Review
Structure, biological activity, and enzymatic transformation of fucoidans from the brown seaweeds
Mikhail Kusaykin,
Irina Bakunina,
Victoria Sova,
Svetlana Ermakova,
Tatyana Kuznetsova,
Natalya Besednova,
Tatyana Zaporozhets,
Tatyana Zvyagintseva Dr.,
Mikhail Kusaykin
Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
Search for more papers by this authorIrina Bakunina
Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
Search for more papers by this authorVictoria Sova
Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
Search for more papers by this authorSvetlana Ermakova
Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
Search for more papers by this authorTatyana Kuznetsova
Research Institute of Epidemiology and Microbiology, Russian Academy of Medical Sciences, Vladivostok, Russia
Search for more papers by this authorNatalya Besednova
Research Institute of Epidemiology and Microbiology, Russian Academy of Medical Sciences, Vladivostok, Russia
Search for more papers by this authorTatyana Zaporozhets
Research Institute of Epidemiology and Microbiology, Russian Academy of Medical Sciences, Vladivostok, Russia
Search for more papers by this authorCorresponding Author
Tatyana Zvyagintseva Dr.
Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
Prospect 100-Letiya Vladivostoka 159, 690022, Vladivostok, Russia, Fax: +7-4232-314050Search for more papers by this author
Mikhail Kusaykin,
Irina Bakunina,
Victoria Sova,
Svetlana Ermakova,
Tatyana Kuznetsova,
Natalya Besednova,
Tatyana Zaporozhets,
Tatyana Zvyagintseva Dr.,
Mikhail Kusaykin
Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
Search for more papers by this authorIrina Bakunina
Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
Search for more papers by this authorVictoria Sova
Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
Search for more papers by this authorSvetlana Ermakova
Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
Search for more papers by this authorTatyana Kuznetsova
Research Institute of Epidemiology and Microbiology, Russian Academy of Medical Sciences, Vladivostok, Russia
Search for more papers by this authorNatalya Besednova
Research Institute of Epidemiology and Microbiology, Russian Academy of Medical Sciences, Vladivostok, Russia
Search for more papers by this authorTatyana Zaporozhets
Research Institute of Epidemiology and Microbiology, Russian Academy of Medical Sciences, Vladivostok, Russia
Search for more papers by this authorCorresponding Author
Tatyana Zvyagintseva Dr.
Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia
Prospect 100-Letiya Vladivostoka 159, 690022, Vladivostok, Russia, Fax: +7-4232-314050Search for more papers by this authorAbstract
Recent advances in the study of fucoidans, biologically active sulfated α-L-fucans of diverse structures and synthesized exclusively by marine organisms, are overviewed. Their structure, biological activity, the products of their enzymatic degradation and the different enzymes of degradation and modification are considered.
REFERENCES
- 1 Berteau, O., Mulloy, B., Sulfated fucans, fresh perspectives: Structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology 2003, 13, 29R–40R.
- 2 Gacesa, P., Enzymic degradation of alginates. Int. J. Biochem. 1992, 24, 545–552.
- 3 Wong, T. Y., Preston, L. A., Schiller, N. L., Alginate lyase: Review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu. Rev. Microbiol. 2000, 54, 289–340.
- 4 Giordano, A., Andreotti, G., Tramice, A., Trincone, A., Marine glycosyl hydrolases in the hydrolysis and synthesis of oligosaccharides. Biotechnol. J. 2006, 1, 511–530.
- 5 Mourao, P. A., Use of sulfated fucans as anticoagulant and antithrombotic agents: Future perspectives. Curr. Pharm. Des. 2004, 10, 967–981.
- 6 Linhardt, R. J., Galliher, P. M., Cooney, C. L., Polysaccharide lyases. Appl. Biochem. Biotechnol. 1986, 12, 135–176.
- 7 Sutherland, I. W., Polysaccharide lyases. FEMS Microbiol. Rev. 1995, 16, 323–347.
