Immunostimulatory Activity of Fucoidan from the Brown Alga Fucus evanescens: Role of Sulfates and Acetates

REFERENCES

• Berteau , O. and Mulloy , B. 2003 . Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide . Glycobiology , 13 : 29R – 40R .
   PubMed Web of Science ®Google Scholar
• Holtkamp , A. D. , Kelly , S. , Ulber , R. and Lang , S. 2009 . Fucoidans and fucoidanases–focus on techniques for molecular structure elucidation and modification of marine polysaccharides . Appl. Microbiol. Biotechnol. , 82 : 1 – 11 .
   PubMed Web of Science ®Google Scholar
• Seeberger , P. H. and Werz , D. B. 2007 . Synthesis and medical applications of oligosaccharides . Nature , 446 : 1046 – 1051 .
   PubMed Web of Science ®Google Scholar
• Ernst , B. and Magnani , J. L. 2009 . From carbohydrate leads to glycomimetic drugs . Nat. Rev. Drug Discov. , 8 : 661 – 677 .
   PubMed Web of Science ®Google Scholar
• Kuznetsova , T. A. , Besednova , N. N. , Mamaev , A. N. , Momot , A. P. , Shevchenko , N. M. and Zvyagintseva , T. N. 2003 . Anticoagulant activity of fucoidan from brown algae Fucus evanescens of the Okhotsk Sea . Bull. Exp. Biol. Med. , 136 : 471 – 473 .
   PubMed Web of Science ®Google Scholar
• Li , B. , Lu , F. , Wei , X. and Zhao , R. 2008 . Fucoidan: structure and bioactivity . Molecules (Basel, Switzerland) , 13 : 1671 – 1695 .
   PubMed Web of Science ®Google Scholar
• Dürig , J. , Bruhn , T. , Zurborn , K. H. , Gutensohn , K. , Bruhn , H. D. and Beress , L. 1997 . Anticoagulant fucoidan fractions from Fucus vesiculosus induce platelet activation in vitro . Thromb. Res. , 85 : 479 – 491 .
   Google Scholar
• Thorlacius , H. , Vollmar , B. , Seyfert , U. T. , Vestweber , D. and Menger , M. D. 2000 . The polysaccharide fucoidan inhibits microvascular thrombus formation independently from P- and L-selectin function in vivo . Eur. J. Clin. Invest. , 30 : 804 – 810 .
   Google Scholar
• Soeda , S. , Sakaguchi , S. , Shimeno , H. and Nagamatsu , A. 1992 . Fibrinolytic and anticoagulant activities of highly sulfated fucoidan . Biochem. Pharmacol. , 43 : 1853 – 1858 .
   Google Scholar
• Boisson-Vidal , C. , Zemani , F. , Caligiuri , G. , Galy-Fauroux , I. , Colliec-Jouault , S. , Helley , D. and Fischer , A. M. 2007 . Neoangiogenesis induced by progenitor endothelial cells: effect of fucoidan from marine algae . Cardiovasc. Hematol. Agents Med. Chem. , 5 : 67 – 77 .
   PubMedGoogle Scholar
• Dias , P. F. , Siqueira , J. M. Jr. , Vendruscolo , L. F. , de Jesus Neiva , T. , Gagliardi , A. R. , Maraschin , M. and Ribeiro-do-Valle , R. M. 2005 . Antiangiogenic and antitumoral properties of a polysaccharide isolated from the seaweed Sargassum stenophyllum . Cancer Chemother. Pharmacol. , 56 : 436 – 446 .
   PubMed Web of Science ®Google Scholar
• Kim , M. H. and Joo , H. G. 2008 . Immunostimulatory effects of fucoidan on bone marrow-derived dendritic cells . Immunol. Lett. , 115 : 138 – 143 .
   Google Scholar
• Religa , P. , Kazi , M. , Thyberg , J. , Gaciong , Z. , Swedenborg , J. and Hedin , U. 2000 . Fucoidan inhibits smooth muscle cell proliferation and reduces mitogen-activated protein kinase activity . Eur. J. Vasc. Endovasc. Surg. , 20 : 419 – 426 .
   PubMed Web of Science ®Google Scholar
• Preobrazhenskaya , M. E. , Berman , A. E. , Mikhailov , V. I. , Ushakova , N. A. , Mazurov , A. V. , Semenov , A. V. , Usov , A. I. , Nifant’ev , N. E. and Bovin , N. V. 1997 . Fucoidan inhibits leukocyte recruitment in a model peritoneal inflammation in rat and blocks interaction of P-selectin with its carbohydrate ligand . Biochem. Mol. Biol. Int. , 43 : 443 – 451 .
