Neutrophil chemorepulsion in defined interleukin-8 gradients in vitro and in vivo

J Leukoc Biol. 2006 Mar;79(3):539-54. doi: 10.1189/jlb.0905516. Epub 2005 Dec 19.

Abstract

We report for the first time that primary human neutrophils can undergo persistent, directionally biased movement away from a chemokine in vitro and in vivo, termed chemorepulsion or fugetaxis. Robust neutrophil chemorepulsion in microfluidic gradients of interleukin-8 (IL-8; CXC chemokine ligand 8) was dependent on the absolute concentration of chemokine, CXC chemokine receptor 2 (CXCR2), and was associated with polarization of cytoskeletal elements and signaling molecules involved in chemotaxis and leading edge formation. Like chemoattraction, chemorepulsion was pertussis toxin-sensitive and dependent on phosphoinositide-3 kinase, RhoGTPases, and associated proteins. Perturbation of neutrophil intracytoplasmic cyclic adenosine monophosphate concentrations and the activity of protein kinase C isoforms modulated directional bias and persistence of motility and could convert a chemorepellent to a chemoattractant response. Neutrophil chemorepulsion to an IL-8 ortholog was also demonstrated and quantified in a rat model of inflammation. The finding that neutrophils undergo chemorepulsion in response to continuous chemokine gradients expands the paradigm by which neutrophil migration is understood and may reveal a novel approach to our understanding of the homeostatic regulation of inflammation.

Publication types

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

MeSH terms

  • Animals
  • Cell Polarity / drug effects
  • Cell Polarity / immunology
  • Cells, Cultured
  • Chemotaxis, Leukocyte / drug effects
  • Chemotaxis, Leukocyte / immunology*
  • Cyclic AMP / metabolism
  • Cytoskeleton / drug effects
  • Cytoskeleton / immunology
  • Cytoskeleton / metabolism
  • Dose-Response Relationship, Drug
  • Humans
  • Inflammation / immunology*
  • Inflammation / physiopathology
  • Interleukin-8 / immunology*
  • Interleukin-8 / pharmacology
  • Neutrophils / drug effects
  • Neutrophils / immunology*
  • Pertussis Toxin / pharmacology
  • Phosphatidylinositol 3-Kinases / drug effects
  • Phosphatidylinositol 3-Kinases / metabolism
  • Protein Kinase C / drug effects
  • Protein Kinase C / metabolism
  • Pseudopodia / drug effects
  • Pseudopodia / immunology
  • Pseudopodia / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Interleukin-8B / immunology*
  • Signal Transduction / drug effects
  • Signal Transduction / immunology
  • rho GTP-Binding Proteins / drug effects
  • rho GTP-Binding Proteins / metabolism

Substances

  • Interleukin-8
  • Receptors, Interleukin-8B
  • Cyclic AMP
  • Pertussis Toxin
  • Phosphatidylinositol 3-Kinases
  • Protein Kinase C
  • rho GTP-Binding Proteins