- 8 Honya, M., Mori, H., Anzai, M., Araki, Y. et al., Monthly changes in the content of fucans, their constituent sugars and sulphate in cultured Laminaria japonica. Hydrobiologia 1999, 399, 411–416.
- 9 Obluchinskaya, E. D., Voskoboynikov, G. M., Galinkin, V. A., Content of alginic acid and fucoidan in the Fucales of Barentsev sea. Prikl. Biokhim. Microbiol. 2002, 38, 213–216.
- 10 Usov, A. I., Smirnova, G. P., Bilan, M. I., Shashkov, A. S., Polysaccharide of seaweeds. Brown alga Laminaria saccharina (L.). Bioorgan. Khim. (Russia) 1998, 24, 437–445.
- 11 Zvyagintseva, T. N., Shevchenko, N. M., Chizhov, A. O. et al., Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions. J. Exp. Mar. Biol. Ecol. 2003, 294, 1–13.
- 12 Bilan, M. I., Grachev, A. A., Ustuzhanina, N. E., Shashkov, A. S. et al., A highly regular fraction of a fucoidan from the brown seaweed Fucus distichus L. Carbohydr. Res. 2004, 339, 511–517.
- 13 Fitton, J. H., Fucoidans: Healthful saccharides from the sea. GlycoSci. Nutr. 2005, 6, 1–6.
- 14 Zvyagintseva, T., Shevchenko, N., Nazarenko, E., Gorbach, V. et al., Water-soluble polysaccharides of some brown algae of the Russian Far-East. Structure and biological action of low-molecular mass polyuronans. J. Exp. Mar. Biol. Ecol. 2005, 320, 123–131.
- 15 Percival, E., McDowell, R. H., Chemistry and enzymology of marine algal polysaccharides. Academic Press, London 1967, pp. 157–175.
- 16 Alves, A. P., Mulloy, B., Diniz, J. A., Mourao, P. A., Sulfated polysaccharides from the egg jelly layer are species-specific inducers of acrosomal reaction in sperms of sea urchins. J. Biol. Chem. 1997, 272, 6965–6971.
- 17 Bilan, M. I., Grachev, A. A., Ustuzhanina, N. E., Shashkov, A. S. et al., Structure of a fucoidan from the brown seaweed Fucus evanescens C. Ag. Carbohydr. Res. 2002, 337, 719–730.
- 18 Chevolot, L., Mulloy, B., Ratiskol, J., Foucault, A. et al., A disaccharide repeat unit is the major structure in fucoidans from two species of brown algae. Carbohydr. Res. 2001, 330, 529–535.
- 19 Chizhov, A. O., Dell, A., Morris, H. R., Haslam, S. M. et al., A study of fucoidan from the brown seaweed Chorda filum. Carbohydr. Res. 1999, 320, 108–119.
- 20 Kusaykin, M. I., Chizhov, A. O., Grachev, A. A., Alekseeva, S. A. et al., A comparative study of specificity of fucoidanases from marine microorganisms and invertebrates. J. Appl. Phycol. 2006, 18, 369–373.
- 21 Nagaoka, M., Shibata, H., Kimura-Takagi, I., Hashimoto, S. et al., Structural study of fucoidan from Cladosiphon okamuranus TOKIDA. Glycoconj. J. 1999, 16, 19–26.
- 22 Nishino, T., Nagumo, T., Kiyohara, H., Yamada, H., Structural characterization of a new anticoagulant fucan sulfate from the brown seaweed Ecklonia kurome. Carbohydr. Res. 1991, 211, 77–90.
- 23 Patankar, M. S., Oehninger, S., Barnett, T., Williams, R. L. et al., A revised structure for fucoidan may explain some of its biological activities. J. Biol. Chem. 1993, 268, 21770–21776.
- 24 Ribeiro, A. C., Vieira, R. P., Mourao, P. A., Mulloy, B., A sulfated α-L-fucan from sea cucumber. Carbohydr. Res. 1994, 255, 225–240.
