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Originally published In Press as doi:10.1074/jbc.M205417200 on July 1, 2002

J. Biol. Chem., Vol. 277, Issue 38, 34808-34814, September 20, 2002
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Transcription Factor Sp1 Phosphorylation Induced by Shear Stress Inhibits Membrane Type 1-Matrix Metalloproteinase Expression in Endothelium*

Sangseob YunDagger §, Alan DardikDagger , Masae HagaDagger , Akimasa YamashitaDagger , Seiichi YamaguchiDagger , Yongbok Koh§, Joseph A. Madri, and Bauer E. SumpioDagger ||

From the Departments of Dagger  Surgery and  Pathology, Yale University School of Medicine, New Haven, Connecticut 06510 and the § Department of Surgery, Catholic University School of Medicine, Seoul 121817, Korea

Membrane type 1-matrix metalloproteinase (MT1-MMP) plays a key role in endothelial cell migration, matrix remodeling, and angiogenesis. Previous studies demonstrated that a mechanical force, cyclic strain, increases MT1-MMP expression by displacing Sp1 with increased Egr-1 expression and binding to the promoter site. However, the effect of shear stress (SS) on MT1-MMP expression is poorly understood. Although Egr-1 mRNA transcription and protein was induced (7.6-fold) in response to SS (n = 5, 0-8 h, p < 0.05), SS decreased MT1-MMP mRNA transcription and protein levels in a time-dependent fashion (10, 50, and 90% reduction at 1, 4, and 8 h, respectively; n = 5, p < 0.05). Egr-1 protein was increased after SS and cyclic strain, but Sp1 was serine-phosphorylated only after SS. SS increased Sp1 DNA binding (3.8-, 5.8-, and 2.4-fold increase at 1, 4, and 8 h, respectively; n = 5, p < 0.05) that was inhibitable by calf intestinal phosphatase. Thus, SS inhibits MT1-MMP expression despite Egr-1 up-regulation by inducing the serine phosphorylation of Sp1, which in turn increases its binding affinity for its site on the MT1-MMP promoter, reducing the ability of Egr-1 to displace it. These data illustrate the complex control of microvascular endothelial cell MT1-MMP expression in response to distinct environmental stimuli (cyclic strain versus shear stress), consisting of both the modulation of specific transcription factor expression (Egr-1) as well as transcription factor post-translational modification (serine phosphorylation of Sp1).

* This work was supported by NHLBI Grant ROI HL-54732 from the National Institutes of Health, the Veterans Affairs Merit Review (to B. E. S.), and NHLBI Grant ROI HL-51018 from the National Institutes of Health (to J. A. M.).The costs of publication of this article were defrayed in part by the payment of page charges. The 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: Dept. of Surgery (Vascular), Yale University School of Medicine, 333 Cedar St., FMB 137, New Haven, CT 06510. Tel.: 203-785-2561; Fax: 203-785-7609; E-mail: bauer.sumpio@yale.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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