Sulfated polysaccharides of brown algae (“fucoidans”) constitute a wide variety of biopolymers from simple sulfated fucans up to complex heteropolysaccharides composed of several neutral monosaccharides, uronic acid and sulfate. The increased interest in this class of polysaccharides is explained by their high and versatile biological activities, and hence, by their possible use in new drug design. Structural analysis of several fucoidans demonstrates that their biological properties are determined not only by charge density, but also by fine chemical structure, although distinct correlations between structure and biological activity cannot be formulated at present. The aim of this review is to describe the methods of structural analysis currently used in fucoidan chemistry, and to discuss some new information on the structures of fucoidans presented in recent publications.
PainterTJ. (1983) Algal polysaccharides. In The Polysaccharides. Vol. 2, AspinallGO (Ed). Academic Press, London, UK, 195–285.
2.
MulloyB, RibeiroAC, AlvesAP, VieiraRP, MouraoPAS. (1994) Sulfated fucans from echinoderms have a regular tetrasaccharide repeating unit defined by specific patterns of sulfation at the O-2 and O-4 positions. Journal of Biological Chemistry, 269, 22113–22123.
3.
NagumoT, NishinoT. (1996) Fucan sulfates and their anticoagulant activities. In Polysaccharides in Medicinal Applications.DumitriuS (Ed). Marcel Dekker, New York, 545–574.
4.
MouraoPAS. (2004) Use of sulfated fucans as anticoagulant and antithrombotic agents: future perspectives. Current Pharmaceutical Design, 10, 967–981.
5.
BerteauO, MulloyB. (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.
6.
DischeZ, ShettlesLB. (1948) A specific colour reaction of methylpentoses and a spectrophotometric micromethod for their determination. Journal of Biological Chemistry, 175, 595–603.
7.
LarsenB. (1978) Fucoidan. In Handbook of Phycological Methods. Physiological and Biochemical Methods.HellebustJA, CraigieJS (Eds). Cambridge University Press, Cambridge, UK, 151–156.
8.
UsovAI, SmirnovaGP, KlochkovaNG. (2001) Polysaccharides of algae. 55. Polysaccharide composition of some brown algae from Kamchatka. Bioorganicheskaya Khimiya, 27, 444–448 [Russian Journal of Bioorganic Chemistry, 27, 395–399, English translation].
9.
UsovAI, SmirnovaGP. (2003) A new procedure for determination of alginate and fucoidan in brown seaweeds. In Proceedings of the XVIIth International Seaweed Symposium, ChapmanARO, AndersonRJ, VreelandVJ, DavisonIR (Eds). Oxford University Press, Oxford, UK, 209–212.
10.
AdhikariU, MateuCG, ChattopadhyayK, PujolCA, DamonteEB, RayB. (2006) Structure and antiviral activity of sulfated fucans from Stoechospermum marginatum. Phytochemistry, 67, 2474–2482.
11.
HemmingsonJA, FalshawR, FurneauxRH, ThompsonK. (2006) Structure and antiviral activity of the galactofucan sulfates extracted from Undaria pinnatifida (Phaeophyta). Journal of Applied Phycology, 18, 185–193.
12.
YoonS-J, PyunY-R, HwangJ-K, MouraoPAS. (2007) A sulfated fucan from the brown alga Laminaria cichorioides has mainly heparin cofactor II-dependent anticoagulant activity. Carbohydrate Research, 342, 2326–2330.
13.
BilanMI, GrachevAA, UstuzhaninaNE, ShashkovAS, NifantievNE, UsovAI. (2002) Structure of a fucoidan from the brown seaweed Fucus evanescens C. Ag. Carbohydrate Research, 337, 719–730.
14.
PonceNMA, PujolCA, DamonteEB, FloresML, StortzCA. (2003) Fucoidans from the brown seaweed Adenocystis utricularis: extraction methods, antiviral activity and structural studies. Carbohydrate Research, 338, 153–165.