- 25 Sakai, T., Kawai, T., Kato, I., Isolation and characterization of a fucoidan-degrading marine bacterial strain and its fucoidanase. Mar. Biotechnol. 2004, 6, 335–346.
- 26 Shevchenko, N. M., Anastyuk, S. D., Gerasimenko, N. I., Dmitrenok, P. S. et al., Polysaccharide and lipid composition of the brown seaweed Laminaria gurjanovae. Bioorgan. Khim. (Russia) 2007, 33, 96–107.
- 27 Lee, J. B., Hayashi, K., Hashimoto, M., Nakano, T. et al., Novel antiviral fucoidan from sporophyll of Undaria pinnatifida (Mekabu). Chem. Pharm. Bull. (Tokyo) 2004, 52, 1091–1094.
- 28 Colin, S., Deniaud, E., Jam, M., Descamps, V. et al., Cloning and biochemical characterization of the fucanase FcnA: Definition of a novel glycoside hydrolase family specific for sulfated fucans. Glycobiology 2006, 16, 1021–1032.
- 29 Descamps, V., Colin, S., Lahaye, M., Jam, M. et al., Isolation and culture of a marine bacterium degrading the sulfated fucans from marine brown algae. Mar. Biotechnol. 2006, 8, 27–39.
- 30 Ellouali, M., Boisson-Vidal, C., Durand, P., Jozefonvicz, J., Antitumor activity of low molecular weight fucans extracted from brown seaweed Ascophyllum nodosum. Anticancer Res. 1993, 13, 2011–2019.
- 31 Maruyama, H., Nakajima, J., Yamamoto, I., A study on the anticoagulant and fibrinolytic activities of a crude fucoidan from the edible brown seaweed Laminaria religiosa, with special reference to its inhibitory effect on the growth of sarcoma-180 ascites cells subcutaneously implanted into mice. Kitasato Arch. Exp. Med. 1987, 60, 105–121.
- 32 Yamamoto, I., Takahashi, M., Suzuki, T., Seino, H. et al., Antitumor effect of seaweeds. IV. Enhancement of antitumor activity by sulfation of a crude fucoidan fraction from Sargassum kjellmanianum. Jpn. J. Exp. Med. 1984, 54, 143–151.
- 33 Zapopozhets, T. S., Besednova, N. N., Loenko, I. N., Antibacterial and immunomodulating activity of fucoidan. Antibiot. Khimioter. 1995, 40, 9–13.
- 34 Zaporozhets, T. S., Kuznetsova, T. A., Smolina, T. P., Shevchenko, N. M. et al., Immunotropic and anticoagulant activity of fucoidan from brown seaweed Fucus evanescens: Prospects of application in medicine. J. Microbiol. 2006 54–58.
- 35 Hirmo, S., Utt, M., Ringner, M., Wadstrom, T., Inhibition of heparan sulfate and other glycosaminoglycans binding to Helicobacter pylori by various polysulfated carbohydrates. FEMS Immunol. Med. Microbiol. 1995, 10, 301–306.
- 36 Shibata, H., Kimura, T. I., Nagaoka, M., Hashimoto, S. et al., Inhibitory effect of Cladosiphon fucoidan on the adhesion of Helicobacter pylori to human gastric cells. J. Nutr. Sci. Vitaminol. (Tokyo) 1999, 45, 325–336.
- 37 Adhikari, U., Mateu, C. G., Chattopadhyay, K., Pujol, C. A. et al., Structure and antiviral activity of sulfated fucans from Stoechospermum marginatum. Phytochemistry 2006, 67, 2474–2482.
- 38 McClure, M. O., Moore, J. P., Blanc, D. F., Scotting, P. et al., Investigations into the mechanism by which sulfated polysaccharides inhibit HIV infection in vitro. AIDS Res. Hum. Retroviruses 1992, 8, 19–26.
- 39 Cumashi, A., Ushakova, N. A., Preobrazhenskaya, M. E., D'Incecco, A. et al., A comparative study of the antiinflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 2007, 17, 541–552.
