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A more recent version of this article appeared on October 1, 2002
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Submitted on April 18, 2002
Revised on June 27, 2002
Accepted on July 10, 2002
1 Department of Physiology, Rockefeller Building, University College London, University St., London WC1E 6JJ, UK
* Corresponding author. E-mail address: s.cockcroft{at}ucl.ac.uk.
Phospholipase Ds (PLD) are regulated enzymes, which generate phosphatidic acid (PA), a putative second messenger implicated in the regulation of vesicular trafficking and cytoskeletal reorganisation. 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 as 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 30min. PLD1 and PLD2 are both expressed in mast cells and GFP-tagged proteins were used to identify PLD2 localising to membrane ruffles of antigen-stimulated mast cells together with endogenous ARF6. In contrast, GFP-PLD1 localised to intracellular vesicles and remained in this location after stimulation with antigen. Membrane ruffling was independent of exocytosis of secretory granules as PMA increased membrane ruffling in the absence of exocytosis. Antigen or PMA stimulation increased both PLD1 and PLD2 activity when expressed individually in RBL-2H3 cells. Although basal activity of PLD2-over-expressing cells is very high, membrane ruffling was still dependent on antigen stimulation. In permeabilised cells antigen-stimulated phosphatidylinositol(4,5)bisphosphate (PI(4,5)P2) 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 is essential for local PI(4,5)P2 generation that regulates dynamic actin cytoskeletal rearrangements.
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