15.
SilvaTMA, AlvesLG, de QueirozKCS, SantosMGL, MarquesCT, ChavanteSF, RochaHAO, LeiteEL. (2005) Partial characterization and anticoagulant activity of a heterofucan from the brown seaweed Padina gymnospora. Brazilian Journal of Medical and Biological Research, 38, 523–533.
16.
RochaHAO, MoraesFA, TrindadeES, FrancoCRC, TorquatoRJS, VeigaSS, ValenteAP, MouraoPAS, LeiteEL, NaderHB, DietrichCP. (2005) Structural and hemostatic activities of a sulfated galactofucan from the brown alga Spatoglossum schroederi. An ideal antithrombotic agent? Journal of Biological Chemistry, 280, 41278–41288.
17.
WhyteJNC, SouthcottBA. (1970) An extraction procedure for plants: extracts from the red alga Rhodomela larix. Phytochemistry, 9, 1159–1161.
18.
MabeauS, KloaregB, JoseleauJ-P. (1990) Fractionation and analysis of fucans from brown algae. Phytochemistry, 29, 2441–2445.
19.
ChizhovAO, DellA, MorrisHR, HaslamSM, McDowellRA, ShashkovAS, NifantievNE, KhatuntsevaEA, UsovAI. (1999) A study of fucoidan from the brown seaweed Chorda filum. Carbohydrate Research, 320, 108–119.
20.
SlonekerJH. (1972) Gas-liquid chromatography of alditol acetates. In Methods in Carbohydrate Chemistry, Vol.6. WhistlerRL, BeMillerJN (Eds). Academic Press, New York, 20–24.
21.
LeonteinK, LindbergB, LonngrenJ. (1978) Assignment of absolute configuration of sugars by g.l.c. of their acetylated glycosides formed from chiral alcohols. Carbohydrate Research, 62, 359–362.
22.
GerwigGJ, KamerlingJP, VliegenthartJFG. (1978) Determination of D and L configuration of neutral monosaccharides by high-resolution capillary g.l.c. Carbohydrate Research, 62, 349–357.
23.
CasesMR, CerezoAS, StortzCA. (1995) Separation and quantitation of enantiomeric galactoses and their mono-O-methylethers as their diastereomeric acetylated 1-deoxy-1-(2-hydroxypropylamino)alditols. Carbohydrate Research, 269, 333–341.
24.
UsovAI, SmirnovaGP, BilanMI, ShashkovAS. (1998) Polysaccharides of algae. 53. Brown alga Laminaria saccharina (L.) Lam. as a source of fucoidan. Bioorganicheskaya Khimiya, 24, 437–445 [Russian Journal of Bioorganic Chemistry, 24, 382–389, English translation].
25.
BlumenkrantzN, Asboe-HansenG. (1973) New method for quantitative determination of uronic acids. Analytical Biochemistry, 54, 484–489.
26.
UsovAI, BilanMI, KlochkovaNG. (1995) Polysaccharides of algae. 48. Polysaccharide composition of several calcareous red algae: Isolation of alginate from Corallina pilulifera P. et R. (Rhodophyta, Corallinaceae). Botanica Marina, 38, 43–51.
27.
HestrinS. (1949) The reaction of acetylcholine and other carboxylic acid derivatives with hydroxylamine, and its analytical application. Journal of Biological Chemistry, 180, 249–261.
28.
DodgsonKS, PriceRG. (1962) A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochemical Journal, 84, 106–110.
29.
AndersonNS, DolanTCS, PenmanA, ReesDA, MuellerGP, StancioffDJ, StanleyNF. (1968) Carrageenans. Part IV. Variations in the structure and gel properties of κ-carrageenan, and the characterisation of sulphate esters by infrared spectroscopy. Journal of the Chemical Society, C, 602–606.
30.
RochasC, LahayeM, YapheW. (1986) Sulfate content of carrageenan and agar determined by infrared spectroscopy. Botanica Marina, 29, 335–340.