- 40 Matsui, M. S., Muizzuddin, N., Arad, S., Marenus, K., Sulfated polysaccharides from red microalgae have antiinflammatory properties in vitro and in vivo. Appl. Biochem. Biotechnol. 2003, 104, 13–22.
- 41 Semenov, A. V., Mazurov, A. V., Preobrazhenskaya, M. E., Sulfated polysaccharides as inhibitors of receptor activity of Pselectin and P-selectin-dependent inflammation. Quest. Med. Chem. 1999, 2, 135–143.
- 42 Zen, K., Liu, Y., Cairo, D., Parkos, C. A., CD11b/CD18-dependent interactions of neutrophils with intestinal epithelium are mediated by fucosylated proteoglycans. J. Immunol. 2002, 169, 5270–5278.
- 43 Zhang, X. W., Liu, Q., Thorlacius, H., Inhibition of selectin function and leukocyte rolling protects against dextran sodium sulfate-induced murine colitis. Scand. J. Gastroenterol. 2001, 36, 270–275.
- 44 Drozd, N. N., Tolstenkov, A. S., Makarov, V. A., Kuznetsova, T. A. et al., Pharmacodynamic parameters of anticoagulants based on sulfated polysaccharides from marine algae. Bull. Exp. Biol. Med. 2006, 142, 591–593.
- 45 Millet, J., Jouault, S. C., Mauray, S., Theveniaux, J. et al., Antithrombotic and anticoagulant activities of a low molecular weight fucoidan by the subcutaneous route. Thromb. Haemost. 1999, 81, 391–395.
- 46 Nishino, T., Yamauchi, T., Horie, M., Nagumo, T. et al., Effects of a fucoidan on the activation of plasminogen by u-PA and t-PA. Thromb. Res. 2000, 99, 623–634.
10.1016/S0049-3848(00)00289-9 Google Scholar
- 47 Soeda, S., Ohmagari, Y., Shimeno, H., Nagamatsu, A., Preparation of aminated fucoidan and its evaluation as an antithrombotic and antilipemic agent. Biol. Pharm. Bull. 1994, 17, 784–788.
- 48 Boisson-Vidal, C., Chaubet, F., Chevolot, L., Sinquin, C. et al., Relationship between antithrombotic activities of fucans and their structure. Drug Dev. Res. 2000, 51, 216–224.
- 49 Grauffel, V., Kloareg, B., Mabeau, S., Durand, P. et al., New natural polysaccharides with potent antithrombic activity: Fucans from brown algae. Biomaterials 1989, 10, 363–368.
- 50 Nishino, T., Aizu, Y., Nagumo, T., The influence of sulfate content and molecular weight of a fucan sulfate from the brown seaweed Ecklonia kurome on its antithrombin activity. Thromb. Res. 1991, 64, 723–731.
- 51 Springer, G. F., Wurzel, H. A., McNeal, G. M. J., Ansell, N. J., Isolation of anticoagulant fractions from crude fucoidan. Proc. Soc. Biol. Med. 1957, 94, 404–409.
- 52 Kuitunen, A., Suojaranta-Ylinen, R., Raivio, P., Kukkonen, S. et al., Heparin-induced thrombocytopenia following cardiac surgery is associated with poor outcome. J. Cardiothorac. Vasc. Anesth. 2007, 21, 18–22.
- 53 Mattioli, A. V., Heparin-induced thrombocytopenia: Implictions for cardiologist. G. Ital. Cardiol. (Rome) 2006, 7, 675–683.
- 54 Moore, B. R., Hinchcliff, K. W., Heparin: A review of its pharmacology and therapeutic use in horses. J. Vet. Intern. Med. 1994, 8, 26–35.
- 55 Scott, J. R., Klein, M. B., Gernsheimer, T., Honari, S. et al., Arterial and venous complications of heparin-induced thrombocytopenia in burn patients. J. Burn Care Res. 2007, 28, 71–75.
