A polysaccharide isolated from the brown seaweed Sargassum stenophyllum exerts antivasculogenic effects evidenced by modified morphogenesis

Microvascular Research

Volumn 75, Issue 1, 2008, Pages 34-44

  Dias, Paulo Fernando ^a   Siqueira Jr , Jarbas Mota ^a   Maraschin, Marcelo ^a   Ferreira, Antônio Gilberto ^b   Gagliardi, Antônio Ricardo ^c   Ribeiro do Valle, Rosa Maria ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

^c UNILUS   (Brazil)

Author keywords

Angiostatic activity; Morphogenesis; Polysaccharide; Sargassum stenophyllum; Vasculogenesis

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; HYDROCORTISONE; MORPHOGEN; PLANT EXTRACT; POLYSACCHARIDE; SARGASSUM STENOPHYLLUM EXTRACT; UNCLASSIFIED DRUG;

ANGIOGENESIS; ARTICLE; BODY BUILD; BRAIN SIZE; CELL WALL; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFECT; DRUG INHIBITION; DRUG ISOLATION; EMBRYO; EMBRYOTOXICITY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; SARGASSUM STENOPHYLLUM; SEAWEED; VITELLINE MEMBRANE;

ANGIOGENESIS INHIBITORS; ANIMALS; BLOOD VESSELS; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBROBLAST GROWTH FACTOR 2; HYDROCORTISONE; MOLECULAR STRUCTURE; MORPHOGENESIS; NEOVASCULARIZATION, PHYSIOLOGIC; POLYSACCHARIDES; SARGASSUM; TIME FACTORS;

ALGAE; SARGASSUM STENOPHYLLUM;

EID: 37249084197     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2007.05.004     Document Type: Article

References (68)

