ANTİCOAGULANT AND ANTİLİPAEMİC ACTİVİTİES OF POLYSACCHARİDES FROM MARİNE ALGAE
07/27/2019Anticoagulant and antilipaemic activities of polysaccharides from marine algae
Kasım Cemal Güven, Burak Coban, Ekrem Sezik
Turkish Marine Research Foundation (TUDAV), PK 10, Beykoz, Istanbul, TURKEY
Department of Chemistry, Bulent Ecevit University, Incivez, 67100 Zonguldak, TURKEY
Institute of Health Sciences, Yeditepe University, 34755, Istanbul, TURKEY
Abstract
In this review the research on the anticoagulant and antilipaemic activity of sulfated and synthetically modified polysaccharides extracted from marine macro algae between 1913 and 2018 was summarized and the results were compared with a long known natural polysaccharide from animal sources, heparin which contain N-sulfate group. The highest anticoagulant activity of algal sulfated polysaccharide was obtained from Dictiyota menstrualis, red alga, found to be 4.8 times more active than heparin. Antilipaemic activity of some algal sulfated polysaccharides showed similar activity as heparin.
Keywords: Anticoagulant, antilipaemic, polysaccharides
References
Abdel-Fattah, A.F., Hussein, M.M.-E., Salem, H.M. (1973) Sargassan: A sulphated heteropolysaccharide from Sargassum linifolium. Phytochem 12(8): 1995-1998.
Abdel-Fattah, A.F., Hussein, M.M.-D., Salem, H.M. (1974) Studies of the purification and some properties of sargassan, a sulphated heteropolysaccharide from Sargassum linifolium. Carbohydr Res 33(1): 9-17.
Abou-Zeid, A.H., Aboutabl, E.A., Sleem, A.A., El-Rafie, H.M. (2014) Water soluble polysaccharides extracted from Pterocladia capillacea and Dictyopteris membranacea and their biological activities. Carbohydr Polym 113: 62-66.
Adams, S.S., Heathcote, B.V., Walker, D. (1962) Sulphated degraded laminarin: an antilipaemic agent. J Atheroscler Res 2: 314-316.
Adams, S.S., Thorpe, H.M. (1957) The anticoagulant activity and toxicity of laminarine sulphate K. J Pharm Pharmacol 9(1): 459-463.
Aktin, E., Güven, K.C. (1965) Studies on antilipemic properties of the algae collected from Turkish coasts – III. Sargassum vulgare Ag., Polysiphonia subulifera (C. Agardh) Harvey. Qual Plant Mater Veget 12(2): 210-215.
Aktin, E., Güven, K.C. (1969) Studies on the lipase released by the substances obtained from Gracilaria verrucosa (Hunds.) and Gelidium latifolium (Greville). Arzneimittel-Forsch 19(2): 190-193.
Alban, S., Kraus, J., Franz, G. (1992) Synthesis of laminarin sulfates with anticoagulant activity. Arzneimittel-Forsch 42(8): 1005-1008.
Albuquerque, I.R., Queiroz, K.C., Alves, L.G., Santos, E.A., Leite, E.L., Rocha, H.A. (2004) Heterofucans from Dictyota menstrualis have anticoagulant activity. Braz J Med Biol Res 37(2): 167-171.
Almeida-Lima, J., Costa, L.S., Silva, N.B., Melo-Silveira, R.F., Silva, F.V., Felipe, M.B., Medeiros, S.R., Leite, E.L., Rocha, H.A. (2010) Evaluating the possible genotoxic, mutagenic and tumor cell proliferation-inhibition effects of a non-anticoagulant, but antithrombotic algal heterofucan. J Appl Toxicol 30(7): 708-715.
Almeida-Lima, J., Dantas-Santos, N.L., Gomes, D., Cordeiro, S.L., Sabry, D.A., Costa, L.S., Freitas, M.D.L., Silva, N.B., Moura, C.E.B., Lemos, T.M.A.M., Leite, E.L., Rocha, H.A.O. (2011) Evaluation of acute and subchronic toxicity of a non-anticoagulant, but antithrombotic algal heterofucan from the Spatoglossum schröederi in Wistar rats. Rev Bras Farmacogn 21: 674-679.
