Abstract
Sulfated galactans (SGs) are highly anionic marine galactose-composed homopolysaccharides. Although their structures vary among species, their main features are conserved among phyla. Green algal SGs are quite heterogeneous, although preponderantly composed of 3-β-D-Galp units. The red algal SGs (like agar and carrageen) are composed of repeating disaccharide units with different sulfation patterns which vary among species. The SGs from invertebrates such as sea urchins and ascidians (tunicates), and from the unique description of a sea-grass, are composed of well-defined repetitive units. Chains of 3-linked β-galactoses are highly conserved in some marine taxonomic groups, with a strong tendency toward 4-sulfation in algae and marine angiosperm, and 2-sulfation in invertebrates. These carbohydrates are extracellular components of the cell wall in plants, of the body wall in tunicates, and of the jelly coat in sea urchin eggs. In sea urchins, the SGs are also responsible to induce the acrosome reaction. However, the wide range of potential pharmacological uses, especially as anticoagulants and antithrombotics, is the main reason for the increasing interest in these sugars. Both natural and clinical actions of SGs have a direct relation to their structural features, since the intermolecular complexes between SG and target proteins are much more stereospecific than only electric charge-dependent. This review will present an overview about the principle structural and functional information of SGs. Other important aspects concerning occurrence, biology, phylogeny, and future directions, will also be reported.
Similar content being viewed by others
Abbreviations
- aPPT:
-
activated partial thromboplastin time
- AR:
-
acrosome reaction
- AT:
-
antithrombin
- CAM:
-
chorioallantoic membrane
- FGF-2:
-
fibroblast growth factor 2
- HCII:
-
heparin cofactor II
- IC50 :
-
inhibitory concentration 50%
- SG:
-
sulfated galactan
- MW:
-
molecular weight
- 5-Fu:
-
Fluorouracil
References
Pomin, V.P., Mourão, P.A.: Structure, biology, evolution, and medical importance of sulfated fucans and galactans. Glycobiology. 18, 1016–1027 (2008)
Pomin, V.P.: An overview about the structure-function relationship of marine sulfated homopolysaccharides with regular chemical structures. Biopolymers. 91, 601–609 (2009)
Alves, A.P., Mulloy, B., Diniz, J.A., Mourão, P.A.: Sulfated polysaccharides from the egg jelly layer are species-specific inducers of acrosomal reaction in sperms of sea urchins. J. Biol. Chem. 272, 6965–6971 (1997)
Castro, M.O., Pomin, V.H., Santos, L.L., Vilela-Silva, A.C., Hirohashi, N., Pol-Fachin, L., Verli, H., Mourão, P.A.: A unique 2-sulfated beta-galactan from the EGG jelly of the sea urchin glyptocidaris crenularis: Conformation flexibility versus induction of the sperm acrosome reaction. J. Biol. Chem. (2009), in press
Vilela-Silva, A.C., Hirohashi, N., Mourão, P.A.: The structure of sulfated polysaccharides ensures a carbohydrate-based mechanism for species recognition during sea urchin fertilization. Int. J. Dev. Biol. 52, 551–559 (2008)
Mourão, P.A.: A carbohydrate-based mechanism of species recognition in sea urchin fertilization. Braz. J. Med. Biol. Res. 40, 5–17 (2007)
Matsuhiro, B., Conte, A.F., Damonte, E.B., Kolender, A.A., Matulewicz, M.C., Mejías, E.G., Pujol, C.A., Zúñiga, E.A.: Structural analysis and antiviral activity of a sulfated galactan from the red seaweed Schizymenia binderi (Gigartinales, Rhodophyta). Carbohydr. Res. 340, 2392–2402 (2005)
Talarico, L.B., Zibetti, R.G., Faria, P.C., Scolaro, L.A., Duarte, M.E., Noseda, M.D., Pujol, C.A., Damonte, E.B.: Anti-herpes simplex virus activity of sulfated galactans from the red seaweeds Gymnogongrus griffithsiae and Cryptonemia crenulata. Int. J. Biol. Macromol. 34, 63–71 (2004)
Mazumder, S., Ghosal, P.K., Pujol, C.A., Carlucci, M.J., Damonte, E.B., Ray, B.: Isolation, chemical investigation and antiviral activity of polysaccharides from Gracilaria corticata (Gracilariaceae, Rhodophyta). Int. J. Biol. Macromol. 31, 87–95 (2002)
