Genetic analysis of the role of the PI3K-Akt pathway in lipopolysaccharide-induced cytokine and tissue factor gene expression in monocytes/macrophages

J Immunol. 2008 Mar 15;180(6):4218-26. doi: 10.4049/jimmunol.180.6.4218.

Abstract

LPS stimulation of monocytes/macrophages induces the expression of genes encoding proinflammatory cytokines and the procoagulant protein, tissue factor. Induction of these genes is mediated by various signaling pathways, including mitogen-activated protein kinases, and several transcription factors, including Egr-1, AP-1, ATF-2, and NF-kappaB. We used a genetic approach to determine the role of the phosphatidylinositol-3-kinase (PI3K)-protein kinase B (Akt) pathway in the regulation of LPS signaling and gene expression in isolated macrophages and in mice. The PI3K-Akt pathway is negatively regulated by the phosphatase and tensin homologue (PTEN). We used peritoneal exudate cells from Pik3r1-deficient mice, which lack the p85alpha regulatory subunit of PI3K and have reduced PI3K activity, and peritoneal macrophages from PTEN(flox/flox)/LysMCre mice (PTEN(-/-)), which have increased Akt activity. Analysis of LPS signaling in Pik3r1(-/-) and PTEN(-/-) cells indicated that the PI3K-Akt pathway inhibited activation of the ERK1/2, JNK1/2, and p38 mitogen-activated protein kinases and reduced the levels of nuclear Egr-1 protein and phosphorylated ATF-2. Modulating the PI3K-Akt pathway did not affect LPS-induced degradation of IkappaBalpha or NF-kappaB nuclear translocation. LPS induction of TNF-alpha, IL-6, and tissue factor gene expression was increased in Pik3r1(-/-) peritoneal exudate cells and decreased in PTEN(-/-) peritoneal macrophages compared with wild-type (WT) cells. Furthermore, LPS-induced inflammation and coagulation were enhanced in WT mice containing Pik3r1(-/-) bone marrow compared with WT mice containing WT bone marrow and in mice lacking the p85alpha subunit in all cells. Taken together, our results indicate that the PI3K-Akt pathway negatively regulates LPS signaling and gene expression in monocytes/macrophages.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ascitic Fluid / cytology
  • Ascitic Fluid / enzymology
  • Ascitic Fluid / metabolism
  • Cells, Cultured
  • Cytokines / antagonists & inhibitors
  • Cytokines / biosynthesis
  • Cytokines / genetics*
  • Down-Regulation / immunology
  • Female
  • Gene Expression Regulation, Enzymologic / immunology*
  • Lipopolysaccharides / pharmacology*
  • MAP Kinase Signaling System / immunology
  • Macrophages, Peritoneal / enzymology
  • Macrophages, Peritoneal / immunology
  • Macrophages, Peritoneal / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Monocytes / enzymology
  • Monocytes / immunology
  • Monocytes / metabolism*
  • PTEN Phosphohydrolase / biosynthesis
  • PTEN Phosphohydrolase / deficiency
  • PTEN Phosphohydrolase / genetics
  • Phosphatidylinositol 3-Kinases / biosynthesis
  • Phosphatidylinositol 3-Kinases / genetics
  • Phosphatidylinositol 3-Kinases / physiology*
  • Proto-Oncogene Proteins c-akt / biosynthesis
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-akt / physiology*
  • Thromboplastin / antagonists & inhibitors
  • Thromboplastin / biosynthesis
  • Thromboplastin / genetics*
  • Up-Regulation / immunology

Substances

  • Cytokines
  • Lipopolysaccharides
  • Thromboplastin
  • Phosphatidylinositol 3-Kinases
  • Proto-Oncogene Proteins c-akt
  • PTEN Phosphohydrolase