MicroRNA regulation of STAT4 protein expression: rapid and sensitive modulation of IL-12 signaling in human natural killer cells

Blood. 2011 Dec 22;118(26):6793-802. doi: 10.1182/blood-2011-05-356162. Epub 2011 Nov 10.

Abstract

IL-12 exerts several regulatory effects on natural killer (NK) cells by activating IL-12 signaling. IL-12 signaling is tightly auto-regulated to control its onset and termination, with prolonged IL-12 treatment resulting in IL-12 hyporesponsiveness. However, the mechanisms underlying IL-12 auto-regulation are still unclear. In this study we report that prolonged IL-12 treatment significantly up-regulates microRNAs (miRNAs), including miR-132, -212, and -200a in primary human NK cells. This up-regulation correlates temporally with gradually decreasing STAT4 levels and decreasing IFN-γ expression, after an initial increase within the first 16 hours of IL-12 treatment. The IL-12 hyporesponsiveness is dependent on IL-12 concentration, and associated up-regulation of miR-132, -212, and -200a. Furthermore, IL-12-hyporesponsive cells regain responsiveness of IFN-γ production 24 hours after IL-12 removal, which correlates with decreases in miR-132, -212, and -200a levels. Overexpression of miR-132, -212, and -200a by transfection into NK cells mimics IL-12 priming, inducing IL-12 hyporesponsiveness, whereas transfection of miR-132, -212, and -200a inhibitors largely abolishes IL-12 induction of IL-12 hyporesponsiveness. These data suggest that miR-132, -212, and -200a up-regulation during prolonged IL-12 treatment, negatively regulates the IL-12 signaling pathway by reducing STAT4 expression in primary human NK cells.

MeSH terms

  • 3' Untranslated Regions / genetics
  • Binding Sites / genetics
  • Blotting, Western
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Flow Cytometry
  • Gene Expression Regulation / drug effects
  • Humans
  • Interferon-gamma / genetics
  • Interferon-gamma / metabolism
  • Interleukin-12 / pharmacology
  • Killer Cells, Natural / drug effects
  • Killer Cells, Natural / metabolism
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Protein Biosynthesis / genetics*
  • Receptors, Interleukin-12 / genetics
  • Receptors, Interleukin-12 / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • STAT4 Transcription Factor / genetics*
  • STAT4 Transcription Factor / metabolism
  • Up-Regulation / drug effects

Substances

  • 3' Untranslated Regions
  • MIRN132 microRNA, human
  • MIRN200 microRNA, human
  • MIRN212 microRNA, human
  • MicroRNAs
  • Receptors, Interleukin-12
  • STAT4 Transcription Factor
  • STAT4 protein, human
  • Interleukin-12
  • Interferon-gamma