Glycogen synthase kinase-3beta (GSK3beta) inhibition suppresses the inflammatory response to Francisella infection and protects against tularemia in mice

Mol Immunol. 2009 Feb;46(4):677-87. doi: 10.1016/j.molimm.2008.08.281. Epub 2008 Oct 17.

Abstract

Francisella tularensis, the causative agent of tularemia, is currently considered a category A bioterrorism agent due to its high virulence. Infection with F. tularensis results in an inflammatory response that plays an important role in the pathogenesis of the disease; however, the cellular mechanisms regulating this response are poorly understood. Glycogen synthase kinase-3beta (GSK3beta) is a serine/threonine protein kinase that has recently emerged as a key regulatory switch in the modulation of the inflammatory response. In this study, we investigated the effect of GSK3beta inhibition in regulating F. tularensis LVS-induced inflammatory responses. F. tularensis LVS infection of murine peritoneal macrophages induced a TLR2 dependent phosphorylation of GSK3beta. Inhibition of GSK3beta resulted in a significant decrease in the production of pro-inflammatory cytokine IL-6, IL-12p40 and TNF-alpha, as well as a significant increase in the production of the anti-inflammatory cytokine IL-10. GSK3beta regulated the F. tularensis LVS-induced cytokine response by differentially affecting the activation of transcription factors NF-kappaB and CREB. Inhibition of GSK3beta by lithium in vivo suppressed the inflammatory response in mice infected with F. tularensis LVS and conferred a survival advantage. In addition, we show that the production of IFN-gamma contributed to the development of tularemia and to the fatal outcome of the infected animals, depending on the timing and the relative level of the IFN-gamma produced. IFN-gamma potentiated F. tularensis LVS-induced cytokine production by increasing GSK3beta activity and the nuclear translocation of NF-kappaB. Taken together, these results demonstrate a regulatory function of GSK3beta in modulating inflammatory responses that can be detrimental to the host during an F. tularensis LVS infection, and suggest that inhibition of GSK3beta may represent a novel therapeutic approach in the treatment of tularemia.

Publication types

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

MeSH terms

  • Animals
  • Cells, Cultured
  • Cyclic AMP Response Element-Binding Protein / immunology
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Disease Models, Animal
  • Female
  • Francisella tularensis*
  • Glycogen Synthase Kinase 3 / antagonists & inhibitors*
  • Glycogen Synthase Kinase 3 / immunology*
  • Glycogen Synthase Kinase 3 / metabolism
  • Glycogen Synthase Kinase 3 beta
  • Interleukin-10 / immunology
  • Interleukin-10 / metabolism
  • Interleukin-12 Subunit p40 / immunology
  • Interleukin-12 Subunit p40 / metabolism
  • Interleukin-6 / immunology
  • Interleukin-6 / metabolism
  • Lithium Chloride / therapeutic use
  • Macrophages, Peritoneal / immunology*
  • Macrophages, Peritoneal / metabolism
  • Macrophages, Peritoneal / microbiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NF-kappa B / immunology
  • NF-kappa B / metabolism
  • Phosphorylation / drug effects
  • Phosphorylation / immunology
  • Toll-Like Receptor 2 / immunology
  • Toll-Like Receptor 2 / metabolism
  • Tularemia / drug therapy*
  • Tularemia / enzymology*
  • Tularemia / immunology
  • Tumor Necrosis Factor-alpha / immunology
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Creb1 protein, mouse
  • Cyclic AMP Response Element-Binding Protein
  • Interleukin-12 Subunit p40
  • Interleukin-6
  • NF-kappa B
  • Toll-Like Receptor 2
  • Tumor Necrosis Factor-alpha
  • Interleukin-10
  • Glycogen Synthase Kinase 3 beta
  • Gsk3b protein, mouse
  • Glycogen Synthase Kinase 3
  • Lithium Chloride