   PubMedGoogle Scholar
• Shibata , H. , Kimura-Takagi , I. , Nagaoka , M. , Hashimoto , S. , Aiyama , R. , Iha , M. , Ueyama , S. and Yokokura , T. 2000 . Properties of fucoidan from Cladosiphon okamuranus tokida in gastric mucosal protection . BioFactors , 11 : 235 – 245 .
   PubMed Web of Science ®Google Scholar
• Nakamura , S. , Nambu , M. , Ishizuka , T. , Hattori , H. , Kanatani , Y. , Takase , B. , Kishimoto , S. , Amano , Y. , Aoki , H. , Kiyosawa , T. , Ishihara , M. and Maehara , T. 2008 . Effect of controlled release of fibroblast growth factor-2 from chitosan/fucoidan micro complex-hydrogel on in vitro and in vivo vascularization . J. Biomed. Mater. Res. , 85 : 619 – 627 .
   Google Scholar
• Sezer , A. D. and Akbuga , J. 2006 . Fucosphere–new microsphere carriers for peptide and protein delivery: preparation and in vitro characterization . J. Microencapsul. , 23 : 513 – 522 .
   PubMed Web of Science ®Google Scholar
• Kusaykin , M. , Bakunina , I. , Sova , V. , Ermakova , S. , Kuznetsova , T. , Besednova , N. , Zaporozhets , T. and Zvyagintseva , T. 2008 . Structure, biological activity, and enzymatic trans-formation of fucoidans from the brown seaweeds . Biotechnol. J. , 3 : 904 – 915 .
   PubMedGoogle Scholar
• Preeprame , S. , Hayashi , K. , Lee , J. B. , Sankawa , U. and Hayashi , T. 2001 . A novel antivirally active fucan sulfate derived from an edible brown alga, Sargassum horneri . Chem. Pharm. Bull. , 49 : 484 – 485 .
   PubMed Web of Science ®Google Scholar
• Evans , L. V. 1989 . Mucilaginous substances from macroalgae: an overview . Symp. Soc. Exp. Biol. , 43 : 455 – 461 .
   PubMedGoogle Scholar
• Honya , M. , Mori , H. , Anzai , M. , Araki , Y. and Nisizawa , K. 1999 . Monthly changes in the content of fucans, their constituent sugars and sulphate in cultured Laminaria japonica . Hydrobiologia , : 398 – 399 . 411–416
   Google Scholar
• Skriptsova , A. , Shevchenko , N. , Zvyagintseva , T. and Imbs , T. 2010 . Monthly changes in the content and monosaccharide composition of fucoidan from Undaria pinnatifida (Laminariales, Phaeophyta) . J. Appl. Phycol. , 22 : 79 – 86 .
   Google Scholar
• Zvyagintseva , T. N. , Shevchenko , N. M. , Chizhov , A. O. , Krupnova , T. N. , Sundukova , E. V. and Isakov , V. V. 2003 . Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions . J. Exp. Mar. Bio. Ecol. , 294 : 1 – 13 .
   Web of Science ®Google Scholar
• Yang , C. , Chung , D. , Shin , I. S. , Lee , H. , Kim , J. , Lee , Y. and You , S. 2008 . Effects of molecular weight and hydrolysis conditions on anticancer activity of fucoidans from sporophyll of Undaria pinnatifida . Int. J. Biol. Macromol. , 43 : 433 – 437 .
   PubMed Web of Science ®Google Scholar
• Mabeau , S. , Kloareg , B. and Joseleau , J. P. 1990 . Fractionation and analysis of fucans from brown algae . Phytochemistry , 29 : 2441 – 2445 .
   Web of Science ®Google Scholar
• Nishino , T. , Nishioka , C. , Ura , H. and Nagumo , T. 1994 . Isolation and partial characterization of a novel amino sugar-containing fucan sulfate from commercial Fucus vesiculosus fucoidan . Carbohydr. Res. , 255 : 213 – 224 .
   PubMed Web of Science ®Google Scholar
• Dubois , M. , Gilles , K. , Hamilton , J. K. , Rebers , P. A. and Smith , F. 1951 . A colorimetric method for the determination of sugars . Nature , 168 : 167
   PubMed Web of Science ®Google Scholar
• Dodgson , K. S. 1961 . Determination of inorganic sulphate in studies on the enzymic and non-enzymic hydrolysis of carbohydrate and other sulphate esters . Biochemical J. , 78 : 312 – 319 .
   PubMed Web of Science ®Google Scholar
• Waffenschmidt , S. and Jaenicke , L. 1987 . Assay of reducing sugars in the nanomole range with 2,2’-bicinchoninate . Anal. Biochem. , 165 : 337 – 340 .