31.
PereiraMS, MulloyB, MouraoPAS. (1999) Structure and activity of sulphated fucans: comparison between the regular, repetitive and linear fucans from echinoderms with the more heterogeneous and branched polymers from brown algae. Journal of Biological Chemistry, 274, 7656–7667.
32.
BilanMI, GrachevAA, UstuzhaninaNE, ShashkovAS, NifantievNE, UsovAI. (2004) A highly regular fraction of a fucoidan from the brown seaweed Fucus distichus L. Carbohydrate Research, 339, 511–517.
33.
TakanoR. (2002) Desulfation of sulfated carbohydrates. Trends in Glycoscience and Glycotechnology, 14, 343–351.
34.
KantorTG, SchubertM. (1957) A method for the desulfation of chondroitin sulfate. Journal of the American Chemical Society, 79, 152–153.
NagasawaK, InoueY, KamataK. (1977) Solvolytic desulfation of glycosaminoglycuronan sulfates with dimethyl sulfoxide containing water or methanol. Carbohydrate Research, 58, 47–55.
KolenderAA, MatulewiczMC. (2004) Desulfation of sulfated galactans with chlorotrimethylsilane. Characterization of β-carrageenan by 1H NMR spectroscopy. Carbohydrate Research, 339, 1619–1629.
40.
PominVH, PereiraMS, ValenteA-P, TollefsenDM, PavaoMSG, MouraoPAS. (2005) Selective cleavage and anticoagulant activity of a sulfated fucan: stereospecific removal of a 2-sulfate ester from the polysaccharide by mild acid hydrolysis, preparation of oligosaccharides, and heparin cofactor II-dependent anticoagulant activity. Glycobiology, 15, 369–381.
41.
PominVH, ValenteAP, PereiraMS, MouraoPAS. (2005) Mild acid hydrolysis of sulfated fucans: a selective 2-desulfation reaction and an alternative approach for prearing tailored sulfated oligosaccharides. Glycobiology, 15, 1376–1385.
42.
SaillardS, GareilP, JozefonviczJ, DanielR. (1999) Development of a capillary electrophoresis assay based on free sulfate determination for the direct monitoring of sulfoesterase activity. Analytical Biochemistry, 275, 11–21.
43.
DanielR, BerteauO, ChevolotL, VarenneA, GareilP, GoasdoueN. (2001) Regioselective desulfation of sulfated L-fucopyranoside by a new sulfoesterase from the marine mollusk Pecten maximus. European Journal of Biochemistry, 268, 561–5626.
44.
KusaykinMI, BurtsevaYV, SvetashevaTG, SovaVV, ZvyagintsevaTN. (2003) Distribution of O-glycosylhydrolases in marine invertebrates. Enzymes of marine mollusk Littorina kurila that catalyze fucoidan transformation. Biokhimiya, 68, 384–392 [Biochemistry (Moscow), 68, 317–324, English translation].
45.
CiucanuI, KerekF. (1984) A simple and rapid method for the permethylation of carbohydrates. Carbohydrate Research, 131, 209–217.
46.
MillerIJ, BluntJW. (2002) Mobility of sulfate ester during structural determinations of red algal galactans. Botanica Marina, 45, 559–565.
47.
BjorndalH, HellerqvistCG, LindbergB, SvenssonS. (1970) Gas-liquid chromatography and mass spectrometry in methylation analysis of polysaccharides. Angewandte Chemie, International Edition English, 9, 610–619.
48.
BilanMI, ZakharovaAN, GrachevAA, ShashkovAS, NifantievNE, UsovAI. (2007) Polysaccharides of algae. 60. Fucoidan from the Pacific brown alga Analipus japonicus (Harv.) Winne (Ectocarpales, Scytosiphonaceae). Bioorganicheskaya Khimiya, 33, 44–53 [Russian Journal of Bioorganic Chemistry, 33, 38–46, English translation].
