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Glycobiology Advance Access published online on March 2, 2006
Glycobiology, doi:10.1093/glycob/cwj098
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© The Author 2006. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Received September 30, 2005
Revised February 9, 2006
Accepted February 27, 2006

Article

The shedding of syndecan-4 and syndecan-1 from HeLa cells and human primary macrophages is accelerated by SDF-1/CXCL12 and mediated by the Matrix Metalloproteinase-9

Severine Brule 1, Nathalie Charnaux 2, Angela Sutton 3, Dominique Ledoux 4, Thomas Chaigneau 5, Line Saffar 3, and Liliane Gattegno 3 *

1 These authors contributed equally to the work; Laboratoire de Biologie Cellulaire, Biothérapies Bénéfices et Risques, UPRES 3410, Université Paris XIII, 74, rue Marcel Cachin, 93017, Bobigny, France
2 These authors contributed equally to the work; Laboratoire de Biochimie, Hôpital Jean Verdier, 93017, Bondy, France
3 Laboratoire de Biologie Cellulaire, Biothérapies Bénéfices et Risques, UPRES 3410, Université Paris XIII, 74, rue Marcel Cachin, 93017, Bobigny, France
4 ATHSCO, UPRES 3406, Université Paris XIII, 74, rue Marcel Cachin, 93017, Bobigny, France
5 Laboratoire de Biologie Cellulaire, Biothérapies Bénéfices et Risques, UPRES 3410, Université Paris XIII, 74, rue Marcel Cachin, 93017, Bobigny, France; Laboratoire de Biochimie, Hôpital Jean Verdier, 93017, Bondy, France

* To whom correspondence should be addressed.
Liliane Gattegno, E-mail: liliane.gattegno{at}jvr.ap-hop-paris.fr


  Abstract

We recently demonstrated that Stromal cell-Derived Factor-1 (SDF-1/CXCL12) forms complexes with CXCR4, but also with syndecan-4 expressed by human primary lymphocytes and macrophages, and HeLa cells. We also suggested that syndecan-4 behaves as a SDF-1 signaling molecule. Here, we demonstrate that SDF-1 strongly accelerates the shedding of syndecan-4 ectodomains, and in a lesser extent that of syndecan-1 from HeLa cells. The fact that this acceleration was not inhibited by the CXCR4 antagonist AMD 3100, anti-CXCR4 mAb 12G5, and by CXCR4 gene silencing, suggests its CXCR4-independence. Pretreating the cells with heparitinases I, III or with the protein kinase C inhibitor, bisindolylmaleimide, significantly inhibited this accelerated shedding, which suggests the involvement of both, cell surface heparan sulfate and protein kinase C transduction pathway. In contrast, Map Kinase or NF-{kappa}B pathway inhibitors had no effect. Moreover, SDF-1 increases the matrix metalloproteinase-9 (MMP-9) mRNA level as well as MMP-9 activity in HeLa cells and MMP-9 silencing by RNA interference strongly decreases the syndecan-1 and -4 ectodomain shedding accelerated by SDF-1. Finally, SDF-1 also accelerates in a CXCR4 independent manner, the shedding of syndecan-1 and -4 from human primary macrophages, which is significantly inhibited by anti-MMP-9 antibodies. This strongly indicates the role of MMP-9 in these events occurring in both, a tumoral cell line as well as in human primary macrophages. Because MMP-9 plays a crucial role in extracellular matrix degradation during cancer cell metastasis and invasion, and shed ectodomains of syndecans may likely be involved in tumor cell proliferation, these data further indicate the multiplicity of the roles played by SDF-1 on tumor cell biology.

Keywords: Chemokine/Proteoglycan/Shedding/Glycosaminoglycan/CXCR4.
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