Low molecular weight fucoidan and heparin enhance the basic fibroblast growth factor-induced tube formation of endothelial cells through heparan sulfate-dependent α6 overexpression

Molecular Pharmacology

Volumn 64, Issue 3, 2003, Pages 696-702

  Chabut, Delphine ^a   Fischer, Anne Marie ^a,c   Colliec Jouault, Sylvia ^d   Laurendeau, Ingrid ^b   Matou, Sabine ^d   Le Bonniec, Bernard ^a   Helley, Dominique ^a,c  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^d IFREMER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; BASIC FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FUCOIDIN; HEPARAN SULFATE; LOW MOLECULAR WEIGHT HEPARIN; MATRIGEL; MESSENGER RNA; POLYSACCHARIDE; PROTEOHEPARAN SULFATE;

ANGIOGENESIS; ARTICLE; CELL STIMULATION; ENDOTHELIUM CELL; FLOW CYTOMETRY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; ISCHEMIA; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REVASCULARIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CELLS, CULTURED; ENDOTHELIUM, VASCULAR; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; HEPARIN, LOW-MOLECULAR-WEIGHT; HEPARITIN SULFATE; HUMANS; INTEGRIN ALPHA6; MUSCLE FIBERS; NEOVASCULARIZATION, PHYSIOLOGIC; POLYSACCHARIDES; RNA, MESSENGER;

EID: 0041854298     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: 10.1124/mol.64.3.696     Document Type: Article

References (42)

