Glycosaminoglycans and syndecan-4 are involved in SDF-1/CXCL12-mediated invasion of human epitheloid carcinoma HeLa cells

Biochimica et Biophysica Acta - General Subjects

Volumn 1790, Issue 12, 2009, Pages 1643-1650

  Brule, Severine ^a   Friand, Véronique ^a   Sutton, Angela ^a,b   Baleux, Françoise ^c   Gattegno, Liliane ^a,b   Charnaux, Nathalie ^a,b  

^a UNIVERSITÉ PARIS 13   (France)

^b HÔPITAL JEAN VERDIER   (France)

^c INSTITUT PASTEUR   (France)

Author keywords

Chemokine; Glycosaminoglycan; Invasion; Proteoglycan; SDF 1 CXCL12; Syndecan

Indexed keywords

GELATINASE B; GLYCOSAMINOGLYCAN; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN KINASE C DELTA; PROTEOHEPARAN SULFATE; STRESS ACTIVATED PROTEIN KINASE; STROMAL CELL DERIVED FACTOR 1; SYNDECAN 4;

ARTICLE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIOID CELL; FEMALE; FLOW CYTOMETRY; HELA CELL; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; RNA INTERFERENCE;

EID: 71549123983     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2009.08.001     Document Type: Article

References (44)

