for IFIT1 in type I interferon expression, implicating IFIT1 as a reciprocal modulator of LPS-induced gene classes. We demonstrate that these effects of IFIT1 are mediated through modulation of a Sin3A-HDAC2 transcriptional regulatory complex at LPS-induced gene loci. Beyond the well-studied role of cytosolic IFIT1 in restricting viral replication, our data demonstrate a function for nuclear IFIT1 in differential transcriptional regulation of separate branches of the LPS-induced gene program.

Keywords: IFIT1; RNAi screen; TLR4; TNF-α; interferon; interferon gene program; pro-inflammatory gene program.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics*
  • Adaptor Proteins, Signal Transducing / immunology*
  • Animals
  • Gene Expression Profiling
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / immunology
  • HEK293 Cells
  • Humans
  • Inflammation / genetics
  • Inflammation / immunology
  • Interferon Regulatory Factor-3 / genetics
  • Interferon Regulatory Factor-3 / immunology
  • Interferon Type I / genetics*
  • Interferon Type I / immunology*
  • Lipopolysaccharides / pharmacology
  • Macrophage Activation / drug effects
  • Macrophages / drug effects
  • Macrophages / immunology*
  • Mice
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / immunology*
  • Repressor Proteins / genetics
  • Repressor Proteins / immunology
  • Signal Transduction
  • Sin3 Histone Deacetylase and Corepressor Complex
  • Tumor Necrosis Factor-alpha / immunology
  • U937 Cells

Substances

  • Adaptor Proteins, Signal Transducing
  • IFIT1 protein, human
  • IRF3 protein, human
  • Ifit1 protein, mouse
  • Interferon Regulatory Factor-3
  • Interferon Type I
  • Lipopolysaccharides
  • RNA-Binding Proteins
  • Repressor Proteins
  • SIN3A transcription factor
  • TNF protein, human
  • Tumor Necrosis Factor-alpha
  • Sin3 Histone Deacetylase and Corepressor Complex