Glycobiology Advance Access originally published online on March 2, 2006
Glycobiology 2006 16(6):488-501; doi:10.1093/glycob/cwj098
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
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
2 Laboratoire de Biologie Cellulaire, Biothérapies Bénéfices et Risques, UPRES 3410, Université Paris XIII, 74 Rue Marcel Cachin, 93017 Bobigny, France; 3 Laboratoire de Biochimie, Hôpital Jean Verdier, 93017 Bondy, France; and 4 ATHSCO, UPRES 3406, Université Paris XIII, 74 Rue Marcel Cachin, 93017 Bobigny, France
1 To whom correspondence should be addressed; e-mail: liliane.gattegno{at}jvr.ap-hop-paris.fr
Received on September 30, 2005; revised on February 9, 2006; accepted on February 27, 2006
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 to a lesser extent that of syndecan-1 from HeLa cells. The fact that this acceleration was not inhibited by the CXCR4 antagonist AMD3100, anti-CXCR4 mAb 12G5, and CXCR4 gene silencing suggests its CXCR4-independence. Pre-treating the cells with heparitinases I, III, or with the protein kinase C (PKC) inhibitor, bisindolylmaleimide, significantly inhibited this accelerated shedding, which suggests the involvement of both cell-surface heparan sulfate and PKC transduction pathway. In contrast, Map Kinase or NF-
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 and 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.
Key words: chemokine / CXCR4 / glycosaminoglycan / proteoglycan / shedding
* These authors contributed equally to the work.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  K. Hayashida, W. C. Parks, and P. W. Park Syndecan-1 shedding facilitates the resolution of neutrophilic inflammation by removing sequestered CXC chemokines Blood, October 1, 2009; 114(14): 3033 - 3043. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. J. Heilpern, W. Wertheim, J. He, G. Perides, R. T. Bronson, and L. T. Hu Matrix Metalloproteinase 9 Plays a Key Role in Lyme Arthritis but Not in Dissemination of Borrelia burgdorferi Infect. Immun., July 1, 2009; 77(7): 2643 - 2649. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Vaisar, S. Y. Kassim, I. G. Gomez, P. S. Green, S. Hargarten, P. J. Gough, W. C. Parks, C. L. Wilson, E. W. Raines, and J. W. Heinecke MMP-9 Sheds the {beta}2 Integrin Subunit (CD18) from Macrophages Mol. Cell. Proteomics, May 1, 2009; 8(5): 1044 - 1060. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. D. Bass, M. R. Morgan, and M. J. Humphries Syndecans Shed Their Reputation as Inert Molecules Sci. Signal., March 31, 2009; 2(64): pe18 - pe18. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. Nikolova, C.-Y. Koo, S. A. Ibrahim, Z. Wang, D. Spillmann, R. Dreier, R. Kelsch, J. Fischgrabe, M. Smollich, L. H. Rossi, et al. Differential roles for membrane-bound and soluble syndecan-1 (CD138) in breast cancer progression Carcinogenesis, March 1, 2009; 30(3): 397 - 407. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Kuriyama and R. Mayor A role for Syndecan-4 in neural induction involving ERK- and PKC-dependent pathways Development, February 15, 2009; 136(4): 575 - 584. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Hayashida, P. D. Stahl, and P. W. Park Syndecan-1 Ectodomain Shedding Is Regulated by the Small GTPase Rab5 J. Biol. Chem., December 19, 2008; 283(51): 35435 - 35444. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Purushothaman, L. Chen, Y. Yang, and R. D. Sanderson Heparanase Stimulation of Protease Expression Implicates It as a Master Regulator of the Aggressive Tumor Phenotype in Myeloma J. Biol. Chem., November 21, 2008; 283(47): 32628 - 32636. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Su, S. A. Blaine, D. Qiao, and A. Friedl Membrane Type 1 Matrix Metalloproteinase-Mediated Stromal Syndecan-1 Shedding Stimulates Breast Carcinoma Cell Proliferation Cancer Res., November 15, 2008; 68(22): 9558 - 9565. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Szklarczyk, O. Ewaleifoh, J.-C. Beique, Y. Wang, D. Knorr, N. Haughey, T. Malpica, M. P. Mattson, R. Huganir, and K. Conant MMP-7 cleaves the NR1 NMDA receptor subunit and modifies NMDA receptor function FASEB J, November 1, 2008; 22(11): 3757 - 3767. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Hayashida, Y. Chen, A. H. Bartlett, and P. W. Park Syndecan-1 Is an in Vivo Suppressor of Gram-positive Toxic Shock J. Biol. Chem., July 18, 2008; 283(29): 19895 - 19903. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K Svennevig, T. Hoel, A. Thiara, S. Kolset, A Castelheim, T. Mollnes, F Brosstad, E Fosse, and J. Svennevig Syndecan-1 plasma levels during coronary artery bypass surgery with and without cardiopulmonary bypass Perfusion, May 1, 2008; 23(3): 165 - 171. [Abstract] [PDF]
|
|
|
|
 |
|
 P. Van Lint and C. Libert Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation J. Leukoc. Biol., December 1, 2007; 82(6): 1375 - 1381. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Sutton, V. Friand, D. Papy-Garcia, M. Dagouassat, L. Martin, R. Vassy, O. Haddad, O. Sainte-Catherine, M. Kraemer, L. Saffar, et al. Glycosaminoglycans and their synthetic mimetics inhibit RANTES-induced migration and invasion of human hepatoma cells Mol. Cancer Ther., November 1, 2007; 6(11): 2948 - 2958. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Su, S. A. Blaine, D. Qiao, and A. Friedl Shedding of Syndecan-1 by Stromal Fibroblasts Stimulates Human Breast Cancer Cell Proliferation via FGF2 Activation J. Biol. Chem., May 18, 2007; 282(20): 14906 - 14915. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Sutton, V. Friand, S. Brule-Donneger, T. Chaigneau, M. Ziol, O. Sainte-Catherine, A. Poire, L. Saffar, M. Kraemer, J. Vassy, et al. Stromal Cell-Derived Factor-1/Chemokine (C-X-C Motif) Ligand 12 Stimulates Human Hepatoma Cell Growth, Migration, and Invasion Mol. Cancer Res., January 1, 2007; 5(1): 21 - 33. [Abstract] [Full Text] [PDF]
|
|