Coordinated regulation of IFITM1, 2 and 3 genes by an IFN-responsive enhancer through long-range chromatin interactions

Biochim Biophys Acta Gene Regul Mech. 2017 Aug;1860(8):885-893. doi: 10.1016/j.bbagrm.2017.05.003. Epub 2017 May 13.

Abstract

Interferon-induced transmembrane protein (IFITM) 1, 2 and 3 genes encode a family of interferon (IFN)-induced transmembrane proteins that block entry of a broad spectrum of pathogens. However, the transcriptional regulation of these genes, especially whether there exist any enhancers and their roles during the IFN induction process remain elusive. Here, through public data mining, episomal luciferase reporter assay and in vivo CRISPR-Cas9 genome editing, we identified an IFN-responsive enhancer located 35kb upstream of IFITM3 gene promoter upregulating the IFN-induced expression of IFITM1, 2 and 3 genes. Chromatin immunoprecipitation (ChIP), electrophoretic mobility shift assay (EMSA) and luciferase reporter assay demonstrated that signal transducers and activators of transcription (STAT) 1 bound to the enhancer with the treatment of IFN and was indispensable for the enhancer activity. Furthermore, using chromosome conformation capture technique, we revealed that the IFITM1, 2 and 3 genes physically clustered together and constitutively looped to the distal enhancer through long-range interactions in both HEK293 and A549 cells, providing structural basis for coordinated regulation of IFITM1, 2 and 3 by the enhancer. Finally, we showed that in vivo truncation of the enhancer impaired IFN-induced resistance to influenza A virus (IAV) infection. These findings expand our understanding of the mechanisms underlying the transcriptional regulation of IFITM1, 2 and 3 expression and its ability to mediate IFN signaling.

Keywords: Enhancer; IFITM; IFN; Influenza A virus; Long-range interactions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A549 Cells
  • Antigens, Differentiation / genetics*
  • Cell Line
  • Cell Line, Tumor
  • Chromatin / genetics*
  • Clustered Regularly Interspaced Short Palindromic Repeats / genetics
  • Enhancer Elements, Genetic / genetics*
  • Gene Editing / methods
  • Gene Expression Regulation / genetics
  • HEK293 Cells
  • Humans
  • Influenza A virus / pathogenicity
  • Influenza, Human / genetics
  • Interferons / genetics*
  • Membrane Proteins / genetics*
  • Promoter Regions, Genetic / genetics
  • RNA-Binding Proteins / genetics*
  • STAT1 Transcription Factor / genetics
  • Signal Transduction / genetics
  • Transcriptional Activation / genetics
  • Up-Regulation / genetics

Substances

  • Antigens, Differentiation
  • Chromatin
  • IFITM2 protein, human
  • IFITM3 protein, human
  • Membrane Proteins
  • RNA-Binding Proteins
  • STAT1 Transcription Factor
  • leu-13 antigen
  • Interferons