- 56 Ben-Zaken, O., Tzaban, S., Tal, Y., Horonchik, L. et al., Cellular heparan sulfate participates in the metabolism of prions. J. Biol. Chem. 2003, 278, 40041–40049.
- 57 Starke, R., Mackie, I., Drummond, O., MacGregor, I. et al., Prion protein in patients with renal failure. Transfus. Med. 2006, 16, 165–168.
- 58 Zsila, F., Gedeon, G., Binding of anti-prion agents to glycosaminoglycans: Evidence from electronic absorption and circular dichroism spectroscopy. Biochem. Biophys. Res. Commun. 2006, 346, 1267–1274.
- 59 Doctor, V. M., Hill, C., Jackson, G. J., Effect of fucoidan during activation of human plasminogen. Thromb. Res. 1995, 79, 237–247.
- 60 Drozd, N. N., Tolstenkov, A. S., Migal, I., Kijutina, M. et al., Pharmacodynamic parameters of anticoagulants on a basis of sulfated polysaccharides from seaweed. Bull. Exp. Biol. Med. 2006 537–540.
- 61 Kuznetsova, T. A., Besednova, N. N., Mamaev, A. N., Momot, A. P. et al., Anticoagulant activity of fucoidan from brown seaweed of Okhotsk Sea Fucus evanescens. Bull. Exp. Biol. Med. 2003, 136, 532–534.
- 62 Nezgovorov, D. V., Dobrodeeva, L. K., Mokrousova, E. V., Menshikova, E. A., Influence of fucoidan on cells of peritoneal exudates at intraperitoneal introduction to outbred white mice. Med. Immunol. 2004, 3-5, 242–243.
- 63 Mytar, B., Gawlicka, M., Szatanek, R., Woloszyn, M. et al., Induction of intracellular cytokine production in human monocytes/macrophages stimulated with ligands of pattern recognition receptors. Inflamm. Res. 2004, 53, 100–106.
- 64 Shibata, H., Kimura-Takagi, I., Nagaoka, M., Hashimoto, S. et al., Properties of fucoidan from Cladosiphon okamuranus tokida in gastric mucosal protection. Biofactors 2000, 11, 235–245.
- 65 Zaporozhets, T. S., Ivanushko, L. A., Zvyagintseva, T. A., Molchanova, V. I. et al., Cytokine inducing activity of biopolymers from sea hydrobionts. Med. Immunol. 2004, 6, 89–96.
- 66 Blondin, C., Fischer, E., Boisson-Vidal, C., Kazatchkine, M. D. et al., Inhibition of complement activation by natural sulfated polysaccharides (fucans) from brown seaweed. Mol. Immunol. 1994, 31, 247–253.
- 67 Zvyagintseva, T. N., Shevchenko, N. M., Nazarova, I. V., Scobun, A. S. et al., Inhibition of complement activation by water-soluble polysaccharides of some far-eastern brown seaweeds. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2000, 126, 209–215.
- 68 Makarenkova, I. D., Zaporozhets, T. S., Besednova, N. N., Elyakova, L. A. et al., Feasibility of decreasing the adhesive activity of Corynebacterium diphtheriae by biopolymers of natural origin. Antibiot. Khimioter. 1999, 44, 11–14.
- 69 Makarenkova, I. D., Kompanets, G. G., Zaporozhets, T. S., Inhibition of adhesion of the pathogenic microorganism to the eucaryotic cells. J. Microbiol. 2006 121–125.
- 70 Okai, Y., Higashi-Okai, K., Ishizaka, S., Yamashita, U., Enhancing effect of polysaccharides from an edible brown alga Hijikia fusiforme (Hijiki), on release of tumor necrosis factor-α from macrophages of endotoxin-nonresponder C3H/HeJ mice., Nutr. Cancer 1997, 27, 74–79.
- 71 Vischer, P., Buddecke, E., Different action of heparin and fucoidan on arterial smooth muscle cell proliferation and thrombospondin and fibronectin metabolism. Eur. J. Cell. Biol. 1991, 56, 407–414.