Anderson, W., Duncan, J.G.C., Harthill, J. E. (1965) The anticoagulant activity of carrageenan. J Pharm Pharmacol 17(10): 647-654.
Arenajo, A.R., Ybanez, A.P., Ababan, M.M.P., Villajuan, C. E., Lasam, M.R.M., Young, C.P., Reyes, J.L.A. (2017) The potential anticoagulant property of Caulerpa lentillifera crude extract. Int J Health Sci 11(3): 29-32.
Astrup, T., Mullertz, S. (1952) The fibrin plate method for estimating fibrinolytic activity. Arch Biochem Biophys 40(2): 346-351.
Athukorala, Y., Jung, W.-K., Vasanthan, T., Jeon, Y.-J. (2006) An anticoagulative polysaccharide from an enzymatic hydrolysate of Ecklonia cava. Carbohydr Polym 66(2): 184-191.
Athukorala, Y., Lee, K., Kim, S., Jeon, Y. (2007) Anticoagulant activity of marine green and brown algae collected from Jeju Island in Korea. Bioresour Technol 98(9): 1711-1716.
Baker, S.P. (1957) Heparin-activated clearing factor; standardized test, agewise application, and clinical observations. Circulation 15(6): 889-896.
Ben Gara, A., Ben Abdallah Kolsi, R., Chaaben, R., Hammami, N., Kammoun, M., Paolo Patti, F., El Feki, A., Fki, L., Belghith, H., Belghith, K. (2017) Inhibition of key digestive enzymes related to hyperlipidemia and protection of liver-kidney functions by Cystoseira crinita sulphated polysaccharide in highfat diet-fed rats. Biomed Pharmacother 85: 517-526.
Bergström, S. (1935) Über die wirkungsgruppe des heparins. Naturwissenschaften 23(41): 706-706.
Bergström, S. (1936) Über polysaccharides terschwefelsäuren mit heparin wirkung. H-S Z Physiol Chem 238(4-5): 163-168.
Bernardi, G., Springer, G.F. (1962) Properties of highly purified fucan. J Biol Chem 237: 75-80.
Besterman, E.M.M., Evans, J. (1957) Antilipaemic agent without anticoagulant action. Brit Med J 1: 310-312.
Bilan, M.I., Klochkova, N.G., Ustyuzhanina, N.E., Chizhov, A.O., Shashkov, A.S., Nifantiev, N.E., Usov, A.I. (2016) Polysaccharides of algae 68. Sulfated polysaccharides from the Kamchatka brown alga Laminaria bongardiana. Russ Chem Bull 65(11): 2729-2736.
Camara, R.B.G., Costa, L.S., Fidelis, G.P., Nobre, L.T.D.B., Dantas-Santos, N., Cordeiro, S.L., Costa, M.S.S.P., Alves, L.G., Rocha, H.A.O. (2011) Heterofucans from the brown seaweed Canistrocarpus cervicornis with anticoagulant and antioxidant activities. Mar Drugs 9(1): 124.
Cao, J., Wang, S.C., Yao, C.W., Xu, Z., Xu, X.M. (2016) Hypolipidemic effect of porphyran extracted from Pyropia yezoensis in ICR mice with high fatty diet. J Appl Phycol 28: 1315-1322.
Carlucci, M.J., Pujol, C.A., Ciancia, M., Noseda, M.D., Matulewicz, M.C., Damonte, E.B., Cerezo, A.S. (1997) Antiherpetic and anticoagulant properties of carrageenans from the red seaweed Gigartina skottsbergii and their cyclized derivatives: correlation between structure and biological activity. Int J Biol Macromol 20(2): 97-105.
Chandía, N.P., Matsuhiro, B. (2008) Characterization of a fucoidan from Lessonia vadosa (Phaeophyta) and its anticoagulant and elicitor properties. Int J Biol Macromol 42(3): 235-240.
Chargaff, E., Bancroft, F.W., Brown, M.S. (1936) Studies on the chemistry of blood coagulation: II. On the inhibition of blood clotting by substances of high molecular weight. J Biol Chem 115: 155-161.
Chen, X., Yang, S., Wang, J., Song, L., Xing, R., Liu, S., Yu, H., Li, P. (2015) Sulfated polysaccharides isolated from cloned Grateloupia filicina and their anticoagulant activity. BioMed Res Int. doi: 10.1155/2015/612352.