1. Abdel-Fattah A.F., Hussein M.M.-D., and Salem H.M. Studies of purification and some properties of sargassan, a sulphated heteropolysaccharide from Sargassum linifolium. Carbohydr. Res. 33 (1974) 9-17
2. Aybar M.J., and Mayor R. Early induction of neural crest cells: lessons learned from frog, fish and chick. Curr. Opin. Genet. Dev. 12 (2002) 452-458
3. Bergers G., and Benjamin L.E. Tumorigenesis and the angiogenesis switch. Nat. Rev., Cancer 3 (2003) 401-410
4. Burg M.A., Halfter W., and Cole G.J. Analysis of proteoglycan expression in developing chicken brain: characterization of a heparan sulfate proteoglycan that interacts with the neural cell adhesion molecule. J. Neurosci. Res. 41 (1995) 49-64
5. Carmeliet P. Angiogenesis in health and disease. Nat. Med. 9 6 (2003) 653-660
6. Carmeliet P., and Jain R.K. Angiogenesis in cancer and other diseases. Nature 407 (2000) 249-257
7. Chapman S.C., Collignon J., Schoenwolf G.C., and Lumsden A. Improved method for chick whole-embryo culture using a filter paper carrier. Dev. Dyn. 220 (2001) 284-289
8. Coffey Jr. R.J., Leof E.B., Shipley G.D., and Moses H.L. Suramin inhibition of growth factor receptor binding and mitogenicity in AKR-2B cells. J. Cell. Physiol. 132 (1987) 143-148
9. Crum R., Szabo S., and Folkman J. A new class of steroids inhibits angiogenesis in the presence of heparin or a heparin fragment. Science 230 (1985) 1375-1378
10. Dethlefsen S.M., Shepro D., and D'amore P.A. Arachidonic acid metabolites in bFGF-, PDGF-, and serum stimulated vascular cell growth. Exp. Cell Res. 212 (1994) 262-273
11. Dhoot G.K., Gustafsson M.K., Al X., Sun W., Standiford D.M., and Emerson Jr. C.P. Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293 (2001) 1663-1666
12. Dias P.F., Siqueira J.M., Vendruscolo L.F., Neiva T.J., Maraschin M., Gagliardi A.R., and Ribeiro-Do-Valle R.M. Antiangiogenic and antitumoral properties of polysaccharide isolated from the seaweed Sargassum stenophyllum. Cancer Chemother. Pharmacol. 56 4 (2005) 436-446
13. Dowd C.J., Cooney C.L., and Nugent M.A. Heparan sulfate mediates bFGF transport through basement membrane by diffusion with rapid reversible binding. J. Biol. Chem. 274 (1999) 5236-5244
14. Duarte M.E.R., Cardoso M.A., Noseda M., and Cerezo A.S. Structural studies on fucoidans from the brown seaweed Sargassum stenophyllum. Carbohydr. Res. 333 (2001) 281-293
15. Fafeur V., Jiang Z.P., and Bohlen P. Signal transduction by bFGF, but not TGFB1, involves arachidonic acid metabolism in endothelial cells. J. Cell. Physiol. 149 (1991) 277-283
16. Fairbrother W.J., Champe M.A., Christinger H.W., Keyt B.A., and Starovasnik M.A. Solution structure of the heparin-binding domain vascular endothelial growth factor. Structure 6 (1998) 637-648
17. Fidler I.J. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat. Rev. Cancer 3 (2003) 1-6
18. Folberg R., Hendrix M.J., and Maniotis A.J. Vasculogenic mimicry and tumor angiogenesis. Am. J. Pathol. 156 2 (2000) 361-381
19. Folkman J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285 (1971) 1182-1186
20. Folkman J., and Shing Y. Control of angiogenesis by heparin and other sulfated polysaccharides. Adv. Exp. Med. Biol. 313 (1992) 355-364
21. Gallagher J.T. Heparan sulphates as membrane receptors for the fibroblast growth factor. Eur. J. Clin. Chem. Clin. Biochem. 32 (1994) 239-247
22. Gagliardi A.R., and Collins D.C. Inhibition of angiogenesis by antiestrogens. Cancer Res. 53 (1993) 533-535
23. Gagliardi A.R., Hadd H.E., and Collins D.C. Inhibition of angiogenesis by suramin. Cancer Res. 52 (1992) 5073-5075
24. Gridley T. Notch signaling during vascular development. PNAS USA 98 (2001) 10733-10738
25. Grumet M., Flaceus A., and Margolis R.R.U. Functional characterization of chondroitin sulphate proteoglycans of brain: interaction with neuron and neural cell adhesion molecules. J. Cell Biol. 120 3 (1993) 815-824
26. Gullino P.M. Angiogenesis and oncogenesis. J. Natl. Cancer Inst. 61 (1978) 639-643
27. Hanahan D., and Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86 (1996) 353-364
28. Hamburger V., and Hamilton H. A series of normal stages in the development of the chick embryo. J. Morphol. 88 (1951) 49-92
29. Hendrix M.J.C., Seftor E.A., Hess A.R., and Seftor R.E.B. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nat. Rev., Cancer 3 (2003) 411-421
30. Hlatky L., and Folkman F. Clinical application antiangiogenic therapy: microvessel density, what it does and doesn't tell us. J. Natl. Cancer Inst. 94 (2002) 883-893
31. Jakob W., Jentzsch K.D., Mauersberger B., and Heder G. The chick embryo chorioallantoic membrane as a bioassay for angiogenesis factors: reactions induced by carrier materials. Exp. Pathol. 15 5 (1978) 241-249
32. Jackson C.J., Giles I., Knop A., Nethery A., and Schrieber L. Sulfated polysaccharides are required for collagen-induced vascular tube formation. Exp. Cell Res. 215 (1994) 294-302
33. Katz B.Z., and Yamada K.M. Integrins in morphogenesis and signaling. Biochimie 79 (1997) 467-476
34. Koyanagi S., Tanigawa N., Nakagawa H., Soeda S., and Shimeno H. Oversulfation of fucoidan enhances its anti-angiogenic and antitumor activities. Biochem. Pharmacol. 65 (2003) 173-179
35. Leali D., Belleri M., Urbinati C., Coltrini D., Oreste P., Zoppetti G., Ribatti D., Rusnati M., and Presta M. Fibroblast growth factor-2 antagonist activity and angiostatic capacity of sulfated Escherichia coli K5 polysaccharide derivatives. J. Biol. Chem. 41 (2001) 37900-37908
36. Lim S.N., Cheung P.C.K., Ooi V.E.C., and Ang P.O. Evaluation of antioxidative activity of extracts from a brown seaweed, Sargassum siliquastrum. J. Agric. Food Chem. 50 (2002) 3862-3866
