Structures, Functions, and Biological Properties of Sulfated Fucans and An

Glycobiology vol. 13 no. 6 pp. 29R±40R, 2003 DOI: 10.1093/glycob/cwg058 REVIEW Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide Downloaded from https://academic.oup.com/glycob/article/13/6/29R/572950 by guest on 02 October 2021 Olivier Berteau2 and Barbara Mulloy1,3 egg jelly coat of sea urchins (Mulloy et al., 1994) and in the body wall of sea cucumber (Mourao~ and Bastos, 1987). 2Department of Chemistry, Swedish University of Agricultural Sciences, Arrheniusplan 8, P.O. Box 7015, SE-750 07 Uppsala, Sweden; and The fucans of brown algae, often called fucoidans, have 3National Institute for Biological Standards and Control, been known for some time to act as modulators of coagula- Blanche Lane, South Mimms, Potters Bar, Hertfordshire ENG 3QG, tion, as have other algal polysaccharides (Chargaff et al., United Kingdom 1936). Fucoidan preparations have been proposed as alter- Accepted on February 12, 2003 natives to the anticoagulant heparin, which is prepared from mammalian mucosa; being of vegetable origin they Sulfated fucans, frequently referred to simply as fucans, are less likely to contain infectious agents, such as viruses or constitute a class of polysaccharides first isolated in 1913. prions. Like heparin, it has been shown that fucoidans For many years fucans were regarded only as a potential affect many biological activities, such as inflammation, source of L-fucose, although their anticoagulant activity was cell proliferation and adhesion, viral infection, and fertiliza- known. Even as the potent effects of fucans on physiological tion (Boisson-Vidal et al., 1995). systems have become better characterized, structural studies However, relatively few studies have interpreted the bio- have lagged behind. Recently the search for new drugs has logical activity of fucoidans in terms of molecular structure. raised increased interest in sulfated fucans. In the past few Almost all biological studies use a commercially available, years, several structures of algal and invertebrate fucans have crude preparation of sulfated polysaccharides from Fucus been solved, and many aspects of their biological activity have vesiculosus rather than a purified fucoidan (Mulloy et al., been elucidated. From this work emerges a more interesting 1994). Recent insights into the structures of fucans from picture of this class of polysaccharides than was previously different plant and animal species may help explain their suspected. The availability of purified fucans and fucan frac- mode of activity, whether as research reagents or as poten- tions with simple, but varied structures, in conjunction with tial therapeutics. the development of new enzymatic tools, demonstrate that the The aim of this review is to give an up-to-date view of the biological properties of sulfated fucans are not only a simple physiological and structural properties of sulfated fucans function of their charge density but also are determined by from marine algae and invertebrates and to present a dis- detailed structural features. cussion of specific hydrolytic enzymes, which are expected to simplify structural and structure/function studies. Key words: fucan/fucoidan/fucoidin/sulfated fucan/ Algal fucoidans are present in several orders, mainly fucoidanase Fucales and Laminariales but also in Chordariales, Dictyo- tales, Dictyosiphonales, Ectocarpales, and Scytosiphonales (Table I). In fact they are widely present among all the Introduction brown algae (Phaeophyceae) so far investigated. On the other hand, fucoidans seem to be absent from green The first isolation of ``fucoidin'' from marine brown algae algae (Chlorophyceae), red algae (Rhodophyceae), and was reported 90 years ago (Killing, 1913). Thirty-five years golden algae (Xanthophyceae) and from freshwater algae later, evidence was published showing that fucans also and terrestrial plants. occur in marine invertebrates (Vasseur, 1948). These poly- The only other sources of sulfated fucan known to date saccharides, mainly constituted of sulfated L-fucose, are are marine invertebrates. The first report was made by easily extracted from the cell wall of brown algae (i.e., Vasseur (1948), who extracted a polysaccharide mainly con- Phaeophyceae) with hot water (Percival and Ross, 1950) stituted of sulfated methyl-pentose from eggs of sea urchin. or acid solution (Black, 1954) and can account for more Since then, sulfated fucans have been isolated from the egg than 40% of the dry weight of isolated cell walls (Kloareg, jelly coat of many species of sea urchin (Mulloy et al., 1994; 1984). In marine invertebrates, sulfated fucans occur in the Alves et al., 1997, 1998; Vilela-Silva et al., 1999, 2002) and from the body wall of another type of marine echinoderm, the sea cucumber Ludwigothurea grisea (Mourao~ and Bastos, 1To whom correspondence should be addressed; e-mail: 1987; Ribeiro et al., 1994). To date, naturally occurring [email protected] fucans without sulfate groups have never been reported. Glycobiology vol. 13 no. 6 # Oxford University Press 2003; all rights reserved. 