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Originally published In Press as doi:10.1074/jbc.M201283200 on June 26, 2002

J. Biol. Chem., Vol. 277, Issue 36, 32970-32977, September 6, 2002
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Syndecan-4 Modulates Focal Adhesion Kinase Phosphorylation*

Sarah A. Wilcox-AdelmanDagger , Fabienne Denhez, and Paul F. Goetinck§

From the Cutaneous Biology Research Center, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts 02129

The cell-surface heparan sulfate proteoglycan syndecan-4 acts in conjunction with the alpha 5beta 1 integrin to promote the formation of actin stress fibers and focal adhesions in fibronectin (FN)-adherent cells. Fibroblasts seeded onto the cell-binding domain (CBD) fragment of FN attach but do not fully spread or form focal adhesions. Activation of Rho, with lysophosphatidic acid (LPA), or protein kinase C, using the phorbol ester phorbol 12-myristate 13-acetate, or clustering of syndecan-4 with antibodies directed against its extracellular domain will stimulate formation of focal adhesions and stress fibers in CBD-adherent fibroblasts. The distinct morphological differences between the cells adherent to the CBD and to full-length FN suggest that syndecan-4 may influence the organization of the focal adhesion or the activation state of the proteins that comprise it. FN-null fibroblasts (which express syndecan-4) exhibit reduced phosphorylation of focal adhesion kinase (FAK) tyrosine 397 (Tyr397) when adherent to CBD compared with FN-adherent cells. Treating the CBD-adherent fibroblasts with LPA, to activate Rho, or the tyrosine phosphatase inhibitor sodium vanadate increased the level of phosphorylation of Tyr397 to match that of cells plated on FN. Treatment of the fibroblasts with PMA did not elicit such an effect. To confirm that this regulatory pathway includes syndecan-4 specifically, we examined fibroblasts derived from syndecan-4-null mice. The phosphorylation levels of FAK Tyr397 were lower in FN-adherent syndecan-4-null fibroblasts compared with syndecan-4-wild type and these levels were rescued by the addition of LPA or re-expression of syndecan-4. These data indicate that syndecan-4 ligation regulates the phosphorylation of FAK Tyr397 and that this mechanism is dependent on Rho but not protein kinase C activation. In addition, the data suggest that this pathway includes the negative regulation of a protein-tyrosine phosphatase. Our results implicate syndecan-4 activation in a direct role in focal adhesion regulation.

* This work was supported in part by National Institute of Health, NICHD Grant HD-37490 and grants from the Cutaneous Biology Research Center through the MGH/Shiseido Company (to P. F. G.) and the Dermatology Foundation Research (to F. D.)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.

This paper is dedicated to the memory of Merton Bernfield who pioneered the field of syndecan biology.

Dagger Supported by National Institutes of Health Postdoctoral Fellowship F32 HD41235.

§ To whom correspondence should be addressed: Cutaneous Biology Research Center, MGH-East, Bldg. 149, 13th St., Charlestown, MA 02129. Tel.: 617-726-4183; Fax: 617-726-4189; E-mail: paul.goetinck@cbrc2.mgh.harvard.edu.

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