37. Lee Y.S., Yang H.O., Shin K.H., Choi H.S., Jung S.H., Hoon S., Kim Y.M., Oh D.K., Linhardt R.J., and Kim Y.S. Suppression of tumor growth by a new glycosaminoglycan isolated from the African giant snail Achatina fulica. Eur. J. Pharmacol. 465 (2003) 191-198
38. Maniotis A.J., Folberg R., Hess A., Seftor E.A., Gardner L.M., Pe'er J., Trent J.M., Meltzer P.S., and Hendrix M.J. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am. J. Pathol. 155 3 (1999) 739-752
39. Männer J., Seidl W., and Steding G. Formation of cervical flexure: an experimental study on chick embryos. Acta Anat. 152 (1995) 1-10
40. Maraschin M., Carobrez S.G., Persike D., Peixoto M.L., Ferreira A.G., Ferracin R., Verpoorte R., and Fontana J.D. Cell wall polysaccharides from Mandevilla velutina (Apocynaceae) cultured cells: extraction and chemical structure. Carbohyd. Polym. 41 (2000) 55-60
41. Matou S., Helly D., Chabut D., Bros A., and Fischer A.-M. Effect of fucoidan on fibroblast growth factor-2-induced angiogenesis in vitro. Thromb. Res. 106 (2002) 213-221
42. McCormick J.F., Nassauer J., Bielunas J., and Leighton J. Anatomy of the chick chorioallantoic membrane relevant to its use as a substrate in bioassay systems. Scan. Electron. Microsc. 4 (1984) 2023-2030
43. Miao H., Ornitz D.M., Aingorn E., Ben-Sasson S.A., and Vlodavsky I. Modulation of fibroblast growth factor-2 receptor binding, dimerization, signaling, and angiogenic activity by a synthetic heparin-mimicking polyanionic compound. J. Clin. Invest. 99 (1997) 1565-1575
44. Mundhenke C., Meyer K., Drew S., and Friedl A. Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 receptor binding in breast carcinomas. Am. J. Pathol. 160 (2002) 185-194
45. Nguyen M., Shing Y., and Folkman J. Quantitation of angiogenesis and antiangiogenesis. In the chick embryo chorioallantoic membrane. Microvasc. Res. 47 (1994) 31-40
46. Noda H., Amano H., Arashima K., Hashimoto S., and Nisizawa K. Studies on the antitumor activity of marine algae. Nipp. Suiss. Gak. 55 7 (1989) 1259-1264
47. Peek M.J., Norman C., Markhan R., and Frases I.S. The chick chorioallantoic membrane assay: an improved technique for the study of angiogenic activity. Exp. Pathol. 34 1 (1988) 35-40
48. Pesenti E., Sol F., Mongelli N., Grandi M., and Spreafico F. Suramin prevents neovascularization and tumor growth through blocking of basic fibroblast growth factor activity. Br. J. Cancer 66 (1992) 367-374
49. Princivalle M., and de Agostini A. Developmental roles of heparan sulfate proteoglycans a comparative review in Drosophyla, mouse and human. Int. J. Dev. Biol. 46 (2002) 267-278
50. Rafii S., and Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med. 9 6 (2003) 702-712
51. Rafii S., Lyden D., Benezra R., Hattori K., and Heissig B. Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy?. Nat. Rev., Cancer 2 8 (2002) 626-635
52. Risau W., Sariola H., Zerves H.G., Sasse J., Ekblom P., Kemler R., and Doetschman T. Vasculogenesis and angiogenesis in embryonic-stem-cell-derived embryoid bodies. Development 102 3 (1988) 471-478
53. Ruiter M.C., De Poelmann E., Mentink M.M.T., Vaniperen L., and Gittenberger-De-Groot A.C. The early formation of the vascular system in quail embryos. In: Ruiter M.C. (Ed). Development of the Vascular System in the Embryo. A Concept of the Origin of Systemic-Pulmonary Collateral Arteries, Leiden (1992) 99-186
54. Selvendran R.R., Stevens B.J.H., and O'neill M.A. Developments in the isolation and analysis of cell walls from edible plants. In: Brett C.T., and Hillman J.R. (Eds). Biochemistry of the Plant Cell Wall, London (1985) 39-78
55. Shubik P., and Warren B.A. Additional literature on 'vasculogenic mimicry' not cited. Am. J. Pathol. 156 (2000) 736-741
56. Simon H., Hornbruch A., and Lumsden A. Independent assignment of antero-posterior and dorso-ventral positional values in the developing chick hindbrain. Curr. Biol. 5 2 (1995) 205-214
57. Sinaÿ P. Sugars slide into heparin activity. Nature 398 (1999) 377-378
58. Soeda S., Kosako T., Iwata K., and Shimeno H. 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 (2000) 127-134
59. Takaku T., Kimura Y., and Okuda H. Isolation of an antitumor compound from Agaricus blazei Murill and its mechanism of action. J. Nutr. 131 (2001) 1409-1413
60. Takamatsu T., and Fujita S. Growth of notochord and formation of cranial and mesencephalic flexures in chicken embryo. Dev. Growth Differ. 29 5 (1987) 497-502
61. Tan W., Lin L., Li M., Zhang Y.X., Tong Y., Xiao D., and Ding J. Quercetin, a dietary-derived flavonoid, possesses antiangiogenic potential. Eur. J. Pharmacol. 459 2-3 (2003) 255-262
62. Tobelem G. Endothelial cell growth: biology and pharmacology in relation to angiogenesis. Blood Coagul. Fibrinolysis 1 (1990) 703-705
63. Trento F., Cattaneo F., Pescador R., Porta R., and Ferro L. Antithrombin activity of an algal polysaccharide. Thromb. Res. 102 5 (2001) 457-465
64. Vu M.T., Smith C.F., Burger P.C., and Klintworth G.K. An evaluation of methods to quantitate the chick chorioallantoic membrane assay in angiogenesis. Lab. Invest. 53 4 (1985) 499-508
65. Yancopoulos G.D., Davis S., Gale N.W., Rudge J.S., Wiegand S.J., and Holash J. Vascular specific growth factors and blood vessel formation. Nature 407 (2000) 242-248
66. Yayon A., and Klagsbrun M. Autocrine transformation by chimeric signal peptide-basic fibroblast growth factor: reversal by suramin. PNAS USA 87 (1990) 5346-5350
67. Zammaretti P., and Zisch A.H. Adult endothelial progenitor cells renewing vasculature. Int. J. Biochem. Cell Biol. 37 3 (2005) 493-503
68. Zhou Y., Damsky C.H., and Fisher S.J. Pre-eclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype: one cause of defective endovascular invasion in this syndrome?. J. Clin. Invest. 99 (1997) 2152-2164