- 72 Aisa, Y., Miyakawa, Y., Nakazato, T., Shibata, H. et al., Fucoidan induces apoptosis of human HS-sultan cells accompanied by activation of caspase-3 and down-regulation of ERK pathways. Am. J. Hematol. 2005, 78, 7–14.
- 73 Bakunina, I., Nedashkovskaia, O. I., Alekseeva, S. A., Ivanova, E. P. et al., Degradation of fucoidan by the marine proteobacterium Pseudoalteromonas citrea. Mikrobiologiia 2002, 71, 49–55.
- 74 Bakunina, I., Shevchenko, L. S., Nedashkovskaia, O. I., Shevchenko, N. M. et al., Screening of marine bacteria for fucoidan hydrolases. Mikrobiologiia 2000, 69, 370–376.
- 75 Ivanova, E. P., Bakunina, I. Y., Nedashkovskaya, O. I., Gorshkova, N. M. et al., Ecophysiological variabilities in ectohydrolytic enzyme activities of some Pseudoalteromonas sp., P. citrea, P. issachenkonii, and P. nigrifaciens. Curr. Microbiol. 2003, 46, 6–10.
- 76 Morigana, T., Araki, T., Ito, M., Kitamikado, M., A search for fucoidan-degrading bacteria in coastal sea environments of Japan. Bull. Jpn. Soc. Sci. Fish 1981, 47, 621–625.
- 77 Burtseva, Y. V., Kusajkin, M. I., Sova, V. V., Shevchenko, N. M. et al., The distribution of fucoidanases and some glycosidases in marine invertebrates. Biologia Morya 2000, 26, 429–432.
- 78 Daniel, R., Berteau, O., Jozefonvicz, J., Goasdoue, N., Degradation of algal (Ascophyllum nodosum) fucoidan by an enzymatic activity contained in digestive glands of the marine mollusc Pecten maximus. Carbohydr. Res. 1999, 322, 291–297.
- 79 Kusaykin, M. I., Burtseva, Y. V., Svetasheva, T. G., Sova, V. V. et al., Distribution of O-glycosylhydrolases in marine invertebrates. Enzymes of the marine mollusk Littorina kurila that catalyze fucoidan transformation. Biochemistry (Mosc) 2003, 68, 317–324.
- 80 Furukawa, S., Fujikawa, T., Koga, D., Ide, A., Purification and some properties of exo-type fucoidanases from Vibrio sp. N-5. Biosci. Biotechnol. Biochem. 1992, 56, 1829–1834.
- 81 Kitamura, K., Matsuo, M., Yasui, T., Enzymatic degradation of fucoidan by fucoidanase from the hepatopancreas of Patinopecten yessoensis. Biosci. Biotechnol. Biochem. 1992, 56, 490–494.
- 82 Thanassi, N. M., Nakada, H. I., Enzymatic dagradation of fucoidan by enzymes from the hepatopancreas of abalone Haliotis species. Arch. Biochem. Biophys. 1967, 118, 172–177.
- 83 Daniel, R., Berteau, O., Chevolot, L., Varenne, A. et al., Regioselective desulfation of sulfated L- fucopyranoside by a new sulfoesterase from the marine mollusk Pecten maximus: Application to the structural study of algal fucoidan (Ascophyllum nodosum). Eur. J. Biochem. 2001, 268, 5617–5626.
- 84 Sakai, T., Amarume, H., Kawai, T., Kojima, K. et al., Sulfated fucan oligosaccharide. USA Patent 6720419, 2004.
- 85 Sakai, T., Ishizuka, K., Shimanaka, K., Ikai, K. et al., Structures of oligosaccharides derived from Cladosiphon okamuranus fucoidan by digestion with marine bacterial enzymes. Mar. Biotechnol. 2003, 5, 536–544.