1. Zlotnik A., and Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity 12 (2000) 121-127
2. Muller K., van Zandbergen G., Hansen B., et al. Chemokines, natural killer cells and granulocytes in the early course of Leishmania major infection in mice. Med. Microbiol. Immunol. 190 (2001) 73-76
3. Gerard C., and Rollins B.J. Chemokines and disease. Nat. Immunol. 2 (2001) 108-115
4. Hamon M., Mbemba E., Charnaux N., et al. A syndecan-4/CXCR4 complex expressed on human primary lymphocytes and macrophages and HeLa cell line binds the CXC chemokine stromal cell-derived factor-1 (SDF-1). Glycobiology 14 (2004) 311-323
5. Burger J.A., and Kipps T.J. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 107 (2006) 1761-1767
6. Mbemba E., Gluckman J.C., and Gattegno L. Glycan and glycosaminoglycan binding properties of stromal cell-derived factor (SDF)-1alpha. Glycobiology 10 (2000) 21-29
7. Kryczek I., Lange A., Mottram P., et al. CXCL12 and vascular endothelial growth factor synergistically induce neoangiogenesis in human ovarian cancers. Cancer Res. 65 (2005) 465-472
8. Gotte M. Syndecans in inflammation. FASEB J. 17 (2003) 575-591
9. Zimmermann P., and David G. The syndecans, tuners of transmembrane signaling. FASEB J. 13 Suppl (1999) S91-S100
10. Carey D.J. Syndecans: multifunctional cell-surface co-receptors. Biochem. J. 327 Pt 1 (1997) 1-16
11. Charnaux N., Brule S., Hamon M., et al. Syndecan-4 is a signaling molecule for stromal cell-derived factor-1 (SDF-1)/CXCL12. FEBS J. 272 (2005) 1937-1951
12. Amara A., Lorthioir O., Valenzuela A., et al. Stromal cell-derived factor-1alpha associates with heparan sulfates through the first beta-strand of the chemokine. J. Biol. Chem. 274 (1999) 23916-23925
13. Brule S., Charnaux N., Sutton A., et al. 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. Glycobiology 16 (2006) 488-501
14. Lucas M., and Mazzone T. Cell surface proteoglycans modulate net synthesis and secretion of macrophage apolipoprotein E. J. Biol. Chem. 271 (1996) 13454-13460
15. Sutton A., Friand V., Brule-Donneger S., 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. 5 (2007) 21-33
16. Zhou N., Fang J., Mukhtar M., Acheampong E., and Pomerantz R.J. Inhibition of HIV-1 fusion with small interfering RNAs targeting the chemokine coreceptor CXCR4. Gene Ther. 11 (2004) 1703-1712
17. Peng S.B., Peek V., Zhai Y., et al. Akt activation, but not extracellular signal-regulated kinase activation, is required for SDF-1alpha/CXCR4-mediated migration of epitheloid carcinoma cells. Mol. Cancer Res. 3 (2005) 227-236
18. Balabanian K., Lagane B., Infantino S., et al. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J. Biol. Chem. 280 (2005) 35760-35766
19. Schols D., Struyf S., Van Damme J., Este J.A., Henson G., and De Clercq E. Inhibition of T-tropic HIV strains by selective antagonization of the chemokine receptor CXCR4. J. Exp. Med. 186 (1997) 1383-1388
20. Charnaux N., Brule S., Chaigneau T., et al. RANTES (CCL5) induces a CCR5-dependent accelerated shedding of syndecan-1 (CD138) and syndecan-4 from HeLa cells and forms complexes with the shed ectodomains of these proteoglycans as well as with those of CD44. Glycobiology 15 (2005) 119-130
21. Strieter R.M. Chemokines: not just leukocyte chemoattractants in the promotion of cancer. Nat. Immunol. 2 (2001) 285-286
22. Gotte M., and Echtermeyer F. Syndecan-1 as a regulator of chemokine function. Sci. World J. 3 (2003) 1327-1331
23. Taylor K.R., and Gallo R.L. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J. 20 (2006) 9-22
24. Butcher E.C., and Picker L.J. Lymphocyte homing and homeostasis. Science 272 (1996) 60-66
25. Tang C.H., Tan T.W., Fu W.M., and Yang R.S. Involvement of matrix metalloproteinase-9 in stromal cell-derived factor-1/CXCR4 pathway of lung cancer metastasis. Carcinogenesis 29 (2008) 35-43
26. Kajiyama H., Shibata K., Terauchi M., Ino K., Nawa A., and Kikkawa F. Involvement of SDF-1alpha/CXCR4 axis in the enhanced peritoneal metastasis of epithelial ovarian carcinoma. Int. J. Cancer 122 (2008) 91-99
27. Wang Z., Ma Q., Liu Q., et al. Blockade of SDF-1/CXCR4 signalling inhibits pancreatic cancer progression in vitro via inactivation of canonical Wnt pathway. Br. J. Cancer 99 (2008) 1695-1703
28. Zhou N., Luo Z., Luo J., et al. Structural and functional characterization of human CXCR4 as a chemokine receptor and HIV-1 co-receptor by mutagenesis and molecular modeling studies. J. Biol. Chem. 278 (2001) 42826-42833
29. Brand S., Dambacher J., Beigel F., et al. CXCR4 and CXCL12 are inversely expressed in colorectal cancer cells and modulate cancer cell migration, invasion and MMP-9 activation. Exp. Cell Res. 310 (2005) 117-130
30. Tan C.T., Chu C.Y., Lu Y.C., et al. CXCL12/CXCR4 promotes laryngeal and hypopharyngeal squamous cell carcinoma metastasis through MMP-13-dependent invasion via the ERK1/2/AP-1 pathway. Carcinogenesis 29 (2008) 1519-1527
31. Tsubaki M., Matsuoka H., Yamamoto C., et al. The protein kinase C inhibitor, H7, inhibits tumor cell invasion and metastasis in mouse melanoma via suppression of ERK1/2. Clin. Exp. Metastasis 24 (2007) 431-438
32. Kharait S., Dhir R., Lauffenburger D., and Wells A. Protein kinase Cdelta signaling downstream of the EGF receptor mediates migration and invasiveness of prostate cancer cells. Biochem. Biophys. Res. Commun. 343 (2006) 848-856
33. Langlois A., Chouinard F., Flamand N., Ferland C., Rola-Pleszczynski M., and Laviolette M. Crucial implication of protein kinase C (PKC)-{delta}, PKC-{zeta}, ERK-1/2, and p38 MAPK in migration of human asthmatic eosinophils. J. Leukoc. Biol. 85 (2009) 656-663
34. Fitzgerald M.L., Wang Z., Park P.W., Murphy G., and Bernfield M. Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase. J. Cell Biol. 148 (2000) 811-824
35. Joensuu H., Anttonen A., Eriksson M., et al. Soluble syndecan-1 and serum basic fibroblast growth factor are new prognostic factors in lung cancer. Cancer Res. 62 (2002) 5210-5217
36. Liu W., Litwack E.D., Stanley M.J., Langford J.K., Lander A.D., and Sanderson R.D. Heparan sulfate proteoglycans as adhesive and anti-invasive molecules. Syndecans and glypican have distinct functions. J. Biol. Chem. 273 (1998) 22825-22832
37. Chalkiadaki G., Nikitovic D., Berdiaki A., et al. Fibroblast growth factor-2 modulates melanoma adhesion and migration through a syndecan-4-dependent mechanism. Int. J. Biochem. Cell Biol. 41 (2008) 1323-1331
38. Lundin L. H.Larsson, J. Kreuger, et al, Selectively desulfated heparin inhibits fibroblast growth factor-induced mitogenicity and angiogenesis. J. Biol. Chem. 276 (2000) 24653-24660
39. Netelenbos T., Van den Born J., Kessler F.L., et al. Proteoglycans on bone marrow endothelial cells bind and present SDF-1 towards hematopoietic progenitor cells. Leukemia 17 (2003) 175-184
40. Zhang Z., Coosmans C., and David G. Membrane heparan sulfate proteoglycan-supported FGF2-FGFR1 signaling. Evidence in support of the "cooperative end structures" model. J. Biol. Chem. 276 (2001) 41921-41929
41. Tan W., Martin D., and Gutkind J.S. The Galpha13-Rho signaling axis is required for SDF-1-induced migration through CXCR4. J. Biol. Chem. 281 (2006) 39542-39549
42. Saoncella S., Echtermeyer F., Denhez F., et al. Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 2805-2810
43. Bass M.D., and Humphries M.J. Cytoplasmic interactions of syndecan-4 orchestrate adhesion receptor and growth factor receptor signalling. Biochem. J. 368 (2002) 1-15
44. Simons M., and Horowitz A. Syndecan-4-mediated signalling. Cell. Signal. 13 (2001) 855-862