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Papers In Press, published online ahead of print December 14, 2001
J. Biol. Chem, 10.1074/jbc.M110274200
Submitted on October 25, 2001
Revised on December 12, 2001
Accepted on December 14, 2001

Mechanism of ARF-stimulated phosphatidylinositol 4,5-bisphosphate synthesis in HL60 cells

Alison Skippen, David H. Jones, Clive P. Morgan, Michelle Li, and Shamshad Cockcroft

Department of Physiology, University College London, London WC1E 6JJ

Corresponding Author: S.Cockcroft{at}ucl.ac.uk

Phosphatidylinositol 4,5-bisphosphate (PI(4,5)P2) is required both as substrate for the generation of lipid-derived second messengers as well as an intact lipid for many aspects of cell signalling, endo- and exocytosis, and reorganisation of the cytoskeleton. ARF proteins regulate PI(4,5)P2 synthesis and here we have examined whether this is due to direct activation of Type 1 PIP 5-kinase or indirectly by PA-derived from phospholipase D (PLD) in HL60 cells. ARF1 and ARF6 are both expressed in HL60 cells and can be depleted from the cells by permeabilisation. Both ARFs increased the levels of PIP2 at the expense of PIP when added back to permeabilized cells. The PIP2 could be hydrolysed by phospholipase C, identifying it as PI(4,5)P2. However, the ARF1-stimulated pool of PI(4,5)P2 was accessible to the phospholipase C more efficiently in the presence of phosphatidylinositol transfer protein-a. To examine the role of PLD in the regulation of PI(4,5)P2 synthesis, we used butanol to diminish the PLD-derived PA. PI(4,5)P2 synthesis stimulated by ARF1 was not blocked by 0.5% butanol, but could be blocked by 1.5% butanol. Although 0.5% butanol was optimal for maximal transphosphatidylation, PA production was still detectable. In contrast, 1.5% butanol was found to inhibit completely the activation of PLD by ARF and also decrease PIP levels by 50%. Thus the toxicity of 1.5% butanol prevented us from concluding whether PA was an important factor in raising PI(4,5)P2 levels. To circumvent the use of alcohols, an ARF1 point mutant was identified (N52R-ARF1), that could selectively activate PIP 5-kinase activity but not PLD activity. N52R-ARF1 was still able to increase PI(4,5)P2 levels but at reduced efficiency. We therefore conclude that both PA derived from the PLD pathway and ARF proteins by directly activating PIP 5-kinase both contribute to the regulation of PI(4,5)P2 synthesis at the plasma membrane in HL60 cells.


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