1. Bauer J, Margolis M, Schreiner C, Edgell CJ, Azizkhan J, Lazarowski E, and Juliano RL (1992) In vitro model of angiogenesis using a human endothelium-derived permanent cell line: contributions of induced gene expression, G-proteins and integrins. J Cell Physiol 153:437-449.
2. Boraston AB, Notenboom V, Warren RA, Kilburn DG, Rose DR, and Davies G (2003) Structure and ligand binding of carbohydrate-binding module CsCBM6-3 reveals similarities with fucose-specific lectins and " galactose-binding" domain. J Mol Biol 327:659-669.
3. Carloni V, Romanelli RG, Mercurio AM, Pinzani M, Laffi G, Cotrozzi G, and Gentilini P (1998) Knockout of alpha6 beta1-integrin expression reverses the transformed phenotype of hepatocarcinoma cells. Gastroenterology 115:433-442.
4. Chevolot L, Mulloy B, Ratiskol J, Foucault A, and Colliec-Jouault S (2001) A disaccharide repeat unit is the major structure in fucoidans from two species of brown algae. Carbohydr Res 330:529-535.
5. Collen A, Smorenburg SM, Peters E, Lupu F, Koolwijk P, Van Noorden C, and van Hinsbergh VW (2000) Unfractionated and low molecular weight heparin affect fibrin structure and angiogenesis in vitro. Cancer Res 60:6196-6200.
6. Colliec-Jouault S, Millet J, Helley D, Sinquin C, and Fischer AM (2003) Effect of low-molecular-weight fucoidan on experimental arterial thrombosis in the rabbit and rat. Thromb Haemostasis, in press.
7. Diamond MS and Springer TA (1994) The dynamic regulation of integrin adhesiveness. Curr Biol 4:506-517.
8. Fantl WJ, Johnson DE, and Williams MT (1993) Signalling by receptor tyrosine kinases. Annu Rev Biochem 62:453-481.
9. Firsching A, Nickel P, Mora P, and Allolio B (1995) Antiproliferative and angiostatic activity of suramin analogues. Cancer Res 55:4957-4961.
10. Giraux JL, Matou S, Bros A, Tapon-Bretaudière J, Letourneur D, and Fischer AM (1998) Modulation of human endothelial cell proliferation and migration by fucoidan and heparin. Eur J Cell Biol 77:352-359.
11. Hughes PE, Diaz-Gonzalez F, Leong L, Wu C, McDonald JA, Shattil SJ, and Ginsberg MH (1996) Breaking the integrin hinge. A defined structural constraint regulates integrin signaling. J Biol Chem 271:6571-6574.
12. Klein S, Giancotti FG, Presta M, Albelda SM, Buck CA, and Rifkin DB (1993) Basic fibroblast growth factor modulates integrin expression in microvascular endothelial cells. Mol Biol Cell 4:973-982.
13. Kojima T, Takagi A, Maeda M, Segawa T, Shimizu A, Yamamoto K, Matsushita T, and Saito H (2001) Plasma levels of syndecan-4 (ryudocan) are elevated in patients with acute myocardial infarction. Thromb Haemost 85:793-799.
14. Kroon ME, Koolwijk P, van Goor H, Weidle UH, Collen A, van der Pluijm G, and van Hinsbergh VW (1999) Role and localization of urokinase receptor in the formation of new microvascular structures in fibrin matrices. Am J Pathol 154:1731-1742.
15. Li J, Brown LF, Laham RJ, Volk R, and Simons M (1997) Macrophage-dependent regulation of syndecan gene expression. Circ Res 81:785-796.
16. Liekens S, Leali D, Neyts J, Esnouf R, Rusnati M, Dell'Era P, Maudgal PC, De Clercq E, and Presta M (1999) Modulation of fibroblast growth factor-2 receptor binding, signaling and mitogenic activity by heparin-mimicking polysulfonated compounds. Mol Pharmacol 56:204-213.
17. Logeart D, Prigent-Richard S, Boisson-Vidal C, Chaubet F, Durand P, Jozefonvicz J and Letourneur D (1997a) Fucans, sulfated polysaccharides extracted from brown seaweeds, inhibit vascular smooth muscle cell proliferation. II. Degradation and molecular weight effect. Eur J Cell Biol 74:385-390.
18. Logeart D, Prigent-Richard S, Jozefonvicz J, and Letourneur D (1997b) Fucans, sulfated polysaccharides extracted from brown seaweeds, inhibit vascular smooth muscle cell proliferation. I. Comparison with heparin for antiproliferative activity, binding and internalization. Eur J Cell Biol 74:376-384.
19. Matou S, Helley D, Chabut D, Bros A, and Fischer AM (2002) Effect of fucoidan on fibroblast growth factor-2-induced angiogenesis in vitro. Thromb Res 106:213-221.
20. Millet J, Colliec Jouault S, Mauray S, Theveniaux J, Sternberg C, Boisson Vidal C, and Fischer AM (1999) Antithrombotic and anticoagulant activities of a low molecular weight fucoidan by subcutaneous route. Thromb Haemostasis 81:391-395.