   PubMed Web of Science ®Google Scholar
• Inaba , K. , Inaba , M. , Romani , N. , Aya , H. , Deguchi , M. , Ikehara , S. , Muramatsu , S. and Steinman , R. M. 1992 . Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor . J. Exp. Med. , 176 : 1693 – 1702 .
   PubMed Web of Science ®Google Scholar
• Kusaykin , M. , Chizhov , A. , Grachev , A. , Alekseeva , S. , Bakunina , I. , Nedashkovskaya , O. , Sova , V. and Zvyagintseva , T. 2006 . A comparative study of specificity of fucoidanases from marine microorganisms and invertebrates . J. Appl. Phycol. , 18 : 369 – 373 .
   Google Scholar
• Zvyagintseva , T. N. , Shevchenko , N. M. , Popivnich , I. B. , Isakov , V. V. , Scobun , A. S. , Sundukova , E. V. and Elyakova , L. A. 1999 . A new procedure for the separation of water-soluble polysaccharides from brown seaweeds . Carbohydr. Res. , 322 : 32 – 39 .
   Web of Science ®Google Scholar
• Anastyuk , S. D. , Shevchenko , N. M. , Nazarenko , E. L. , Dmitrenok , P. S. and Zvyagintseva , T. N. 2009 . Structural analysis of a fucoidan from the brown alga Fucus evanescens by MALDI-TOF and tandem ESI mass spectrometry . Carbohydr. Res. , 344 : 779 – 787 .
   PubMed Web of Science ®Google Scholar
• Yang , M. , Ma , C. , Sun , J. , Shao , Q. , Gao , W. , Zhang , Y. , Li , Z. , Xie , Q. , Dong , Z. and Qu , X. 2008 . Fucoidan stimulation induces a functional maturation of human monocyte-derived dendritic cells . Int. Immunopharmacol. , 8 : 1754 – 1760 .
   Google Scholar
• Jin , J. O. , Park , H. Y. , Xu , Q. , Park , J. I. , Zvyagintseva , T. , Stonik , V. A. and Kwak , J. Y. 2009 . Ligand of scavenger receptor class A indirectly induces maturation of human blood dendritic cells via production of tumor necrosis factor-alpha . Blood , 113 : 5839 – 5847 .
   PubMed Web of Science ®Google Scholar
• Teruya , T. , Takeda , S. , Tamaki , Y. and Tako , M. 2010 . Fucoidan isolated from Laminaria angustata var. longissima induced macrophage activation . Biosci. Biotechnol. Biochem. , 74 : 1960 – 1962 .
   PubMed Web of Science ®Google Scholar
• Teruya , T. , Tatemoto , H. , Konishi , T. and Tako , M. 2009 . Structural characteristics and in vitro macrophage activation of acetyl fucoidan from Cladosiphon okamuranus . Glycoconj. J. , 26 : 1019 – 1028 .
   Google Scholar
• Zaporozhets , T. S. , Krylova , N. V. , Ivanushko , L. A. , Gazha , A. K. , Smolina , T. P. and Besednova , N. N. 1997 . [The correction of phagocytosis defects in pseudotuberculosis infection with immunomodulators of natural origin] . Zh. Mikrobiol. Epidemiol. Immunobiol. , : 55 – 58 .
   Google Scholar
• Hayashi , K. , Nakano , T. , Hashimoto , M. , Kanekiyo , K. and Hayashi , T. 2008 . Defensive effects of a fucoidan from brown alga Undaria pinnatifida against herpes simplex virus infection . Int. Immunopharmacol. , 8 : 109 – 116 .
   PubMed Web of Science ®Google Scholar
• Maruyama , H. , Tamauchi , H. , Hashimoto , M. and Nakano , T. 2003 . Antitumor activity and immune response of Mekabu fucoidan extracted from Sporophyll of Undaria pinnatifida . In vivo (Athens, Greece) , 17 : 245 – 249 .
   PubMed Web of Science ®Google Scholar
• Maruyama , H. , Tamauchi , H. , Iizuka , M. and Nakano , T. 2006 . The role of NK cells in antitumor activity of dietary fucoidan from Undaria pinnatifida sporophylls (Mekabu) . Planta Med. , 72 : 1415 – 1417 .
   PubMed Web of Science ®Google Scholar
• Choi , E. M. , Kim , A. J. , Kim , Y. O. and Hwang , J. K. 2005 . Immunomodulating activity of arabinogalactan and fucoidan in vitro . J. Med. Food , 8 : 446 – 453 .
