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Mitogen-activated protein kinase phosphatase 2 regulates the inflammatory response in sepsis

Infect Immun. 2010 Jun;78(6):2868-76. doi: 10.1128/IAI.00018-10. Epub 2010 Mar 29.

Abstract

Sepsis results from a dysregulation of the regulatory mechanisms of the pro- and anti-inflammatory response to invading pathogens. The mitogen-activated protein (MAP) kinase cascades are key signal transduction pathways involved in the cellular production of cytokines. The dual-specific phosphatase 1 (DUSP 1), mitogen-activated protein kinase phosphatase-1 (MKP-1), has been shown to be an important negative regulator of the inflammatory response by regulating the p38 and Jun N-terminal protein kinase (JNK) MAP kinase pathways to influence pro- and anti-inflammatory cytokine production. MKP-2, also a dual-specific phosphatase (DUSP 4), is a phosphatase highly homologous with MKP-1 and is known to regulate MAP kinase signaling; however, its role in regulating the inflammatory response is not known. We hypothesized a regulatory role for MKP-2 in the setting of sepsis. Mice lacking the MKP-2 gene had a survival advantage over wild-type mice when challenged with intraperitoneal lipopolysaccharide (LPS) or a polymicrobial infection via cecal ligation and puncture. The MKP-2(-/-) mice also exhibited decreased serum levels of both pro-inflammatory cytokines (tumor necrosis factor alpha [TNF-alpha], interleukin-1beta [IL-1beta], IL-6) and anti-inflammatory cytokines (IL-10) following endotoxin challenge. Isolated bone marrow-derived macrophages (BMDMs) from MKP-2(-/-) mice showed increased phosphorylation of the extracellular signal-regulated kinase (ERK), decreased phosphorylation of JNK and p38, and increased induction of MKP-1 following LPS stimulation. The capacity for cytokine production increased in MKP-2(-/-) BMDMs following MKP-1 knockdown. These data support a mechanism by which MKP-2 targets ERK deactivation, thereby decreasing MKP-1 and thus removing the negative inhibition of MKP-1 on cytokine production.

Publication types

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

MeSH terms

  • Animals
  • Bacterial Infections / immunology
  • Cytokines / blood
  • Dual Specificity Phosphatase 1 / analysis
  • Female
  • Inflammation / immunology*
  • Lipopolysaccharides / immunology
  • Lipopolysaccharides / toxicity
  • MAP Kinase Kinase 4 / analysis
  • Macrophages / chemistry
  • Macrophages / immunology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Peritonitis / immunology
  • Protein Tyrosine Phosphatases / deficiency
  • Protein Tyrosine Phosphatases / immunology*
  • Sepsis / immunology*
  • Survival Analysis
  • p38 Mitogen-Activated Protein Kinases / analysis

Substances

  • Cytokines
  • Lipopolysaccharides
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase 4
  • Dual Specificity Phosphatase 1
  • Dusp1 protein, mouse
  • MKP2 protein, mouse
  • Protein Tyrosine Phosphatases