MicroRNA-101 targets MAPK phosphatase-1 to regulate the activation of MAPKs in macrophages

J Immunol. 2010 Dec 15;185(12):7435-42. doi: 10.4049/jimmunol.1000798. Epub 2010 Nov 10.

Abstract

MAPK phosphatase-1 (MKP-1) is an archetypical member of the dual-specificity phosphatase family that deactivates MAPKs. Induction of MKP-1 has been implicated in attenuating the LPS- or peptidoglycan-induced biosynthesis of proinflammatory cytokines, but the role of noncoding RNA in the expression of the MKP-1 is still poorly understood. In this study, we show that MKP-1 is a direct target of microRNA-101 (miR-101). Transfection of miR-101 attenuates induction of MKP-1 by LPS as well as prolonged activation of p38 and JNK/stress-activated protein kinase, whereas inhibition of miR-101 enhances the expression of MKP-1 and shortens p38 and JNK activation. We also found that expression of miR-101 is induced by multiple TLR ligands, including LPS, peptidoglycan, or polyinosinic-polycytidylic acid, and that inhibition of PI3K/Akt by LY294002 or Akt RNA interference blocks the induction of miR-101 by LPS in RAW264.7 macrophage cells. Moreover, treatment of cells with dexamethasone, a widely used anti-inflammatory agent, markedly inhibits miR-101 expression and enhances the expression of MKP-1 in LPS-stimulated macrophages. Together, these results indicate that miR-101 regulates the innate immune responses of macrophages to LPS through targeting MKP-1.

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Cell Line
  • Dexamethasone / pharmacology
  • Dual Specificity Phosphatase 1 / biosynthesis
  • Dual Specificity Phosphatase 1 / immunology*
  • Enzyme Activation / drug effects
  • Enzyme Activation / immunology
  • Gene Expression Regulation, Enzymologic / drug effects
  • Immunity, Innate / drug effects
  • Immunity, Innate / physiology*
  • Lipopolysaccharides / pharmacology
  • MAP Kinase Kinase 4 / immunology
  • MAP Kinase Kinase 4 / metabolism
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Mice
  • MicroRNAs / biosynthesis
  • MicroRNAs / immunology*
  • Toll-Like Receptors / agonists
  • Toll-Like Receptors / immunology
  • Toll-Like Receptors / metabolism
  • p38 Mitogen-Activated Protein Kinases / immunology
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Anti-Inflammatory Agents
  • Lipopolysaccharides
  • MicroRNAs
  • Toll-Like Receptors
  • Dexamethasone
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase 4
  • Dual Specificity Phosphatase 1
  • Dusp1 protein, mouse