   PubMed Web of Science ®Google Scholar
• Maruyama , H. , Tamauchi , H. , Hashimoto , M. and Nakano , T. 2005 . Suppression of Th2 immune responses by mekabu fucoidan from Undaria pinnatifida sporophylls . Int. Arch. Allergy Immunol. , 137 : 289 – 294 .
   PubMed Web of Science ®Google Scholar
• Mizuno , M. , Nishitani , Y. , Hashimoto , T. and Kanazawa , K. 2009 . Different suppressive effects of fucoidan and lentinan on IL-8 mRNA expression in in vitro gut inflammation . Biosci. Biotechnol. Biochem. , 73 : 2324 – 2325 .
   PubMed Web of Science ®Google Scholar
• Saito , A. , Yoneda , M. , Yokohama , S. , Okada , M. , Haneda , M. and Nakamura , K. 2006 . Fucoidan prevents concanavalin A-induced liver injury through induction of endogenous IL-10 in mice . Hepatol. Res. , 35 : 190 – 198 .
   Google Scholar
• Kuznetsova , T. A. 2009 . Fucoidan extracted from Fucus evanescens brown algae corrects immunity and hemostasis disorders in experimental endotoxemia . Bull. Exp. Biol. Med. , 147 : 66 – 69 .
   Google Scholar
• Lepenies , B. and Seeberger , P. H. 2010 . The promise of glycomics, glycan arrays and carbohydrate-based vaccines . Immunopharmacol. Immunotoxicol. , 32 : 196 – 207 .
   PubMed Web of Science ®Google Scholar
• Lepenies , B. , Yin , J. and Seeberger , P. H. 2010 . Applications of synthetic carbohydrates to chemical biology . Curr. Opin. Chem. Biol. , 14 : 404 – 411 .
   PubMed Web of Science ®Google Scholar
• Boonyarattanakalin , S. , Liu , X. , Michieletti , M. , Lepenies , B. and Seeberger , P. H. 2008 . Chemical synthesis of all phosphatidylinositol mannoside (PIM) glycans from Mycobacterium tuberculosis . J. Am. Chem. Soc. , 130 : 16791 – 16799 .
   PubMed Web of Science ®Google Scholar
• Bernardes , G. J. , Kikkeri , R. , Maglinao , M. , Laurino , P. , Collot , M. , Hong , S. Y. , Lepenies , B. and Seeberger , P. H. 2010 . Design, synthesis and biological evaluation of carbohydrate-functionalized cyclodextrins and liposomes for hepatocyte-specific targeting . Org. Biomol. Chem. , 8 : 4987 – 4996 .
   PubMed Web of Science ®Google Scholar
• Wang , J. , Zhang , Q. , Zhang , Z. , Song , H. and Li , P. 2010 . Potential antioxidant and anticoagulant capacity of low molecular weight fucoidan fractions extracted from Laminaria japonica . Int. J. Biol. Macromol. , 46 : 6 – 12 .
   PubMed Web of Science ®Google Scholar
• Boisson-Vidal , C. , Chaubet , F. , Chevolot , L. , Sinquin , C. , Theveniaux , J. , Millet , J. , Sternberg , C. , Mulloy , B. and Fischer , A. M. 2000 . Relationship between antithrombotic activities of fucans and their structure . Drug Dev. Res. , 51 : 216 – 224 .
   Web of Science ®Google Scholar
• Teruya , T. , Konishi , T. , Uechi , S. , Tamaki , H. and Tako , M. 2007 . Anti-proliferative activity of oversulfated fucoidan from commercially cultured Cladosiphon okamuranus TOKIDA in U937 cells . Int. J. Biol. Macromol. , 41 : 221 – 226 .
   PubMed Web of Science ®Google Scholar
• Drozd , N. N. , Tolstenkov , A. S. , Makarov , V. A. , Kuznetsova , T. A. , Besednova , N. N. , Shevchenko , N. M. and Zvyagintseva , T. N. 2006 . Pharmacodynamic parameters of anticoagulants based on sulfated polysaccharides from marine algae . Bull. Exp. Biol. Med. , 142 : 591 – 593 .
   Google Scholar
• Dace , R. , McBride , E. , Brooks , K. , Gander , J. , Buszko , M. and Doctor , V. M. 1997 . Comparison of the anticoagulant action of sulfated and phosphorylated polysaccharides . Thromb. Res. , 87 : 113 – 121 .
   PubMed Web of Science ®Google Scholar
• Koyanagi , S. , Tanigawa , N. , Nakagawa , H. , Soeda , S. and Shimeno , H. 2003 . Oversulfation of fucoidan enhances its anti-angiogenic and antitumor activities . Biochem. Pharmacol. , 65 : 173 – 179 .
   PubMed Web of Science ®Google Scholar