IL-4 Inhibits the Biogenesis of an Epigenetically Suppressive PIWI-Interacting RNA To Upregulate CD1a Molecules on Monocytes/Dendritic Cells

J Immunol. 2016 Feb 15;196(4):1591-603. doi: 10.4049/jimmunol.1500805. Epub 2016 Jan 11.

Abstract

The discovery of PIWI-interacting RNAs (piRNAs) revealed the complexity of the RNA world. Although piRNAs were first deemed to be germline specific, substantial evidence shows their various roles in somatic cells; however, their function in highly differentiated immune cells remains elusive. In this study, by initially screening with a small RNA deep-sequencing analysis, we found that a piRNA, tRNA-Glu-derived piRNA [td-piR(Glu)], was expressed much more abundantly in human monocytes than in dendritic cells. By regulating the polymerase III activity, IL-4 potently decreased the biogenesis of tRNA-Glu and, subsequently, td-piR(Glu). Further, we revealed that the td-piR(Glu)/PIWIL4 complex recruited SETDB1, SUV39H1, and heterochromatin protein 1β to the CD1A promoter region and facilitated H3K9 methylation. As a result, the transcription of CD1A was significantly inhibited. Collectively, we demonstrated that a piRNA acted as the signal molecule for a cytokine to regulate the expression of an important membrane protein for lipid Ag presentation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, CD1 / genetics*
  • Antigens, CD1 / immunology
  • Cells, Cultured
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Epigenomics
  • HEK293 Cells
  • Heterochromatin / metabolism
  • Humans
  • Interleukin-4 / metabolism*
  • Monocytes / immunology*
  • Promoter Regions, Genetic
  • RNA, Small Interfering / genetics*
  • RNA, Small Interfering / metabolism
  • Sequence Analysis, DNA
  • Signal Transduction
  • Transcriptional Activation
  • Up-Regulation

Substances

  • Antigens, CD1
  • CD1a antigen
  • Heterochromatin
  • RNA, Small Interfering
  • Interleukin-4