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J. Biol. Chem., Vol. 278, Issue 26, 24153-24163, June 27, 2003

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Cross-talk between Cytosolic Phospholipase A₂ (cPLA₂) and Secretory Phospholipase A₂ (sPLA₂) in Hydrogen Peroxide-induced Arachidonic Acid Release in Murine Mesangial Cells

sPLA₂ REGULATES cPLA₂ ACTIVITY THAT IS RESPONSIBLE FOR ARACHIDONIC ACID RELEASE^*

Won K. Han , Adam Sapirstein , Cheng C. Hung , Alessandro Alessandrini  and Joseph V. Bonventre  ¶ ||

From the Medical and Anesthesia Services, Massachusetts General Hospital, Department of Medicine and Anesthesia, Harvard Medical School, and ^¶Harvard-MIT, Division of Health Science and Technology, Charlestown, Massachusetts 02129-2060

Oxidant stress and phospholipase A₂ (PLA₂) activation have been implicated in numerous proinflammatory responses of the mesangial cell (MC). We investigated the cross-talk between group IV cytosolic PLA₂ (cPLA₂) and secretory PLA₂s (sPLA₂s) during H₂O₂-induced arachidonic acid (AA) release using two types of murine MC: (i) MC^+/+, which lack group IIa and V PLA₂s, and (ii) MC^–/–, which lack groups IIa, V, and IV PLA₂s. H₂O₂-induced AA release was greater in MC^+/+ compared with MC^–/–. It has been argued that cPLA₂ plays a regulatory role enhancing the activity of sPLA₂s, which act on phospholipids to release fatty acid. Group IIa, V, or IV PLA₂s were expressed in MC^–/– or MC^+/+ using recombinant adenovirus vectors. Expression of cPLA₂ in H₂O₂-treated MC^–/– increased AA release to a level approaching that of H₂O₂-treated MC^+/+. Expression of either group IIa PLA₂ or V PLA₂ enhanced AA release in MC^+/+ but had no effect on AA release in MC^–/–. When sPLA₂ and cPLA₂ are both present, the effect of H₂O₂ is manifested by preferential release of AA compared with oleic acid. Inhibition of the ERK and protein kinase C signaling pathways with the MEK-1 inhibitor, U0126, and protein kinase C inhibitor, GF 1092030x, respectively, and chelating intracellular free calcium with 1,2-bis(2-aminophenoyl)ethane-N,N,N',N'-tetraacetic acid-AM, which also reduced ERK1/2 activation, significantly reduced H₂O₂-induced AA release in MC^+/+ expressing either group IIa or V PLA₂s. By contrast, H₂O₂-induced AA release was not enhanced when ERK1/2 was activated by infection of MC^+/+ with constitutively active MEK1-DD. We conclude that the effect of group IIa and V PLA₂s on H₂O₂-induced AA release is dependent upon the presence of cPLA₂ and the activation of PKC and ERK1/2. Group IIa and V PLA₂s are regulatory and cPLA₂ is responsible for AA release.

Received for publication, January 14, 2003 , and in revised form, March 25, 2003.

^* This work was supported in part by National Institutes of Health Awards DK38452, NS10828, and DK39773 (to J. V. B.), a National Kidney Foundation Fellowship Award and Individual National Research Service Award DK10036 (to W. K. H.), a PKR foundation grant (to A. A.), and the Chang Gung Memorial Hospital (to C. C. H.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| To whom correspondence should be addressed: MRB4, Brigham and Women's Hospital, 75 Francis St., Boston, MA 02115. Tel.: 617-732-6020; Fax: 617-582-6010; E-mail: joseph_bonventre{at}hms.harvard.edu.

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