Duarte, M.E., Noseda, D.G., Noseda, M.D., Tulio, S., Pujol, C.A., Damonte, E.B.: Inhibitory effect of sulfated galactans from the marine alga Bostrychia montagnei on herpes simplex virus replication in vitro. Phytomedicine 8, 53–58 (2001)
Duarte, M.E., Cauduro, J.P., Noseda, D.G., Noseda, M.D., Gonçalves, A.G., Pujol, C.A., Damonte, E.B., Cerezo, A.S.: The structure of the agaran sulfate from Acanthophora spicifera (Rhodomelaceae, Ceramiales) and its antiviral activity. Relation between structure and antiviral activity in agarans. Carbohydr. Res. 339, 335–347 (2004)
Chattopadhyay, K., Ghosh, T., Pujol, C.A., Carlucci, M.J., Damonte, E.B., Ray, B.: Polysaccharides from Gracilaria corticata: sulfation, chemical characterization and anti-HSV activities. Int. J. Biol. Macromol. 43, 346–351 (2008)
Cáceres, P.J., Carlucci, M.J., Damonte, E.B., Matsuhiro, B., Zuñiga, E.A.: Carrageenans from chilean samples of Stenogramme interrupta (Phyllophoraceae): structural analysis and biological activity. Phytochemistry 53, 81–86 (2000)
Talarico, L.B., Pujol, C.A., Zibetti, R.G., Faría, P.C., Noseda, M.D., Duarte, M.E., Damonte, E.B.: The antiviral activity of sulfated polysaccharides against dengue virus is dependent on virus serotype and host cell. Antiviral. Res. 66, 103–110 (2005)
Zhou, G., Sun, Y., Xin, H., Zhang, Y., Li, Z., Xu, Z.: In vivo antitumor and immunomodulation activities of different molecular weight lambda-carrageenans from Chondrus ocellatus. Pharmacol. Res. 50, 47–53 (2004)
Zhou, G., Xin, H., Sheng, W., Sun, Y., Li, Z., Xu, Z.: In vivo growth-inhibition of S180 tumor by mixture of 5-Fu and low molecular lambda-carrageenan from Chondrus ocellatus. Pharmacol. Res. 51, 153–157 (2005)
Zhou, G., Sheng, W., Yao, W., Wang, C.: Effect of low molecular lambda-carrageenan from Chondrus ocellatus on antitumor H-22 activity of 5-Fu. Pharmacol. Res. 53, 129–134 (2006)
Bürgermeister, J., Paper, D.H., Vogl, H., Linhardt, R.J., Franz, G.: LaPSvS1, a (1-->3)-beta-galactan sulfate and its effect on angiogenesis in vivo and in vitro. Carbohydr. Res. 337, 1459–1466 (2002)
Farias, W.R., Valente, A.P., Pereira, M.S., Mourão, P.A.: Structure and anticoagulant activity of sulfated galactans. Isolation of a unique sulfated galactan from the red algae Botryocladia occidentalis and comparison of its anticoagulant action with that of sulfated galactans from invertebrates. J. Biol. Chem. 275, 29299–29307 (2000)
Pereira, M.S., Melo, F.R., Mourão, P.A.: Is there a correlation between structure and anticoagulant action of sulfated galactans and sulfated fucans? Glycobiology 12, 573–580 (2002)
Pereira, M.S., Vilela-Silva, A.C., Valente, A.P., Mourão, P.A.: A 2-sulfated, 3-linked alpha-L-galactan is an anticoagulant polysaccharide. Carbohydr. Res. 337, 2231–2238 (2002)
Pereira, M.G., Benevides, N.M., Melo, M.R., Valente, A.P., Melo, F.R., Mourão, P.A.: Structure and anticoagulant activity of a sulfated galactan from the red alga, Gelidium crinale. Is there a specific structural requirement for the anticoagulant action? Carbohydr. Res. 340, 2015–2023 (2005)
Mourão, P.A.: Use of sulfated fucans as anticoagulant and antithrombotic agents: future perspectives. Curr. Pharm. Des. 10, 967–981 (2004)
Mourão, P.A., Pereira, M.S.: Searching for alternatives to heparin: sulfated fucans from marine invertebrates. Trends Cardiovasc. Med. 9, 225–232 (1999)
Fonseca, R.J., Oliveira, S.N., Melo, F.R., Pereira, M.G., Benevides, N.M., Mourão, P.A.: Slight differences in sulfation of algal galactans account for differences in their anticoagulant and venous antithrombotic activities. Thromb. Haemost. 99, 539–545 (2008)
Farias, E.H., Pomin, V.H., Valente, A.P., Nader, H.B., Rocha, H.A., Mourão, P.A.: A preponderantly 4-sulfated, 3-linked galactan from the green alga Codium isthmocladum. Glycobiology 18, 250–259 (2008)
Bilan, M.I., Vinogradova, E.V., Shashkov, A.S., Usov, A.I.: Structure of a highly pyruvylated galactan sulfate from the Pacific green alga Codium yezoense (Bryopsidales, Chlorophyta). Carbohydr. Res. 342, 586–596 (2007)
Love, J., Percival, E.: The polysaccharides of green seaweed Codium fragile: Part III A β-1,4-linked mannan. J. Chem. Soc. 3345–3350 (1964).
