The role of Ets2 transcription factor in the induction of microRNA-155 (miR-155) by lipopolysaccharide and its targeting by interleukin-10

J Biol Chem. 2014 Feb 14;289(7):4316-25. doi: 10.1074/jbc.M113.522730. Epub 2013 Dec 20.

Abstract

MicroRNA-155 (miR-155) is highly expressed in many cancers such as B cell lymphomas and myeloid leukemia and inflammatory disorders such as rheumatoid arthritis, atopic dermatitis, and multiple sclerosis. The role of miR-155 as both a promoter of inflammation and an oncogenic agent provides a clear need for miR-155 itself to be stringently regulated. We therefore investigated the transcriptional regulation of miR-155 in response to the respective pro- and anti-inflammatory mediators LPS and IL-10. Bioinformatic analysis revealed Ets binding sites on the miR-155 promoter, and we found that Ets2 is critical for miR-155 induction by LPS. Truncation and mutational analysis of the miR-155 promoter confirmed the role of the Ets2 binding site proximal to the transcription start site for LPS responsiveness. We observed increased binding of Ets2 to the miR-155 promoter and Ets2 deficient mice displayed decreased induction of miR-155 in response to LPS. IL-10 inhibited the induction of Ets2 mRNA and protein by LPS, thereby decreasing Ets2 function on the pri-155 promoter. We have thus identified Ets2 as a key novel regulator in both the positive and negative control of miR-155 in the inflammatory response.

Keywords: Ets Family Transcription Factor; Ets2; Interleukin; Interleukin 10; Lipopolysaccharide (LPS); MicroRNA; SHIP1; TLR4; Toll-like Receptors (TLR); miR-155.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Humans
  • Inflammation / chemically induced
  • Inflammation / genetics
  • Inflammation / metabolism
  • Inflammation / pathology
  • Interleukin-10 / biosynthesis
  • Interleukin-10 / genetics
  • Lipopolysaccharides / toxicity*
  • Mice
  • MicroRNAs / biosynthesis*
  • MicroRNAs / genetics
  • Proto-Oncogene Protein c-ets-2 / genetics
  • Proto-Oncogene Protein c-ets-2 / metabolism*
  • Response Elements*

Substances

  • ETS2 protein, human
  • Ets2 protein, mouse
  • IL10 protein, human
  • IL10 protein, mouse
  • Lipopolysaccharides
  • MIRN155 microRNA, human
  • MicroRNAs
  • Mirn155 microRNA, mouse
  • Proto-Oncogene Protein c-ets-2
  • Interleukin-10