Cheng, Z., Wang, S. (2003) Study on anticoagulant activities in vitro of fucoidan and fucoidan / collagen blends. J Funct Polym 2003(4): 557-560.
Chevolot, L., Foucault, A., Chaubet, F., Kervarec, N., Sinquin, C., Fisher, A.M., Boisson-Vidal, C. (1999) Further data on the structure of brown seaweed fucans: relationships with anticoagulant activity. Carbohydr Res 319(1-4): 154-165.
Chevolot, L., Mulloy, B., Ratiskol, J., Foucault, A., Colliec-Jouault, S. (2001) A disaccharide repeat unit is the major structure in fucoidans from two species of brown algae. Carbohydr Res 330(4): 529-535.
Ciancia, M., Quintana, I., Vizcarguenaga, M.I., Kasulin, L., DeDios, A., Estevez, J.M., Cerezo, A.S. (2007) Polysaccharides from the green seaweeds Codium fragile and C. vermilara with controversial effects on hemostasis. Int J Biol Macromol 41(5): 641-649.
Colliec, S., Fischer, A.M., Tapon-Bretaudiere, J., Boisson, C., Durand, P., Jozefonvicz, J. (1991) Anticoagulant properties of a fucoidan fraction. Thromb Res 64(2): 143-154.
Colliec-Jouault, S., Millet, J., Helley, D., Sinquin, C., Fischer, A.M. (2003) Effect of low-molecular-weight fucoidan on experimental arterial thrombosis in the rabbit and rat. J Thromb Haemost 1(5): 1114-1115.
Constantinides, P., Cairns, A., Werner, A. (1954) Antilipemic activity of sulfated polysaccharides. Arch Int Pharmacodyn Ther 99(3-4): 334-345.
Constantinides, P., Johnson, C., Fahrni, B.M., Nakashima, R., Mc, I.H. (1960) Human hyperlipaemia and hypercholesterolaemia: rapid correction with a sulphated polymannuronide. Brit Med J 1(5172): 535-540.
Costa, L.S., Fidelis, G.P., Cordeiro, S.L., Oliveira, R.M., Sabry, D.A., Camara, R.B., Nobre, L.T., Costa, M.S., Almeida-Lima, J., Farias, E.H., Leite, E.L., Rocha, H.A. (2010) Biological activities of sulfated polysaccharides from tropical seaweeds. Biomed Pharmacother 64(1): 21-28.
Cumashi, A., Ushakova, N.A., Preobrazhenskaya, M.E., D’Incecco, A., Piccoli, A., Totani, L., Tinari, N., Morozevich, G.E., Berman, A.E., Bilan, M.I., Usov, A.I., Ustyuzhanina, N.E., Grachev, A.A., Sanderson, C.J., Kelly, M., Rabinovich, G.A., Iacobelli, S., Nifantiev, N.E. (2007) A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 17(5): 541-552.
de Lara-Isassi, G., Alvarez-Hernandez, S., Quintana-Pimentel, A. (2004) Screening for anticoagulant substances in some marine macroalgae. Hydrobiologia 14(1): 47-54.
de Zoysa, M., Nikapitiya, C., Jeon, Y.-J., Jee, Y., Lee, J. (2008) Anticoagulant activity of sulfated polysaccharide isolated from fermented brown seaweed Sargassum fulvellum. J Appl Phycol 20(1): 67-74.
Deacon-Smith, R.A., Lee-Potter, J.P., Rogers, D.J. (1985a) Anticoagulant activity in extracts of British marine algae. Bot Mar 28(8): 333.
Deacon-Smith, R.A., Lee-Potter, J.P., Rogers, D.J. (1985b) Platelet aggregation in the presence of extracts of British marine algae. Med Lab Sci 42(4): 404-405.
Deacon-Smith, R.A., Rogers, D.J. (1982) Antihaemostatic activities of British marine algae. Brit Phycol J 17: 231.
Demole, V., Reinert, M. (1930) Polyanetholsulfosaures Natrium, ein neues synthetisches Mittel zur Hemmung der Blutgerinnung. N-S Arch Exp Pathol Pharmakol 158(1): 211-218.
Dewar, E.T. (1956) Sodium laminarin sulphate as a blood anticoagulant. Paper read at 2nd Int. Seaweed Symposium, Trondheim.