Matsubara, K., Matsuura, Y., Bacic, A., Liao, M.-L., Hori, K., Miyazawa, K.: Anticoagulant properties of a sulfated galactan preparation from a marine green alga. Codium. Cylindricum. Biol. Macromol. 28, 395–399 (2001)
Bixler, H.J.: The carrageenan connection IV. Brit. Food. J. 96, 12–17 (1994)
Knutsen, S.H., Myslabodski, D.E., Larsen, B., Usov, A.I.: A modified system of nomenclature for red algal galactans. Bot. Mar. 37, 163–169 (1994)
Lahaye, M.: Developments on gelling algal galactans, their structure and physico-chemistry. J. Appl. Phycol. 13, 173–184 (2001)
Usov, A.I.: Structural analysis of red seaweed galactans of agar and carrageenan groups. Food Hydrocoll. 12, 301–308 (1998)
van de Velde, F., Pereira, L., Rollema, H.S.: The revised NMR chemical shift data of carrageenans. Carbohydr. Res. 339, 2309–2313 (2004)
Aquino, R.S., Landeira-Fernandez, A.M., Valente, A.-P., Andrade, L.R., Mourão, P.A.S.: Occurrence of sulfated galactans in marine angiosperms: Evolutionary implications. Glycobiology 15, 11–20 (2005)
Santos, J.A., Mulloy, B., Mourão, P.A.: Structural diversity among sulfated alpha-L-galactans from ascidians (tunicates). Studies on the species Ciona intestinalis and Herdmania monus. Eur. J. Biochem. 204, 669–677 (1992)
Mourão, P.A., Perlin, A.S.: Structural features of sulfated glycans from the tunic of Styela plicata Chordata-Tunicata: A unique occurrence of L-galactose in sulfated polysaccharides. Eur. J. Biochem. 166, 431–436 (1987)
Albano, R.M., Pavão, M.S., Mourão, P.A., Mulloy, B.: Structural studies of a sulfated L-galactan from Styela plicata (Tunicate): Analysis of the Smith-degraded polysaccharide. Carbohydr. Res. 208, 163–174 (1990)
Whittaker, R.H.: New concepts of kingdoms of organisms. Science 163, 150–160 (1969)
Amornrut, C., Toida, T., Imanari, T., Woo, E.-R., Park, H., Linhardt, R., Wu, S.J., Kim, Y.S.: A new sulfated beta-galactan from clams with anti-HIV activity. Carbohydr. Res. 321, 121–127 (1999)
Pavão, M.S.G., Albano, R.M., Lawsom, A.M., Mourão, P.A.: Structural heterogeneity among unique sulfated L-galactans from different species of ascidians (tunicates). J. Biol. Chem. 264, 9972–9979 (1989)
Pavão, M.S.G., Mourão, P.A., Mulloy, B.: Structure of a unique sulfated alpha-L-galactofucan from the tunicate Clavelina. Carbohydr. Res. 208, 153–161 (1990)
Scudder, P., Tanq, P.W., Hounsell, E.F., Lawson, A.M., Mehmet, H., Feizi, T.: Isolation and characterization of sulphated oligosaccharides released from bovine corneal keratin sulphate by the action of endo-beta-galactosidase. Eur. J. Biochem. 157, 365–373 (1986)
Vacquier, V.D., Hirohashi, N.: Sea urchin spermatozoa. Methods Cell Biol. 74, 523–544 (2004)
Gunaratne, H.J., Moy, G.W., Kinukawa, M., Miyata, S., Mash, S.A., Vacquier, V.D.: The 10 sea urchin receptor for egg jelly proteins (SpREJ) are members of the polycystic kidney disease-1 (PKD1) family. BMC. Genomics. 8, 235 (2007)
Darszon, A., Acevedo, J.J., Galindo, B.E., Hernández-González, E.O., Nishigaki, T., Treviño, C.L., Wood, C., Beltrán, C.: Sperm channel diversity and functional multiplicity. Reproduction 161, 977–988 (2006)
Darszon, A., López-Martínez, P., Acevedo, J.J., Hernández-Cruz, A., Treviño, C.L.: T-type Ca2+ channels in sperm function. In: Cell Calcium. 40:241–252 (2006)