49.
TissotB, SalpinJ-Y, MartinezM, GaigeotM-P, DanielR. (2006) Differentiation of the fucoidan sulfated L-fucose isomers constituents by CE-ESIMS and molecular modeling. Carbohydrate Research, 341, 598–609.
50.
ChevolotL, FoucaultA, Colliec-JouaultS, RatiskolJ, SinquinC. (2000) Improvement purification of sulfated oligofucan by ion-exchange displacement centrifugal partition chromatography. Journal of Chromatography A, 869, 353–361.
51.
DanielR, ChevolotL, CarrascalM, TissotB, MouraoPAS, AbianJ. (2007) Electrospray ionization mass spectrometry of oligosaccharides derived from fucoidan of Ascophyllum nodosum. Carbohydrate Research, 342, 826–834.
52.
ColliecS, Boisson-VidalC, JozefonviczJ. (1994) A low molecular weight fucoidan fraction from the brown seaweed Pelvetia canaliculata. Phytochemistry, 35, 697–700.
53.
ChevolotL., FoucaultA., ChaubetF, KervarecN, SinquinC, FisherA-M, Boisson-VidalC. (1999) Further data on the structure of brown seaweed fucans: relationships with anticoagulant activity. Carbohydrate Research, 319, 154–165.
54.
NardellaA, ChaubetF, Boisson-VidalC, BlondinC, DurandP, JosefonviczJ. (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. Carbohydrate Research, 289, 201–208.
55.
ChandiaNP, MatsuhiroB. (2008) Characterization of a fucoidan from Lessonia vadosa (Phaeophyta) and its anticoagulant and elicitor properties. International Journal of Biological Macromolecules, 42, 235–240
56.
KusaykinMI, ChizhovAO, AlekseevaSA, BakuninaIY, NedashkovskayaOI, SovaVV, ZvyagintsevaTN, ElyakovGB. (2004) A comparative study of the specificity of fucoidanases of marine microorganisms and invertebrates. Doklady Akademii Nauk, 396, 691–693 [Doklady Biochemistry and Biophysics, 396, 187–189, English translation].
57.
BerteauO, McCortI, GoasdoueN, TissotB, DanielR. (2002) Characterization of a new α-L-fucosidase isolated from the marine mollusk Pecten maximus that catalyzes the hydrolysis of α-L-fucose from algal fucoidan (Ascophyllum nodosum). Glycobiology, 12, 273–282.
58.
DanielR, BerteauO, JozefonviczJ, GoasdoueN. (1999) Degradation of algal (Ascophyllum nodosum) fucoidan by an enzymatic activity contained in digestive glands of the marine mollusk Pecten maximus. Carbohydrate Research, 322, 291–297.
59.
ZvyagintsevaTN, ShevchenkoNM, ChizhovAO, KrupnovaTN, SundukovaEV, IsakovVV. (2003) Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions. Journal of Experimental Marine Biology and Ecology, 294, 1–13.
60.
BilanMI, KusaykinMI, GrachevAA, TsvetkovaEA, ZvyagintsevaTN, NifantievNE, UsovAI. (2005) Effect of enzyme preparation from the marine mollusk Littorina kurila on fucoidan from the brown alga Fucus distichus. Biokhimiya, 70, 1606–1612 [Biochemistry (Moscow), 70, 1321–1326, English translation].
61.
BakuninaIY, NedashkovskayaOI, AlekseevaSA, IvanovaEP, RomanenkoLA, GorshkovaNM, IsakovVV, ZvyagintsevaTN, MikhailovVV. (2002) Degradation of fucoidan by the marine proteobacterium Pseudoalteromonas citrea. Mikrobiologiya, 71, 49–55 [Microbiology, 71, 41–47, English translation].
62.
DescampsV, ColinS, LahayeM, JamM, RichardC, PotinP, BarbeyronT, YvinJ-C, KloaregB. (2006) Isolation and culture of a marine bacterium degrading the sulfated fucans from marine brown algae. Marine Biotechnology, 8, 27–39.