Dobashi, K., Nishino, T., Fujihara, M., Nagumo, T. (1989) Isolation and preliminary characterization of fucose-containing sulfated polysaccharides with blood-anticoagulant activity from the brown seaweed Hizikia fusiforme. Carbohydr Res 194: 315-320.
Doctor, V.M., Lewis, D., Coleman, M., Kemp, M.T., Marbley, E., Sauls, V. (1991) Anticoagulant properties of semisynthetic polysaccharide sulfates. Thromb Res 64(4): 413-425.
Dodgson, K., Price, R. (1962) A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem J 84(1): 106-110.
Dore, C.M.P.G., Faustino Alves, M.G.D.C., Pofírio Will, L.S.E., Costa, T.G., Sabry, D.A., de Souza-Rêgo, L.A.R., Accardo, C.M., Rocha, H.A.O., Filgueira, L.G.A., Leite, E.L. (2013) A sulfated polysaccharide, fucans, isolated from brown algae Sargassum vulgare with anticoagulant, antithrombotic, antioxidant and anti-inflammatory effects. Carbohydr Polym 91(1): 467-475.
Duncombe, W.G. (1963) The colorimetric micro-determination of long-chain fatty acids. Biochem J 88(1): 7-10.
Duncombe, W.G. (1964) The colorimetric micro-determination of non-esterified fatty acids in plasma. Clin Chim Acta 9: 122-125.
Durand, E., Helley, D., Zen, A.A.H., Dujols, C., Bruneval, P., Colliec-Jouault, S., Fischer, A.M., Lafont, A. (2008) Effect of low molecular weight fucoidan and low molecular weight heparin in a rabbit model of arterial thrombosis. J Vasc Res 45(6): 529-537.
Durig, J., Bruhn, T., Zurborn, K.H., Gutensohn, K., Bruhn, H.D., Beress, L. (1997) Anticoagulant fucoidan fractions from Fucus vesiculosus induce platelet activation in vitro. Thromb Res 85(6): 479-491.
Ehrlich, P. (1877) Beitrage zur kenntniss der anilinfarbungen und ihrer verwendung in der mikroskopischen technik. Arch Mikrosk Anat 13: 263-277.
Elmegeed, D.F.A., Ghareeb, D.A., Elsayed, M., El-Saadani, M. (2014) Phytochemical constituents and bioscreening activities of green algae (Ulva Lactuca). IJAPR 2(11): 373-378.
Elsner, H. (1938) Über das Vorkommen von hochwirksamen, die Blutgerinnung hemmenden Stoffen in Meeresalgen. II. Hoppe-Seylers Z Physiol Chem 252(3-4): 196-200.
Elsner, H., Broser, W. Bürgel, E. (1937) Über das Vorkommen von hochwirksamen, die Blutgerinnung hemmenden Stoffen in Rotalgen. HoppeSeylers Z Physiol Chem 246(5-6): 244-247.
Faggio, C., Morabito, M., Minicante, S.A., Piano, G.L., Pagano, M., Genovese, G. (2015) Potential use of polysaccharides from the brown alga Undaria pinnatifida as anticoagulants. Braz Arch Biol Technol 58: 798-804.
Faggio, C., Pagano, M., Dottore, A., Genovese G., Morabito M. (2016) Evaluation of anticoagulant activity of two algal polysaccharides. Nat Prod Res 30: 1934-1937.
Fan, L., Jiang, L., Xu, Y., Zhou, Y., Shen, Y., Xie, W., Long, Z., Zhou, J. (2011) Synthesis and anticoagulant activity of sodium alginate sulfates. Carbohydr Polym 83(4): 1797-1803.
Farias, W.R., Nazareth, R.A., Mourao, P.A.S.(2001) Dual effects of sulfated Dgalactans from the red algae Botryocladia occidentalis preventing thrombosis and inducing platelet aggregation. Thromb Haemost 86(6): 1540-1546.
Farias, W.R., Valente, A.P., Pereira, M.S., Mourao, P.A.S. (2000) 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(38): 29299-29307.
Fernández, P.V., Quintana, I., Cerezo, A.S., Caramelo, J.J., Pol-Fachin, L., Verli, H., Estevez, J.M., Ciancia, M. (2013) Anticoagulant activity of a unique sulfated pyranosic (1→3)-β-l-arabinan through direct interaction with thrombin. J Biol Chem 288(1): 223-233.