21. Moscatelli D, Presta M, and Rifkin DB (1986) Purification of a factor from human placenta that stimulates capillary endothelial cell protease production, DNA synthesis and migration. Proc Natl Acad Sci USA 83:2091-2095.
22. Murata J, Saiki I, Makabe T, Tsuta Y, Tokura S, and Azuma I (1991) Inhibition of tumor-induced angiogenesis by sulfated chitin derivatives. Cancer Res 51:22-26.
23. Nardella A, Chaubet F, Boisson-Vidal C, Blondin C, Durand P and Jozefonvicz J (1996) Anticoagulant low molecular weight fucans produced by radical process and ion exchange chromatography of high molecular weight fucans extracted from the brown seaweed Ascophyllum nodosum, Carbohydr Res 289:201-208.
24. Ornitz DM, Yayon A, Flanagan JG, Svahn CM, Levi E, and Leder P (1992) Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells. Mol Cell Biol 12:240-247.
25. Quarto N and Amalric F (1994) Heparan sulfate proteoglycans as transducers of FGF-2 signalling. J Cell Sci 107:3201-3212.
26. Rabinovitz I, Nagle RB, and Cress AE (1995) Integrin alpha 6 expression in human prostate carcinoma cells is associated with a migratory and invasive phenotype in vitro and in vivo. Clin Exp Metastasis 13:481-491.
27. Rahmanian M, Pertoft H, Kanda S, Christofferson R, Claesson-Welsh L, and Heldin P (1997) Hyaluronan oligosaccharides induce tube formation of a brain endothelial cell line in vitro. Exp Cell Res 237:223-230.
28. Rhogani M and Moscatelli D (1992) Basic fibroblast growth factor is internalized through both receptor-mediated and heparan sulfate-mediated mechanisms. J Biol Chem 267:22156-22162.
29. Ribatti D, Urbinati C, Nico B, Rusnati M, Roncali L, and Presta M (1995) Endogenous basic fibroblast growth factor is implicated in the vascularization of the chick embryo chorioallantoic membrane. Dev Biol 170:39-49.
30. Rifkin DB and Moscatelli D (1989) Recent developments in the cell biology of basic fibroblast growth factor. J Cell Biol 109:1-6.
31. Rosenberg RD, Shworak NW, Liu J, Schwartz JJ, and Zhang L (1997) Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated? J Clin Investig 100:67-75.
32. Saksela O, Moscatelli D, Sommer A, and Rifkin DB (1988) Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J Cell Biol 107:743-751.
33. Sastry SK, Lakonishok M, Wu S, Truong TQ, Huttenlocher A, Turner CE, and Horwitz AF (1999) Quantitative changes in integrin and focal adhesion signaling regulate myoblast cell cycle withdrawal. J Cell Biol 144:1295-1309.
34. Soeda S, Kozako T, Iwata K, and Shimeno H (2000) Oversulfated fucoidan inhibits the basic fibroblast growth factor-induced tube formation by human umbilical vein endothelial cells: its possible mechanism of action. Biochim Biophys Acta 1497: 127-134.
35. Spivak-Kroizman T, Lemmon MA, Dikic I, Ladbury JE, Pinchasi D, Huang J, Jaye M, Crumley G, Schlessinger J, and Lax I (1994) Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation and cell proliferation. Cell 79:1015-1024.
36. Steegmaier M, Levinovitz A, Isenmann S, Borges E, Lenter M, Kocher HP, Kleuser B, and Vestweber D (1995) The E-selectin-ligand ESL-1 is a variant of a receptor for fibroblast growth factor. Nature (Lond) 373:615-620.
37. Tapon-Bretaudière J, Chabut D, Zierer M, Matou S, Helley D, Bros A, Mourao PA, and Fischer AM (2002) A fucosylated chondroitin sulfate from echinoderm modulates in vitro fibroblast growth factor 2-dependent angiogenesis. Mol Cancer Res 1:96-102.
38. Thornton M, Barkley L, Mason JC, and Shaunak S (1999) Anti-Kaposi's sarcoma and antiangiogenic activities of sulfated dextrins. Antimicrob Agents Chemother 43: 2528-2533.
39. Yanagisawa-Miwa A, Uchida Y, Nakamura F, Tomaru T, Kido H, Kamijo T, Sugimoto T, Kaji K, Utsuyama M, and Kurashima C (1992) Salvage of infarcted myocardium by angiogenic action of basic fibroblast growth factor. Science (Wash DC) 257:1401-1403.
40. Yayon A, Klagsbrun M, Esko JD, Leder P, and Ornitz DM (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64:841-848.
41. Yeh CH, Peng HC, and Huang TF (1999) Cytokines modulate integrin alpha(v-)beta(3)-mediated human endothelial cell adhesion and calcium signaling. Exp Cell Res 251:57-66.
42. Zugmaier G, Lippman ME, and Wellstein A (1992) Inhibition by pentosan polysulfate (PPS) of heparin-binding growth factors released from tumor cells and blockage by PPS of tumor growth in animals. J Natl Cancer Inst 84:1716-1724.