de la Sancha, C.U., Martinez-Cadena, G., López-Godínez, J., Castellano, L.E., Nishigaki, T., Darszon, A., García-Soto, J.: Rho-kinase (ROCK) in sea urchin sperm: Its role in regulating the intracellular pH during the acrosome reaction. Biochem. Biophys. Res. Commun. 364, 470–475 (2007)
Vacquier, V.D., Swanson, W.J., Hellberg, M.E.: What have we learned about sea urchin sperm bindin? Dev. Growth Differ. 37, 1–10 (1995)
Cameron, R.A., Walkup, T.S., Rood, K., Moore, J.G., Davidson, E.H.: Specific in vitro interaction between recombinant Strongylocentrotus purpuratus bindin and a recombinant 45A fragment of the putative bindin receptor. Dev. Biol. 180, 348–352 (1996)
Glaser, R.W., Grüne, M., Wandelt, C., Ulrich, A.S.: Structure analysis of a fusogenic peptide sequence from the sea urchin fertilization protein bindin. Biochemistry 38, 2560–2569 (1999)
Kamei, N., Glabe, C.G.: The species-specific egg receptor for sea urchin sperm adhesion is EBR1, a novel ADAMTS protein. Gene. Dev. 17, 2502–2507 (2003)
Zigler, K.S.: The evolution of sea urchin sperm bindin. Int. J. Dev. Biol. 52, 791–796 (2008)
Hirohashi, N., Vacquier, V.D.: Egg sialoglycans increase intracellular pH and potentiate the acrosome reaction of the sea urchin sperm. J. Biol. Chem. 277, 8041–8047 (2002)
Jackson, J.R., Seed, M.P., Kircher, C.H., Willoughby, D.A., Winkler, J.D.: The codependence of angiogenesis and chronic inflammation. FASEB. J. 11, 457–465 (1997)
Fareed, J.W., Hoppensteadt, D., Bick, R.L.: An update of heparins at the beginning of the new millennium. Sem. Thromb. Haemost. 26, 5–21 (2000)
Guerrini, M., Beccati, D., Shriver, Z., Naggi, A., Viswanathan, K., Bisio, A., Capila, I., Lansing, J.C., Guglieri, S., Fraser, B., Al-Hakim, A., Gunay, N.S., Zhang, Z., Robinson, L., Buhse, L., Nasr, M., Woodcock, J., Langer, R., Venkataraman, G., Linhardt, R.J., Casu, B., Torri, G., Sasisekharan, R.: Oversulfated chondroitin sulfate is a contaminant in heparin associated with adverse clinical events. Nat. Biotechnol. 10, 1–7 (2008)
Kishimoto, T.K., Viswanathan, K., Ganguly, T., Elankumaran, S., Smith, S., Pelzer, K., Lansing, J.C., Sriranganathan, N., Zhao, G., Galcheva-Gargova, Z., Al-Hakim, A., Bailey, G.S., Fraser, B., Roy, S., Rogers-Cotrone, T., Buhse, L., Whary, M., Fox, J., Nasr, M., Dal Pan, G.J., Shriver, Z., Langer, R.S., Venkataraman, G., Austen, K.F., Woodcock, J., Sasisekharan, R.: Contaminated heparin associated with adverse clinical events and activation of the contact system. New. Engl. J. Med. 358, 2457–2467 (2008)
Acknowledgements
I would like to kindly thank Prof. Megan Macnaughtan for the careful editing and Prof. James H. Prestegard for the post-doctoral position in his laboratory which allowed me to write this review there.
Conflict of interest statement
None declared.
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by the postdoctoral fellowship number 201019/2008-6 from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
Rights and permissions
About this article
Cite this article
Pomin, V.H. Structural and functional insights into sulfated galactans: a systematic review. Glycoconj J 27, 1–12 (2010). https://doi.org/10.1007/s10719-009-9251-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10719-009-9251-z