Neutrophil functional responses depend on immune complex valency

J Leukoc Biol. 1995 Oct;58(4):403-14. doi: 10.1002/jlb.58.4.403.

Abstract

Ligand-induced cross-linking of Fc gamma receptors (Fc gamma R) on neutrophils plays a significant role in their stimulation, shown here by contrasting the responses induced by low valency immune complexes (LICs) and high valency immune complexes (HICs) and by cross-linking LICs in situ (L/Ab) after their addition to the cells. Multiparameter flow cytometry was used to measure immune complex (IC)-elicited changes in cytoplasmic Ca2+ concentration and initiation of the oxidative burst simultaneously in the same cell and to correlate these with Fc gamma R occupancy. We have previously shown that subpopulations of neutrophils respond maximally to subsaturating concentrations of HIC; saturating dosages stimulate the entire population. This discrepancy was not due to differences in receptor occupancy. The magnitude of the transient Ca2+ increase was independent of the dose of HIC but depended on the dose when an LIC was used. As shown here, L/Ab cross-linking elicited Ca2+ responses similar to those observed in HIC-stimulated cells. In contrast, LIC elicited only minimal intracellular delta pH and no oxidative burst or membrane potential changes at all unless Fc gamma R was cross-linked, accomplished by HIC or by L/Ab. However, azurophilic degranulation, as determined by elastase release, was not observed in cells stimulated by the in situ cross-linking method, whereas the HIC preparation triggered azurophilic degranulation. Thus, some Fc gamma R-mediated neutrophil effector functions such as azurophilic degranulation and oxidative burst initiation have an absolute requirement for Fc gamma R cross-linking, whereas signaling functions such as changes in membrane potential, intracellular pH, and intracellular Ca2+ concentration can occur, albeit more slowly and to a lesser extent, if single Fc gamma R are occupied.

Publication types

  • Comparative Study
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amiloride / analogs & derivatives
  • Amiloride / pharmacology
  • Antibodies / pharmacology
  • Antigen-Antibody Complex / chemistry*
  • Antigen-Antibody Complex / physiology*
  • Calcium / metabolism
  • Cells, Cultured
  • Cytochrome c Group / metabolism
  • Cytoplasmic Granules / metabolism
  • Cytosol / metabolism
  • Flow Cytometry
  • Fluorescence
  • Humans
  • Hydrogen-Ion Concentration
  • Leukocyte Elastase
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Molecular Sequence Data
  • N-Formylmethionine Leucyl-Phenylalanine / pharmacology
  • Neutrophil Activation / physiology
  • Neutrophils / metabolism
  • Neutrophils / physiology*
  • Oxidation-Reduction
  • Pancreatic Elastase / analysis
  • Pancreatic Elastase / metabolism
  • Receptors, IgG / metabolism
  • Receptors, IgG / physiology
  • Respiratory Burst / drug effects
  • Respiratory Burst / physiology
  • Signal Transduction
  • Stimulation, Chemical
  • Superoxide Dismutase / metabolism

Substances

  • Antibodies
  • Antigen-Antibody Complex
  • Cytochrome c Group
  • Receptors, IgG
  • 5-dimethylamiloride
  • N-Formylmethionine Leucyl-Phenylalanine
  • Amiloride
  • Superoxide Dismutase
  • Pancreatic Elastase
  • Leukocyte Elastase
  • Calcium