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MBC in Press, published online ahead of print June 1, 2005
Mol. Biol. Cell 10.1091/mbc.E04-10-0907

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Submitted on October 19, 2004
Revised on May 11, 2005
Accepted on May 25, 2005

Functional Role of Syndecan-1 Cytoplasmic V Region in Lamellipodial Spreading, Actin-bundling, and Cell Migration

Ritu Chakravarti,* Vasileia Sapountzi,{dagger}{ddagger} and Josephine Adams*{dagger}

*Department of Cell Biology, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, OH 44195; {dagger}MRC Laboratory for Molecular Cell Biology and Department of Biochemistry and Molecular Biology, University College London, London WC1E 6BT, United Kingdom

Monitoring Editor: Mark Ginsberg

Cell protrusions contribute to cell motility and migration by mediating the outward extension and initial adhesion of cell edges. In many cells, these extensions are supported by actin-bundles assembled by the actin cross-linking protein, fascin. Multiple extracellular cues regulate fascin and here we focus on the mechanism by which the transmembrane proteoglycan, syndecan-1, specifically activates lamellipodial cell spreading and fascin-and-actin bundling when clustered either by thrombospondin-1, laminin, or antibody to the syndecan-1 extracellular domain. There is almost no knowledge of the signaling mechanisms of syndecan-1 cytoplasmic domain and we have tested the hypothesis that the unique V region of syndecan-1 cytoplasmic domain has a crucial role in these processes. By four criteria -the activities of N-cadherin/V region chimeras, syndecan-1 deletion mutants, or syndecan-1 point mutants, and specific inhibition by a membrane-permeable TAT-V peptide - we demonstrate that the V region is necessary and sufficient for these cell behaviors and map the molecular basis for its activity to multiple residues located across the V region. These activities correlate with a V-region dependent incorporation of cell-surface syndecan-1 into a detergent-insoluble form. We also demonstrate functional roles of syndecan-1 V region in laminin-dependent C2C12 cell adhesion and three-dimensional cell migration. These data identify for the first time specific cell behaviors that depend on signaling through the V region of syndecan-1.

{ddagger}Present address: Prostate Research Group, Northern Institute for Cancer Research, University of Newcastle Medical School, Newcastle Upon Tyne NE2 4HH, United Kingdom.

Address correspondence to: Josephine Adams (adamsj{at}ccf.org)




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