63.
ColinS, DeniaudE, JamM, DescampsV, ChevolotY, KervarecN, YvinJ-C, BarbeyronT, MichelG, KloaregB. (2006) Cloning and biochemical characterization of the fucanase FcnA: definition of a novel glycoside hydrolase family specific for sulfated fucans. Glycobiology, 16, 1021–1032.
64.
SakaiT, IshizukaK, KatoI. (2003) Isolation and characterization of a fucoidan-degrading marine bacterium. Marine Biotechnology, 5, 409–416.
65.
SakaiT, IshizukaK, ShimanakaK, IkaiK, KatoI. (2003) Structures of oligosaccharides derived from Cladosiphon okamuranus fucoidan by digestion with marine bacterial enzymes. Marine Biotechnology, 5, 536–544.
66.
SakaiT, KimuraH, KatoI. (2003) Purification of sulfated fucoglucuronomannan lyase from bacterial strain of Fucobacter marina and study of appropriate conditions for its enzyme digestion. Marine Biotechnology, 5, 380–387.
ChandiaNP, MatsuhiroB, OrtizJS, MansillaA. (2005) Carbohydrates from the sequential extraction of Lessonia vadosa (Phaeophyta). Journal of the Chilean Chemical Society, 50, 501–504.
69.
NagaokaM, ShibataH, Kimura-TakagiI, HashimotoS, KimuraK, MakinoT, AiyamaR, UeyamaS, YokokuraT. (1999) Structural study of fucoidan from Cladosiphon okamuranus Tokida. Glycoconjugate Journal, 16, 19–26.
70.
TakoM, YozaE, TohmaS. (2000) Chemical characterization of acetyl fucoidan and alginate from commercially cultured Cladosiphon okamuranus. Botanica Marina, 43, 393–398.
71.
MaraisM-F, JoseleauJ-P. (2001) A fucoidan fraction from Ascophyllum nodosum. Carbohydrate Research, 336, 155–159.
72.
ChevolotL, MulloyB, RatiskolJ, FoucaultA, Colliec-JouaultS. (2001) A disaccharide repeat unit is the major structure in fucoidans from two species of brown algae. Carbohydrate Research, 330, 529–535.
73.
PatankarMS, OehningerS, BarnettT, WilliamsRL, ClarkGF. (1993) A revised structure for fucoidan may explain some of its biological activities. Journal of Biological Chemistry, 268, 21770–21776.
74.
BilanMI, GrachevAA, ShashkovAS, NifantievNE, UsovAI. (2006) Structure of a fucoidan from the brown seaweed Fucus serratus L. Carbohydrate Research, 341, 238–245.
75.
UsovAI, SmirnovaGP, KlochkovaNG. (2005) Polysaccharides of algae. 58. The polysaccharide composition of the Pacific brown alga Alaria fistulosa P. et R. (Alariaceae, Laminariales). Izvestiya Akademii Nauk. Seriya Khimicheskaya, 1245–1249 [Russian Chemical Bulletin, International Edition, 54, 1282–1286, English translation].
76.
LeeJ-B, HayashiK, HashimotoM, NakanoT, HayashiT. (2004) Novel antiviral fucoidan from sporophyll of Undaria pinnatifida (Mekabu). Chemical and Pharmacological Bulletin, 52, 1091–1094.
77.
XueC-H, FangY, LinH, ChenL, LiZ-J, DengD, LuC-X. (2001) Chemical characters and antioxidative properties of sulfated polysaccharides from Laminaria japonica. Journal of Applied Phycology, 13, 67–70.
78.
ShevchenkoNM, AnastyukSD, GerasimenkoNI, DmitrenokPS, IsakovVV, ZvyagintsevaTN. (2007) Polysaccharide and lipid composition of the brown seaweed Laminaria gurjanovae. Bioorganicheskaya Khimiya, 33, 96–107 [Russian Journal of Bioorganic Chemistry, 33, 88–98, English translation].