Fischer, A. (1931) Inhibition of blood coagulation. Biochem Z 240: 364-380.
Gollin, R.A., Michaclis, R., Waker, D., Adams, S.S. (1965) Process for the preparation of laminarin sulfates. US PATENT 3, 200, 110 A.
Güven, K.C., Aktin, E. (1962) A study on the antilipemic and anticoagulant activities of Phyllophora nervosa (D. C.) Grev. Eczacılık Bülteni 4: 199-206.
Güven, K.C., Aktin, E. (1964) Studies on antilipaemic and anticoagulant properties of the algae collected from Turkish coasts. Bot Mar 7(1-4): 1-3.
Güven, K.C., Aktin, E., Koyuncuoglu, H., Bergisadi, N. (1974a) Lipolytic and hypoglycemic compounds obtained from Cystoseira barbata. J Ag ArzneimittelForsch 24(2): 144-147.
Güven, K.C., Bora, A., Aktin, E., Öker, C., Hatemi, H., Çetin, E.T. (1972) Investigations on Phyllophora nervosa (D. C.) Grev. Bot Mar 15(1): 46-51.
Güven, K.C., Bergişadi, N., Güler, E. (1979a) A modification of Duncombe’s Method and its application to the lipolytic activity assay of heparin. Fett Wiss Technol 81(4): 152-154.
Güven, K.C., Güler, E., Aktin, E., Koyuncuoğlu, H. (1979b) Studies on Pterocladia capillacea (Gmel.) Born et Thur. Part II. In: Marine Algae in Pharmaceutical Science (eds. Hoppe, H. A., Levring, T., Tanaka, Y.) Walter de Gruyter, Berlin, New York, pp 693-710.
Güven, K.C., Güvener, B. (1985a) Metachromatic identification of (iota-,Kappa-, lambda-) carragenans. Bot Mar 28: 221-222.
Güven, K.C., Güvener, B. (1985b) A metachromatic method for identification of alginic acid, agar and carragenan. Fett Wiss Technol 87: 172-176.
Güven, K.C., Kızıl, Z. (1986) Pharmacological studies of Halopytys incurvus (Huds.) Batters (Rhodophyceae). Acta Pharm Turc 28: 47-50.
Güven, K.C., Mutluay, E., Aktin, E., Koyuncuoglu, H. (1975) Chemical and pharmacological investigations on Corallina rubens. Planta Med 27(1): 5-13.
Güven, K.C., Ozsoy, Y., Ulutin, O.N. (1991) Anticoagulant, fibrinolytic and antiaggregant activity of carregeenans and alginic acid. Bot Mar 34(5): 429-432.
Güven, K.C., Ulutin, S.B., Mutluay, E., Ulutin, O.N. (1973) Anticoagulantantithrombin and fibrinolytic actions of extract of marine alga Corallina rubens L. Pathophysiol. Haemost Thromb 2(6): 260-268.
Güven, K. C., Ulutin, S. B., Mutluay, E., Ulutin, O. N. (1974b) Anticoagulant antithrombin and fibrinolytic actions of extract of marine alga Corallina rubens L. Haemostasis 2(6): 260-268.
Haroun-Bouhedja, F., Ellouali, M., Sinquin, C., Boisson-Vidal, C. (2000) Relationship between sulfate groups and biological activities of fucans. Thromb Res 100(5): 453-459.
Hassid, W.Z. (1933) The isolation of a sodium sulfuric acid ester of galactan from Irideae Laminarioides (Rhodophyceae). J Am Chem Soc 55(10): 4163-4167.
Hawkins, W.W., Leonard, V.G. (1958) The physiological activity of laminarin sulphate. Can J Biochem Physiol 36(1): 161-170.
Hawkins, W.W., Leonard, V.G. (1962) Antipeptic and antithrombic properties of carrageenin. J Lab Clin Med 60: 641-648.
Hawkins, W.W., Leonard, V.G. (1963) The antithrombic activity of carrageenin in human blood. Can J Biochem Physiol 41: 1325-1327.
Hawkins, W.W., O’Neill, A.N. (1955) The anticoagulant action in blood of sulphated derivatives of laminarin. Can J Biochem Physiol 33(4): 545-552.
