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Papers In Press, published online ahead of print January 18, 2005
J. Biol. Chem, 10.1074/jbc.M411313200
Submitted on October 4, 2004
Revised on January 14, 2005
Accepted on January 18, 2005

Acidic extracellular pH induces matrix metalloproteinase-9 expression in mouse metastatic melanoma cells through the phospholipase D-MAPKs signaling

Yasumasa Kato, Charles A. Lambert, Alain C. Colige, Pierre Mineur, Agnes Noel, Francis Frankenne, Jean-Michel Foidart, Masaya Baba, Ryu-Ichiro Hata, Kaoru Miyazaki, and Mamoru Tsukuda

Department of Biochemistry and Molecular Biology, Kanagawa Dental College, Yokosuka, Knagawa 238-8580

Corresponding Author: yasumasa{at}kdcnet.ac.jp

The extracellular pH (pHe) of tumor tissues is often acidic, which can induce the expression of several proteins. We previously showed that production of matrix metalloproteinase-9 (MMP-9) was induced by culturing cells at acidic pHe (5.4-6.5). We have here investigated the signal transduction pathway by which acidic pHe induces MMP-9 expression. We found that acidic pHe (5.9) activated phospholipase D (PLD), and inhibition of PLD activity by 1-butanol and Myr-ARF6 suppressed the acidic pHe-induced MMP-9 expression. Exogenous PLD, but not phosphatidylinositol specific PLC or PLA2, mimicked MMP-9 induction by acidic pHe. Western blot analysis revealed that acidic pHe increased the steady-state levels of phosphorylated ERK1/2 and p38 and that the PLD inhibitors suppressed these increases. Using 5'-deletion mutant constructs of the MMP-9 promoter, we found that the acidic pHe-responsive region was located at nt 670 to -531, a region containing the NFkappa B binding site. A mutation into the NFkappa B binding site reduced, but not completely, the acidic pHe-induced MMP-9 promoter activity and NFkappa B activity was induced by acidic pHe. Pharmacological inhibitors specific for MEK1/2 (PD098059) and p38 (SB203580) attenuated the acidic pHe-induced NFkappa B activity and MMP-9 expression. These data suggest that PLD, MAPKs (ERK1/2 and p38), and NFkappa B mediate the acidic pHe signaling to induce MMP-9 expression. A transcription factor(s) other than NFkappa B may also be involved in the MMP-9 expression.


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