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Vol. 13, Issue 10, 3730-3746, October 2002
Department of Physiology, University College London, London WC1E
6JJ, United Kingdom
Phospholipase Ds (PLDs) are regulated enzymes that generate
phosphatidic acid (PA), a putative second messenger implicated in the
regulation of vesicular trafficking and cytoskeletal reorganization. Mast cells, when stimulated with antigen, show a dramatic alteration in
their cytoskeleton and also release their secretory granules by
exocytosis. Butan-1-ol, which diverts the production of PA generated by
PLD to the corresponding phosphatidylalcohol, was found to inhibit
membrane ruffling when added together with antigen or when added after
antigen. Inhibition by butan-1-ol was completely reversible because
removal of butan-1-ol restored membrane ruffling. Measurements of PLD
activation by antigen indicate a requirement for continual PA
production during membrane ruffling, which was maintained for at least
30 min. PLD1 and PLD2 are both expressed in mast cells and green
fluorescent protein-tagged proteins were used to identify PLD2
localizing to membrane ruffles of antigen-stimulated mast cells
together with endogenous ADP ribosylation factor 6 (ARF6). In contrast,
green fluorescent protein-PLD1 localized to intracellular vesicles and
remained in this location after stimulation with antigen. Membrane
ruffling was independent of exocytosis of secretory granules because
phorbol 12-myristate 13-acetate increased membrane ruffling in the
absence of exocytosis. Antigen or phorbol 12-myristate 13-acetate
stimulation increased both PLD1 and PLD2 activity when expressed
individually in RBL-2H3 cells. Although basal activity of
PLD2-overexpressing cells is very high, membrane ruffling was still
dependent on antigen stimulation. In permeabilized cells,
antigen-stimulated phosphatidylinositol(4,5)bisphosphate synthesis was dependent on both ARF6 and PA generated from PLD. We
conclude that both activation of ARF6 by antigen and a continual PLD2
activity are essential for local
phosphatidylinositol(4,5)bisphosphate generation that regulates
dynamic actin cytoskeletal rearrangements.
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