Hayakawa, Y., Hayashi, T., Lee, J.-B., Srisomporn, P., Maeda, M., Ozawa, T., Sakuragawa, N. (2000) Inhibition of thrombin by sulfated polysaccharides isolated from green algae. Biochim Biophys Acta – Prot Struct Mol Enzymol 1543(1): 86-94.
Houck, J.C., Morris, R.K., Lazaro, E.J. (1957) Anticoagulant, lipemia clearing and other effects of anionic polysaccharides extracted from seaweed. Exp Biol Med 96(2): 528-530.
Howell, W.H., Holt, L.E. (1918) Two new factors in blood coagulation-heparin and pro-antithrombin. Am J Physiol 47: 328-341.
Ibrahim, E.A., Aly, H.F., and El-Baz, F.K. (2016) Anticoagulant and antiinflammatory potentials of some Egyptian marine algae. Int J Pharma Bio Sci Blood Coagul Fibrinolysis 7(2): 89-94.
Irhimeh, M.R., Fitton, J.H., Lowenthal, R.M. (2009) Pilot clinical study to evaluate the anticoagulant activity of fucoidan. Blood Coagulation & Fibrinolysis 20(7): 607-610.
Jung, W.-K., Athukorala, Y., Lee, Y.-J., Cha, S. H., Lee, C.-H., Vasanthan, T., Choi, K.-S., Yoo, S.-H., Kim, S.-K., Jeon, Y.-J. (2007) Sulfated polysaccharide purified from Ecklonia cava accelerates antithrombin III-mediated plasma proteinase inhibition. J Appl Phycol 19(5): 425-430.
Jurd, K.M., Rogers, D.J., Blunden, G., McLellan, D.S. (1995) Anticoagulant properties of sulphated polysaccharides and a proteoglycan from Codium fragile ssp. atlanticum. J Appl Phycol 7(4): 339.
Kang, S.-R., Choi, J.-H., Kim, D.-W., Park, S.-E., Sapkota, K., Kim, S., Kim, S.-J. (2016) A bifunctional protease from green alga Ulva pertussa with anticoagulant properties: partial purification and characterization. J Appl Phycol 28(1): 599-607.
Karaki, N., Sebaaly, C., Chahine, N., Faour, T., Zinchenko, A., Rachid, S., Kanaan, H. (2013) The antioxidant and anticoagulant activities of polysaccharides isolated from the brown algae Dictyopteris polypodioides growing on the Lebanese coast. J Appl Pharm Sci 3(2): 43-51.
Kim, K.J., Lee, O.H., Lee, H.H., Lee, B.Y. (2010) A 4-week repeated oral dose toxicity study of fucoidan from the sporophyll of Undaria pinnatifida in Sprague-Dawley rats. Toxicol 267(1-3): 154-158.
Kindness, G., Long, W.F., Williamson, F.B. (1979a) Enhancement of antithrombin III activity by carrageenans. Thromb Res 15(1): 49-60.
Kindness, G., Long, W.F., Williamson, F.B., Boyd, J. (1979b) Effects of carrageenans on the aggregation of human blood platelets. Thromb Res 15(1-2): 3-15.
Kitamura, K., Matsuo, M., Yasui, T. (1991) Fucoidan from brown seaweed Laminaria angustata var. longissima. Agric Biol Chem 55(2): 615-616.
Kolender, A.A., Pujol, C.A., Damonte, E.B., Matulewicz, M.C., Cerezo, A.S. (1997) The system of sulfated alpha-(1–>3)-linked D-mannans from the red seaweed Nothogenia fastigiata: structures, antiherpetic and anticoagulant properties. Carbohydr Res 304(1): 53-60.
Kraan, S. (2012) Algal polysaccharides, novel applications and outlook. In: Carbohydrates –Comprehensive Studies on Glycobiology and Glycotechnology, (ed. Chang, C-F.), InTech, Rijeka, pp. 489-532.
Kuznetsova, T.A., Besednova, N.N., Mamaev, A.N., Momot, A.P., Shevchenko, N.M., Zvyagintseva, T.N. (2003) Anticoagulant activity of fucoidan from brown algae Fucus evanescens of the Okhotsk Sea. Bull Exp Biol Med 136(5): 471-473.