79.
ZhuW, OoiVEC, ChanPKS, AngPOJr. (2003) Isolation and charactarization of a sulfated polysaccharide from the brown alga Sargassum patens and determination of its anti-herpes activity. Biochemistry and Cell Biology, 81, 25–33.
80.
DuarteMER, CardosoMA, NosedaMD, CerezoAS. (2001) Structural studies on fucoidans from the brown seaweed Sargassum stenophyllum. Carbohydrate Research, 333, 281–293.
81.
NishinoT, TakabeY, NagumoT. (1994) Isolation and partial characterization of a novel β-D-galactan sulfate from the brown seaweed Laminaria angustata var. longissima. Carbohydrate Polymers, 23, 165–173.
82.
NishinoT, NagumoT, KiyoharaH, YamadaH. (1991) Structural characterization of a new anticoagulant fucan sulfate from the brown seaweed Ecklonia kurome. Carbohydrate Research, 211, 77–90.
83.
AlbuquerqueIRL, QueirozKCS, AlvesLG, SantosEA, LeiteEL, RochaHAO. (2004) Heterofucans from Dictyota menstrualis have anticoagulant activity. Brazilian Journal of Medical and Biological Research, 37, 167–171.
84.
LeiteEL, MedeirosMGL, RochaHAO, FariasGGM, da SilvaLF, ChavanteSF, de AbreuLD, DietrichCP, NaderHB. (1998) Structure and pharmacological activities of a sulfated xylofucoglucuronan from the alga Spatoglossum schroederi. Plant Science, 132, 215–228.
85.
LiB, WeiX-J, SunJ-L, XuS-Y. (2006) Structural investigation of a fucoidan containing a fucose-free core from the brown seaweed, Hizikia fusiforme. Carbohydrate Research, 341, 1135–1146.
86.
MulloyB, MouraoPAS, GrayE. (2000) Structure/function studies of anticoagulant sulphated polysaccharides using NMR. Journal of Biotechnology, 77, 123–135.
87.
MulloyB. (2005) The specificity of interactions between proteins and sulfated polysaccharides. Annals of the Brazilian Academy of Sciences, 77, 651–664.
88.
PereiraMS, MeloFR, MouraoPAS. (2002) Is there a correlation between structure and anticoagulant action of sulfated galactans and sulfated fucans?Glycobiology, 12, 573–580.
89.
QuiX, AmarasekaraA, DoctorV. (2006) Effect of oversulfation on the chemical and biological properties of fucoidan. Carbohydrate Polymers, 63, 224–228.
90.
BeckerDJ, LoweJB. (2003) Fucose: biosynthesis and biological function in mammals. Glycobiology, 13, 41R–53R.
91.
CumashiA, UshakovaNA, PreobrazhenskayaME, D'Incecco, PiccoliA, TotaniL, TinariN, MorozevichGE, BermanAE, BilanMI, UsovAI, UstyuzhaninaNE, GrachevAA, SandersonCJ, KellyM, RabinovichGA, IacobelliS, NifantievNE. (2007) A comparative study of the antiinflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology, 17, 541–552.
92.
OzawaT, YamamotoJ, YamagushiT, YamazakiN, NishizawaM. (2006) Two fucoidans in the holdfast of cultivated Laminaria japonica. Journal of Natural Medicine, 60, 236–239.
93.
HonyaM, MoriH, AnzaiM, ArakiY, NisizawaK. (1999) Monthly changes in the content of fucans, their constituent sugars and sulphate in cultured Laminaria japonica. Hydrobiologia, 398/399, 411–416.
94.
PreeprameS, HayashiK, LeeJ-B, SankawaU, HayashiT. (2001) A novel antivirally active fucan sulfate derived from an edible brown alga, Sargassum horneri. Chemical and Pharmacological Bulletin, 49, 484–485.
