Involvement of SHIP in TLR2-induced neutrophil activation and acute lung injury

J Immunol. 2005 Jun 15;174(12):8064-71. doi: 10.4049/jimmunol.174.12.8064.

Abstract

The SHIP converts phosphatidylinositol 3,4,5 triphosphate to phosphatidyl 3,4 biphosphate. SHIP has negative regulatory functions on PI3K-dependent signaling pathways, which occupy important roles in modulating neutrophil functions. We used neutrophils from transgenic SHIP(-/-) and SHIP(+/+) mice that were stimulated with peptidoglycan (PGN) to examine the role of SHIP in TLR2-induced neutrophil activation. SHIP(-/-) neutrophils demonstrated significantly increased activation of the PI3K-dependent kinase Akt after exposure to PGN. Release of cytokines and chemokines, including TNF-alpha, IL-1beta, IL-6, IL-10, and MIP-2, was also increased in SHIP(-/-) compared with SHIP(+/+) neutrophils. There was no difference in the nuclear translocation of the transcriptional factor NF-kappaB between PGN-stimulated SHIP(-/-) and SHIP(+/+) neutrophils. However, phosphorylation of the p65 subunit of NF-kappaB, an event essential for optimal transcriptional activity of NF-kappaB, was increased in TLR2-activated SHIP(-/-) neutrophils. SHIP(-/-) neutrophils demonstrated greater activation of ERK1/2 and p38 MAPKs than did SHIP(+/+) neutrophils after exposure to PGN. The severity of acute lung injury induced by PGN was greater in SHIP(-/-) as compared with SHIP(+/+) mice. These results demonstrate that SHIP has a negative regulatory role in TLR2-induced neutrophil activation and in the development of related in vivo neutrophil-dependent inflammatory processes, such as acute lung injury.

Publication types

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

MeSH terms

  • Animals
  • Cells, Cultured
  • Down-Regulation / genetics
  • Down-Regulation / immunology
  • Enzyme Activation / immunology
  • Lung / enzymology*
  • Lung / immunology
  • Lung / pathology*
  • Mice
  • Mice, Transgenic
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • NF-kappa B / metabolism
  • Neutrophil Activation* / genetics
  • Neutrophil Activation* / immunology
  • Neutrophils / enzymology
  • Neutrophils / immunology
  • Neutrophils / pathology
  • Peptidoglycan / toxicity
  • Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases
  • Phosphoric Monoester Hydrolases / deficiency
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / physiology*
  • Phosphorylation
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt
  • Receptors, Immunologic / antagonists & inhibitors
  • Receptors, Immunologic / physiology*
  • Severity of Illness Index
  • Toll-Like Receptor 2
  • Transcription Factor RelA
  • Up-Regulation / genetics
  • Up-Regulation / immunology
  • p38 Mitogen-Activated Protein Kinases / metabolism
  • src Homology Domains / genetics
  • src Homology Domains / immunology

Substances

  • NF-kappa B
  • Peptidoglycan
  • Proto-Oncogene Proteins
  • Receptors, Immunologic
  • Tlr2 protein, mouse
  • Toll-Like Receptor 2
  • Transcription Factor RelA
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • p38 Mitogen-Activated Protein Kinases
  • Phosphoric Monoester Hydrolases
  • INPPL1 protein, human
  • Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases