IL-10-Induced miR-155 Targets SOCS1 To Enhance IgE-Mediated Mast Cell Function

J Immunol. 2016 Jun 1;196(11):4457-67. doi: 10.4049/jimmunol.1502240. Epub 2016 Apr 29.

Abstract

IL-10 is an important regulatory cytokine that modulates a wide range of immune cells. Whereas it is best known for its ability to suppress immune responses, IL-10 has been found to be pathogenic in several human and animal studies of immune-mediated diseases. There is a considerable gap in our understanding of the molecular mechanisms behind the stimulatory effects of IL-10 during allergic inflammation. IL-10 treatment has been shown to suppress mast cell TNF production. In this study, we report that whereas TNF secretion was reduced, IL-10 surprisingly enhanced IgE-mediated protease and cytokine production both in vitro and in vivo. This stimulatory effect was consistent in mouse and human skin mast cells. IL-10 enhanced activation of the key FcεRI signaling proteins Stat5, JNK, and ERK. We demonstrate that IL-10 effects are dependent on Stat3 activation, eliciting miR-155 expression, with a resulting loss of suppressor of cytokine signaling-1. The importance of miR-155 was demonstrated by the inability of IL-10 to enhance anaphylaxis in miR-155-deficient mice. Taken together, our results reveal an IL-10-induced, Stat3-miR-155 signaling pathway that can promote mast cell responses.

Publication types

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

MeSH terms

  • Animals
  • Cells, Cultured
  • Immunoglobulin E / immunology*
  • Interleukin-10 / immunology*
  • Mast Cells / cytology
  • Mast Cells / immunology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • MicroRNAs / genetics*
  • MicroRNAs / immunology
  • Suppressor of Cytokine Signaling 1 Protein / genetics*

Substances

  • MicroRNAs
  • Mirn155 microRNA, mouse
  • Socs1 protein, mouse
  • Suppressor of Cytokine Signaling 1 Protein
  • Interleukin-10
  • Immunoglobulin E