Glycoconjugate Journal

, Volume 27, Issue 1, pp 1–12

Structural and functional insights into sulfated galactans: a systematic review

Article

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.

Keywords

Acrosome reaction Agar Carrageen Pharmacological application Marine organisms 

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

  1. 1.
    Pomin, V.P., Mourão, P.A.: Structure, biology, evolution, and medical importance of sulfated fucans and galactans. Glycobiology. 18, 1016–1027 (2008)CrossRefPubMedGoogle Scholar
  2. 2.
    Pomin, V.P.: An overview about the structure-function relationship of marine sulfated homopolysaccharides with regular chemical structures. Biopolymers. 91, 601–609 (2009)Google Scholar
  3. 3.
    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)CrossRefPubMedGoogle Scholar
  4. 4.
    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 pressGoogle Scholar
  5. 5.
    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)CrossRefPubMedGoogle Scholar
  6. 6.
    Mourão, P.A.: A carbohydrate-based mechanism of species recognition in sea urchin fertilization. Braz. J. Med. Biol. Res. 40, 5–17 (2007)CrossRefPubMedGoogle Scholar
  7. 7.
    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)CrossRefPubMedGoogle Scholar
  8. 8.
    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)CrossRefPubMedGoogle Scholar
  9. 9.
    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)CrossRefPubMedGoogle Scholar
  10. 10.
    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)CrossRefPubMedGoogle Scholar
  11. 11.
    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)CrossRefPubMedGoogle Scholar
  12. 12.
    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)CrossRefPubMedGoogle Scholar
  13. 13.
    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)CrossRefPubMedGoogle Scholar
  14. 14.
    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)CrossRefPubMedGoogle Scholar
  15. 15.
    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)CrossRefPubMedGoogle Scholar
  16. 16.
    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)CrossRefPubMedGoogle Scholar
  17. 17.
    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)CrossRefPubMedGoogle Scholar
  18. 18.
    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)CrossRefPubMedGoogle Scholar
  19. 19.
    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)CrossRefPubMedGoogle Scholar
  20. 20.
    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)CrossRefPubMedGoogle Scholar
  21. 21.
    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)CrossRefPubMedGoogle Scholar
  22. 22.
    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)CrossRefPubMedGoogle Scholar
  23. 23.
    Mourão, P.A.: Use of sulfated fucans as anticoagulant and antithrombotic agents: future perspectives. Curr. Pharm. Des. 10, 967–981 (2004)CrossRefPubMedGoogle Scholar
  24. 24.
    Mourão, P.A., Pereira, M.S.: Searching for alternatives to heparin: sulfated fucans from marine invertebrates. Trends Cardiovasc. Med. 9, 225–232 (1999)CrossRefPubMedGoogle Scholar
  25. 25.
    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)PubMedGoogle Scholar
  26. 26.
    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)CrossRefPubMedGoogle Scholar
  27. 27.
    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)CrossRefPubMedGoogle Scholar
  28. 28.
    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).Google Scholar
  29. 29.
    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)CrossRefGoogle Scholar
  30. 30.
    Bixler, H.J.: The carrageenan connection IV. Brit. Food. J. 96, 12–17 (1994)CrossRefGoogle Scholar
  31. 31.
    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)CrossRefGoogle Scholar
  32. 32.
    Lahaye, M.: Developments on gelling algal galactans, their structure and physico-chemistry. J. Appl. Phycol. 13, 173–184 (2001)CrossRefGoogle Scholar
  33. 33.
    Usov, A.I.: Structural analysis of red seaweed galactans of agar and carrageenan groups. Food Hydrocoll. 12, 301–308 (1998)CrossRefGoogle Scholar
  34. 34.
    van de Velde, F., Pereira, L., Rollema, H.S.: The revised NMR chemical shift data of carrageenans. Carbohydr. Res. 339, 2309–2313 (2004)CrossRefPubMedGoogle Scholar
  35. 35.
    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)CrossRefPubMedGoogle Scholar
  36. 36.
    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)CrossRefPubMedGoogle Scholar
  37. 37.
    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)CrossRefPubMedGoogle Scholar
  38. 38.
    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)CrossRefPubMedGoogle Scholar
  39. 39.
    Whittaker, R.H.: New concepts of kingdoms of organisms. Science 163, 150–160 (1969)CrossRefPubMedGoogle Scholar
  40. 40.
    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)CrossRefPubMedGoogle Scholar
  41. 41.
    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)PubMedGoogle Scholar
  42. 42.
    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)CrossRefPubMedGoogle Scholar
  43. 43.
    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)CrossRefPubMedGoogle Scholar
  44. 44.
    Vacquier, V.D., Hirohashi, N.: Sea urchin spermatozoa. Methods Cell Biol. 74, 523–544 (2004)CrossRefPubMedGoogle Scholar
  45. 45.
    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)CrossRefPubMedGoogle Scholar
  46. 46.
    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)CrossRefGoogle Scholar
  47. 47.
    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)Google Scholar
  48. 48.
    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)CrossRefPubMedGoogle Scholar
  49. 49.
    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)CrossRefGoogle Scholar
  50. 50.
    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)CrossRefPubMedGoogle Scholar
  51. 51.
    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)CrossRefPubMedGoogle Scholar
  52. 52.
    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)CrossRefPubMedGoogle Scholar
  53. 53.
    Zigler, K.S.: The evolution of sea urchin sperm bindin. Int. J. Dev. Biol. 52, 791–796 (2008)CrossRefPubMedGoogle Scholar
  54. 54.
    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)CrossRefPubMedGoogle Scholar
  55. 55.
    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)PubMedGoogle Scholar
  56. 56.
    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)CrossRefGoogle Scholar
  57. 57.
    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)Google Scholar
  58. 58.
    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)CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Complex Carbohydrate Research CenterUniversity of GeorgiaAthensUSA

Personalised recommendations