Kylin, H. (1913) Zur biochemie der meeresalgen. H-S. Z. Physiol. Chem. 83(3): 171-197.
Lee, S.-H., Athukorala, Y., Lee, J.-S., Jeon, Y.-J. (2008) Simple separation of anticoagulant sulfated galactan from marine red algae. J Appl Phycol 20(6): 1053-1059.
Li, N., Mao, W., Yan, M., Liu, X., Xia, Z., Wang, S., Xiao, B., Chen, C., Zhang, L., Cao, S. (2015) Structural characterization and anticoagulant activity of a sulfated polysaccharide from the green alga Codium divaricatum. Carbohydr Polym 121: 175-182.
Li, B., Zhao, R.-X., Wei, X.-J. (2008) Anticoagulant activity of fucoidan from Hizikia fusiforme. Agro Food Industry Hi-Tech 19(1): 22-24.
Lison, L. (1935) Etudes sur la metachromasie colorants metachromatiques et substances chromotropes. Arch Biol 46: 599-668.
Liu, J., Zhan, X., Wan, J., Wang, Y., Wang, C. (2015) Review for carrageenanbased pharmaceutical biomaterials: favourable physical features versus adverse biological effects. Carbohydr Polym 121: 27-36.
Maeda, M., Uehara, T., Harada, N., Sekiguchi, M., Hiraoka, A. (1991) Heparinoid-active sulphated polysaccharides from Monostroma nitidum and their distribution in the Chlorophyta. Phytochem 30(11): 3611-3614.
Majdoub, H., Mansour, M.B., Chaubet, F., Roudesli, M.S., Maaroufi, R.M. (2009) Anticoagulant activity of a sulfated polysaccharide from the green alga Arthrospira platensis. Biochim Biophys Acta 1790(10): 1377-1381.
Mao, W.-J., Fang, F., Li, H.-Y., Qi, X.-H., Sun, H.-H., Chen, Y., Guo, S.-D. (2008) Heparinoid-active two sulfated polysaccharides isolated from marine green algae Monostroma nitidum. Carbohydr Polym 74(4): 834-839.
Mao, W., Li, H., Li, Y., Zhang, H., Qi, X., Sun, H., Chen, Y., Guo, S. (2009) Chemical characteristic and anticoagulant activity of the sulfated polysaccharide isolated from Monostroma latissimum (Chlorophyta). Int J Biol Macromol 44(1): 70-74.
Mao, W., Zang, X., Li, Y., Zhang, H. (2006) Sulfated polysaccharides from marine green algae Ulva conglobata and their anticoagulant activity. J Appl Phycol 18(1): 9-14.
Margolis, J. (1958) The kaolin clotting time a rapid one-stage method for diagnosis of coagulation defects. J Clin Pathol 11(5): 406-409.
Matsubara, K., Matsuura, Y., Bacic, A., Liao, M., Hori, K., Miyazawa, K. (2001) Anticoagulant properties of a sulfated galactan preparation from a marine green alga, Codium cylindricum. Int J Biol Macromol 28(5): 395-399.
Matsubara, K., Matsuura, Y., Hori, K., Miyazawa, K. (2000) An anticoagulant proteoglycan from the marine green alga, Codium pugniformis. J Appl Phycol 12(1): 9.
Mauray, S., Sternberg, C., Theveniaux, J., Millet, J., Sinquin, C., TaponBretaudiere, J., Fischer, A. M. (1995) Venous antithrombotic and anticoagulant activities of a fucoidan fraction. Thromb Haemost 74(5): 1280-1285.
McLean, J. (1916) The tromboplastic action of cephalin. Am J Physiol 41: 250-257.
McMillan, R.M., MacIntyre, D.E., Gordon, J.L. (1979) Stimulation of human platelets by carrageenans. J Pharm Pharmacol 31(3): 148-152.
Melo, F.R., Pereira, M.S., Foguel, D., Mourao, P.A.S. (2004) Antithrombinmediated anticoagulant activity of sulfated polysaccharides: different mechanisms for heparin and sulfated galactans. J Biol Chem 279(20): 20824-20835.
Millet, J., Jouault, S.C., Mauray, S., Theveniaux, J., Sternberg, C., Boisson Vidal, C., