Glycogen synthase kinase-3 negatively regulates anti-inflammatory interleukin-10 for lipopolysaccharide-induced iNOS/NO biosynthesis and RANTES production in microglial cells

Immunology. 2009 Sep;128(1 Suppl):e275-86. doi: 10.1111/j.1365-2567.2008.02959.x. Epub 2008 Oct 29.

Abstract

The inflammatory effects of glycogen synthase kinase-3 (GSK-3) have been identified; however, the potential mechanism is still controversial. In this study, we investigated the effects of GSK-3-mediated interleukin-10 (IL-10) inhibition on lipopolysaccharide (LPS)-induced inflammation. Treatment with GSK-3 inhibitor significantly blocked LPS-induced nitric oxide (NO) production as well as inducible NO synthase (iNOS) expression in BV2 murine microglial cells and primary rat microglia-enriched cultures. Using an antibody array and enzyme-linked immunosorbent assay, we found that GSK-3-inhibitor treatment blocked LPS-induced upregulation of regulated on activation normal T-cell expressed and secreted (RANTES) and increased IL-10 expression. The time kinetics and dose-response relations were confirmed. Reverse transcription-polymerase chain reaction showed changes on the messenger RNA level as well. Inhibiting GSK-3 using short-interference RNA, and transfecting cells with dominant-negative GSK-3beta, blocked LPS-elicited NO and RANTES expression but increased IL-10 expression. In contrast, GSK-3beta overexpression upregulated NO and RANTES but downregulated IL-10 in LPS-stimulated cells. Treating cells with anti-IL-10 neutralizing antibodies to prevent GSK-3 from downregulating NO and RANTES showed that the anti-inflammatory effects are, at least in part, IL-10-dependent. The involvement of Akt, extracellular signal-regulated kinase, p38 mitogen-activated protein kinase and nuclear factor-kappaB that positively regulated IL-10 was demonstrated. Furthermore, inhibiting GSK-3 increased the nuclear translocation of transcription factors, that all important for IL-10 expression, including CCAAT/enhancer-binding protein beat (C/EBPbeta), C/EBPdelta, cAMP response binding element protein and NF-kappaB. Taken together, these findings reveal that LPS induces iNOS/NO biosynthesis and RANTES production through a mechanism involving GSK-3-mediated IL-10 downregulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Neutralizing / pharmacology
  • Cell Line
  • Chemokine CCL5 / immunology
  • Chemokine CCL5 / metabolism
  • Down-Regulation / genetics
  • Down-Regulation / immunology
  • Glycogen Synthase Kinase 3 / antagonists & inhibitors
  • Glycogen Synthase Kinase 3 / immunology*
  • Glycogen Synthase Kinase 3 / metabolism
  • Inflammation / chemically induced
  • Inflammation / immunology*
  • Inflammation / metabolism
  • Interleukin-10 / agonists
  • Interleukin-10 / antagonists & inhibitors
  • Interleukin-10 / immunology
  • Interleukin-10 / metabolism*
  • Lipopolysaccharides / pharmacology
  • Mice
  • Microglia / drug effects
  • Microglia / enzymology
  • Microglia / immunology*
  • NF-kappa B / immunology
  • NF-kappa B / metabolism
  • Nitric Oxide / antagonists & inhibitors
  • Nitric Oxide / immunology
  • Nitric Oxide / metabolism*
  • Nitric Oxide Synthase Type II / antagonists & inhibitors
  • Nitric Oxide Synthase Type II / immunology
  • Nitric Oxide Synthase Type II / metabolism*
  • Protein Kinase Inhibitors / pharmacology
  • Proto-Oncogene Proteins c-akt / immunology
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA, Small Interfering / immunology
  • RNA, Small Interfering / metabolism
  • Rats
  • Up-Regulation / genetics
  • Up-Regulation / immunology
  • p38 Mitogen-Activated Protein Kinases / immunology
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Antibodies, Neutralizing
  • Chemokine CCL5
  • Lipopolysaccharides
  • NF-kappa B
  • Protein Kinase Inhibitors
  • RNA, Small Interfering
  • Interleukin-10
  • Nitric Oxide
  • Nitric Oxide Synthase Type II
  • Proto-Oncogene Proteins c-akt
  • p38 Mitogen-Activated Protein Kinases
  • Glycogen Synthase Kinase 3