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The Journal of Immunology, 2000, 165: 5788-5797.
Copyright © 2000 by The American Association of Immunologists

Amplification of IL-1{beta}-Induced Matrix Metalloproteinase-9 Expression by Superoxide in Rat Glomerular Mesangial Cells Is Mediated by Increased Activities of NF-{kappa}B and Activating Protein-1 and Involves Activation of the Mitogen-Activated Protein Kinase Pathways1

Wolfgang Eberhardt, Andrea Huwiler, Karl-Friedrich Beck, Sebastian Walpen and Josef Pfeilschifter2

Pharmazentrum Frankfurt, Klinikum der Johann Wolfgang Goethe Universität, Frankfurt am Main, Germany

The modulation of cell signaling by free radicals is important for the pathogenesis of inflammatory diseases. Recently, we have shown that NO reduces IL-1{beta}-induced matrix metalloproteinase (MMP-9) expression in glomerular mesangial cells (MC). Here we report that exogenously administrated superoxide, generated by the hypoxanthine/xanthine oxidase system (HXXO) or by the redox cycler 2,3-dimethoxy-1,4-naphtoquinone, caused a marked amplification of IL-1{beta}-primed, steady state, MMP-9 mRNA level and an increase in gelatinolytic activity in the conditioned medium. Superoxide generators alone were ineffective. Cytokine-induced steady state mRNA levels of TIMP-1, an endogenous inhibitor of MMP-9, were affected similarly by HXXO. Transient transfection of rat mesangial cells with 0.6 kb of the 5'-flanking region of the rat MMP-9 gene proved a transcriptional regulation of MMP-9 expression by superoxide. HXXO augmented the IL-1{beta}-triggered nuclear translocation of p65 and c-Jun and, in parallel, increased DNA binding activities of NF-{kappa}B and AP-1. Mutation of either response element completely prevented MMP-9 promoter activation by IL-1{beta}. Moreover, specific inhibitors of the classical extracellular signal-regulated kinase (ERK) pathway and p38 mitogen-activated protein kinase (MAPK) cascade, partially reversed the HXXO-mediated effects on MMP-9 mRNA levels, thus demonstrating involvement of ERKs and p38 MAPKs in MMP-9 expression. Furthermore, IL-1{beta}-triggered phosphorylation of all three MAPKs, including p38-MAPK, c-Jun N-terminal kinase, and ERK, was substantially enhanced by superoxide. Our data identify superoxide as a costimulatory factor amplifying cytokine-induced MMP-9 expression by interfering with the signaling cascades leading to the activation of AP-1 and NF-{kappa}B.




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