Leukocyte phosphoinositide-3 kinase {gamma} is required for chemokine-induced, sustained adhesion under flow in vivo

J Leukoc Biol. 2006 Dec;80(6):1491-9. doi: 10.1189/jlb.0306227. Epub 2006 Sep 22.

Abstract

During inflammation, leukocytes roll along the wall of postcapillary venules scanning the surface for immobilized CXCL1, a chemokine that triggers firm adhesion by activating CXCR2 on the neutrophil. PI-3K are signaling molecules important in cellular processes, ranging from cellular differentiation to leukocyte migration. PI-3Kgamma can be activated directly by the betagamma dimer of heterotrimeric G proteins coupled to CXCR2. Here, we used in vivo and ex vivo intravital microscopy models to test the role of PI-3Kgamma in leukocyte arrest. PI-3Kgamma null mice showed an 80% decrease in CXCL1-induced leukocyte adhesion in venules of the exteriorized mouse cremaster muscle. In wild-type mice, rolling leukocytes showed rapid and sustained adhesion, but in PI-3Kgamma(-/-) mice, adhesion was not triggered at all or was transient, suggesting that absence of PI-3Kgamma interferes with integrin bond strengthening. Wild-type mice reconstituted with PI-3Kgamma null bone marrow showed a 50% decrease in CXCL1-induced leukocyte adhesion. In a blood-perfused micro-flow chamber, leukocytes from PI-3Kgamma(-/-) mice showed a defect in adhesion on a P-selectin/ICAM-1/CXCL1 substrate, indicating that leukocyte PI-3Kgamma was required for adhesion. The adhesion defect in PI-3Kgamma(-/-) mice was as severe as that in mice lacking LFA-1, the major integrin responsible for neutrophil adhesion. We conclude that the gamma isoform of PI-3K must be functional in leukocytes to allow efficient adhesion from rolling in response to chemokine stimulation.

Publication types

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

MeSH terms

  • Animals
  • Cell Adhesion / drug effects
  • Cell Adhesion / physiology
  • Chemokine CXCL1
  • Chemokines, CXC / metabolism*
  • Chemokines, CXC / pharmacology
  • Class Ib Phosphatidylinositol 3-Kinase
  • Heterotrimeric GTP-Binding Proteins / metabolism
  • Intercellular Adhesion Molecule-1 / metabolism
  • Isoenzymes / deficiency
  • Isoenzymes / metabolism
  • Leukocyte Rolling / drug effects
  • Leukocyte Rolling / physiology*
  • Leukocytes / cytology
  • Leukocytes / enzymology*
  • Mice
  • Mice, Knockout
  • Muscle, Skeletal / blood supply
  • Muscle, Skeletal / cytology
  • Muscle, Skeletal / enzymology
  • P-Selectin / metabolism
  • Phosphatidylinositol 3-Kinases / deficiency
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Venules / cytology
  • Venules / enzymology

Substances

  • Chemokine CXCL1
  • Chemokines, CXC
  • Cxcl1 protein, mouse
  • Isoenzymes
  • P-Selectin
  • Intercellular Adhesion Molecule-1
  • Phosphatidylinositol 3-Kinases
  • Class Ib Phosphatidylinositol 3-Kinase
  • Pik3cg protein, mouse
  • Heterotrimeric GTP-Binding Proteins