29R O. Berteau and B. Mulloy Table I. Brown algae containing fucoidan Species Order Reference Cladosiphon okamuranus Chordariales Nagaoka et al., 1999 Chordaria flagelliformis, Ch. gracilis Chordariales Usov et al., 2001 Saundersella simplex Chordariales Usov et al., 2001 Desmarestia intermedia Desmarestiales Usov et al., 2001 Dictyosiphon foeniculaceus Dictyosiphonales Usov et al., 2001 Dictyota dichotoma Dictyotales Abdel-Fattah et al., 1978 Padina pavonica Dictyotales Mian and Percival, 1973 Spatoglossum schroederi Dictyotales Leite et al., 1998 Adenocystis utricularis Ectocarpales Ponce et al., 2003 Downloaded from https://academic.oup.com/glycob/article/13/6/29R/572950 by guest on 02 October 2021 Pylayella littoralis Ectocarpales Usov et al., 2001 Ascophyllum nodosum Fucales Killing, 1913 Bifurcaria bifurcata Fucales Mian and Percival, 1973 Fucus.vesiculosus, F. spiralis, F. serratus, F. evanescens Fucales Killing, 1913; Black, 1954; Usov et al. 2001 Himanthalia lorea Fucales Mian and Percival, 1973 Hizikia fusiforme Fucales Dobashi et al., 1989 Pelvetia canaliculata, P. wrightii Fucales Anno, 1966; Mabeau et al., 1990 Sargassum stenophyllum, S. horneri, S. Kjellmanium, Fucales Yamamoto et al., 1984; Mabeau et al., 1990; S. muticum Duarte et al., 2001; Preeprame et al., 2001 Alaria fistulosa, A. marginata Laminariales Usov et al., 2001 Arthrothamnus bifidus Laminariales Usov et al., 2001 Chorda filum Laminariales Chizhov et al., 1999 Ecklonia kurome, E. cava Laminariales Nishino et al., 1991; Tanaka and Sorai, 1970 Eisenia bicyclis Laminariales Usui et al., 1980 Laminaria angustata, L. brasiliensis, L. cloustoni, L. digitata, Laminariales Killing, 1913; Black, 1954; de Reviers et al., 1983; L. japonica, L. religiosa, L. saccharina Maruyama et al., 1987; Rozkin et al., 1989; Kitamura et al., 1991; Pereira et al., 1999 Macrocystis integrifolia, M. pyrifera Laminariales Wort, 1954; Schweiger, 1962 Nereocystis luetkeana Laminariales Wort, 1954 Undaria pinnatifida Laminariales Mori et al., 1982 Petalonia fascia Scytosiphonales Usov et al., 2001 Scytosiphon lomentaria Scytosiphonales Usov et al., 2001 Nomenclature the generic term fucans, to designate all polysaccharides rich Killing baptized his polysaccharide fucoidin; 40 years later, in L-fucose, was commonly used (Percival and Ross, 1950). McNeely changed fucoidin to fucoidan, to conform with As separation and analytic techniques improved, different polysaccharide nomenclature (McNeely, 1959). The ques- types of sulfated polysaccharides were distinguished in tions of nomenclature and purity have always been linked fucan preparations. The first was ascophyllan or xylofuco- for algal fucoidans; early preparations contained large glycuronan, based on a backbone of uronic acid (mannuronic amounts of sugars other than fucose, such as galactose, acid) with fucose containing branches (3-O-D-xylosyl-L- mannose, xylose, or uronic acid, and sometimes even pro- fucose-4-sulfate) (Larsen et al., 1966; Kloareg et al., 1986). teins. Furthermore, their composition changed according to The other family isolated was sargassan or glycuronofuco- the algal species (Percival and Ross, 1950; Mian and glycan, based on linear chains of D-galactose with branches Percival, 1973), the extraction process (Mabeau et al., 1990), of L-fucose-3-sulfate or occasionally uronic acid (Percival, and the season of harvest and local climatic conditions 1968; Medcalf et al., 1978; Kloareg et al., 1986). Fucoidans, (Black, 1954; Von Holdt et al., 1955; Wort, 1955; Honya as originally defined, were identified as homofucans et al., 1999). Were these contaminants (Percival and Ross, (Kloareg et al., 1986). Many authors still use the outdated 1950; O'Neill, 1954; Bernardi and Springer, 1962) or part of term fucoidin. In some cases, authors create their own the polysaccharide (Schweiger, 1962; Anno et al., 1966)? nomenclature, such as fucansulfate (in one word) (Trento Some authors even considered suppressing the term of et al., 2001). The confusion is increased with some fucoidan (Larsen et al., 1966). To face these uncertainties, publications in which the term fucoidan is used to describe 30R Structure and biological properties of sulfated fucans a complex polysaccharide containing only 20% to 60% A. Ascophyllum nodosum/Fucus vesiculosus/Fucus evanescens B. Ecklonia kurome L-fucose (Duarte et al., 2001).

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