- 86 Barbeyron, T., L'Haridon, S., Michel, G., Czjzek, M., Description of Mariniflexile fucanivorans sp. Nov., a marine Flavobacteriaceae that degrades sulphated fucans from brown algae. Int. J. Syst. Evol. Microbiol. 2008, in press.
- 87 Sakai, T., Ishizuka, K., Kato, I., Isolation and characterization of a fucoidan-degrading marine bacterium. Mar. Biotechnol. 2003, 5, 409–416.
- 88 Takayama, M., Koyama, N., Sakai, T., Kato, I., Enzymes capable of degrading a sulfated fucose-containing polysaccharide and their encoding genes. USA Patent 6489155, 2002.
- 89 Sakai, T., Kimura, H., Kato, I., A marine strain of Flavobacteriaceae utilizes brown seaweed fucoidan. Mar. Biotechnol. 2002, 4, 399–405.
- 90 Sakai, T., Kimura, H., Kato, I., Purification of sulfated fucoglucuronomannan lyase from bacterial strain of Fucobacter marina and study of appropriate conditions for its enzyme digestion. Mar. Biotechnol. 2003, 5, 380–387.
- 91 Sakai, T., Kimura, H., Kojima, K., Shimanaka, K. et al., Marine bacterial sulfated fucoglucuronomannan (SFGM) lyase digests brown algal SFGM into trisaccharides. Mar. Biotechnol. 2003, 5, 70–78.
- 92 Davies, G., Henrissat, B., Structures and mechanisms of glycosyl hydrolases. Structure 1995, 3, 853–859.
- 93 Sinnott, M. L., Catalytic mechanisms of enzymic glycosyl transfer. Chem. Rev. 1990, 90, 1171–1202.
- 94 Hallmann, A., Sumper, M., An inducible arylsulfatase of Volvox carteri with properties suitable for a reporter-gene system. Purification, characterization and molecular cloning. Eur. J. Biochem. 1994, 221, 143–150.
- 95 Parenti, G., Meroni, G., Ballabio, A., The sulfatase gene family. Curr. Opin. Genet. Dev. 1997, 7, 386–391.
- 96 Tanaka, K., Kubushiro, K., Iwamori, Y., Okairi, Y. et al., Estrogen sulfotransferase and sulfatase: Roles in the regulation of estrogen activity in human uterine endometrial carcinomas. Cancer Sci. 2003, 94, 871–876.
- 97 Yang, Q., Angerer, L. M., Angerer, R. C., Structure and tissue-specific developmental expression of a sea urchin arylsulfatase gene. Dev. Biol. 1989, 135, 53–65.
- 98 Takahashi, N., Egami, F., Hydrolysis of polysaccharide sulphate esters by a sulphatase preparation from Charonia lampas. Biochem. J. 1961, 80, 384–386.
- 99 Lloyd, P. F., Lloyd, K. O., Sulphatases and sulphated polysaccharides in the viscera of marine molluscs. Nature 1963, 199, 287.
- 100 Sasaki, K., Sakai, T., Kojima, K., Nakayama, S. et al., Partial purification and characterization of an enzyme releasing 2-sulfo-α-L-fucopyranose from 2-sulfo-α-L-fucopyranosyl-(1,2) pyridylaminated fucose from a sea urchin, Strongylocentrotus nudus., Biosci. Biotechnol. Biochem. 1996, 60, 666–668.
- 101 Kusaykin, M., Pesentseva, M., Silschenko, A., Avilov, S. et al., Aryl sulfatase of unusual specificity from the liver of marine mollusk Littorina kurila. Russian J. Bioorg. Chem. 2006, 32, 63–70.
10.1134/S1068162006010067 Google Scholar
- 102 Yoon, S.-J., Pyun, Y.-R., Hwang, J.-K., Mourão, P. A. S., A sulfated fucan from the brown alga Laminaria cichorioides has mainly heparin cofactor II-dependent anticoagulant activity. Carbohydr. Res. 2007, 342, 2326–2330.
Citing Literature
