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J. Biol. Chem., Vol. 276, Issue 19, 15704-15711, May 11, 2001

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Phospholipase D Activation by Norepinephrine Is Mediated by 12(S)-, 15(S)-, and 20-Hydroxyeicosatetraenoic Acids Generated by Stimulation of Cytosolic Phospholipase A₂
TYROSINE PHOSPHORYLATION OF PHOSPHOLIPASE D₂ IN RESPONSE TO NOREPINEPHRINE^*

Jean-Hugues Parmentier, Mubarack M. Muthalif, Abdelwahab E. Saeed^§, and Kafait U. Malik^¶

From the Department of Pharmacology, College of Medicine, University of Tennessee Health Science Center, Memphis, Tennessee 38163

Norepinephrine (NE) stimulates phospholipase D (PLD) through a Ras/MAPK pathway in rabbit vascular smooth muscle cells (VSMC). NE also activates calcium influx and calmodulin (CaM)-dependent protein kinase II-dependent cytosolic phospholipase A₂ (cPLA₂). Arachidonic acid (AA) released by cPLA₂-catalyzed phospholipid hydrolysis is then metabolized into hydroxyeicosatetraenoic acids (HETEs) through lipoxygenase and cytochrome P450 4A (CYP4A) pathways. HETEs, in turn, have been shown to stimulate Ras translocation and to increase MAPK activity in VSMC. This study was conducted to determine the contribution of cPLA₂-derived AA and its metabolites (HETEs) to the activation of PLD. NE-induced PLD activation was reduced by two structurally distinct CaM antagonists, W-7 and calmidazolium, and by CaM-dependent protein kinase II inhibition. Blockade of cPLA₂ activity or protein depletion with selective cPLA₂ antisense oligonucleotides abolished NE-induced PLD activation. The increase in PLD activity elicited by NE was also blocked by inhibitors of lipoxygenases (baicalein) and CYP4A (17-octadecynoic acid), but not of cyclooxygenase (indomethacin). AA and its metabolites (12(S)-, 15(S)-, and 20-HETEs) increased PLD activity. PLD activation by AA and HETEs was reduced by inhibitors of Ras farnesyltransferase (farnesyl protein transferase III and BMS-191563) and MEK (U0126 and PD98059). These data suggest that HETEs are the mediators of cPLA₂-dependent PLD activation by NE in VSMC. In addition to cPLA₂, PLD was also found to contribute to AA release for prostacyclin production via the phosphatidate phosphohydrolase/diacylglycerol lipase pathway. Finally, a catalytically inactive PLD₂ (but not PLD₁) mutant inhibited NE-induced PLD activity, and PLD₂ was tyrosine-phosphorylated in response to NE by a MAPK-dependent pathway. We conclude that NE stimulates cPLA₂-dependent PLD₂ through lipoxygenase- and CYP4A-derived HETEs via the Ras/ERK pathway by a mechanism involving tyrosine phosphorylation of PLD₂ in rabbit VSMC.

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