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J. Biol. Chem., Vol. 278, Issue 32, 29799-29812, August 8, 2003

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Potentiation of Tumor Necrosis Factor -induced Secreted Phospholipase A₂ (sPLA₂)-IIA Expression in Mesangial Cells by an Autocrine Loop Involving sPLA₂ and Peroxisome Proliferator-activated Receptor Activation^*

Sabine Beck , Gérard Lambeau , Kristen Scholz-Pedretti , Michael H. Gelb ¶, Marcel J. W. Janssen ||, Suzanne H. Edwards **, David C. Wilton **, Josef Pfeilschifter  and Marietta Kaszkin  

From the Center of Pharmacology, University Hospital Frankfurt, 60590 Frankfurt, Germany, the Institut de Pharmacologie Moléculaire et Cellulaire, CNRS-UPR 411, 660 Route de Lucioles, Sophia Antipolis, 06560 Valbonne, France, the ^¶Department of Chemistry and Biochemistry, University of Washington, Seattle, Washington 98195, the ^||Department of Clinical Chemistry, Academic Medical Center, 1100 DD Amsterdam, The Netherlands, and the ^**Division of Biochemistry and Molecular Biology, School of Biological Sciences, University of Southampton, Southampton SO16 7PX, United Kingdom

In rat mesangial cells, exogenously added secreted phospholipases A₂ (sPLA₂s) potentiate the expression of pro-inflammatory sPLA₂-IIA first induced by cytokines like tumor necrosis factor- (TNF) and interleukin-1. The transcriptional pathway mediating this effect is, however, unknown. Because products of PLA₂ activity are endogenous activators of peroxisome proliferator-activated receptor (PPAR, we postulated that sPLA₂s mediate their effects on sPLA₂-IIA expression via sPLA₂ activity and subsequent PPAR activation. This study shows that various sPLA₂s, including venom enzymes, human sPLA₂-IIA, and wild-type and catalytically inactive H48Q mutant of porcine pancreatic sPLA₂-IB, enhance the TNF-induced sPLA₂-IIA expression at the mRNA and protein levels. In cells transfected with luciferase sPLA₂-IIA promoter constructs, sPLA₂s are active only when the promoter contains a functional PPRE-1 site. The effect of exogenous sPLA₂s is also blocked by the PPAR inhibitor MK886. Interestingly, the expression of sPLA₂-IIA induced by TNF alone is also attenuated by MK886, by the sPLA₂-IIA inhibitor LY311727, by heparinase, which prevents the binding of sPLA₂-IIA to heparan sulfate proteoglycans, and by the specific cPLA₂- inhibitor pyrrolidine-1. Together, these data indicate that sPLA₂-IIA released from mesangial cells by TNF stimulates its own expression via an autocrine loop involving cPLA₂ and PPAR. This signaling pathway is also used by exogenously added sPLA₂s including pancreatic sPLA₂-IB and is distinct from that used by TNF.

Received for publication, November 19, 2002 , and in revised form, May 23, 2003.

^* This work was supported by a grant from the Wilhelm Sander Stiftung (to M. K.). 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: Pharmazentrum Frankfurt, Klinikum der J. W. Goethe-Universität, Theodor-Stern-Kai 7, 60590 Frankfurt, Germany. Tel.: 49-69-6301-83105; Fax: 49-69-6301-83202; E-mail: kaszkin{at}em.uni-frankfurt.de.

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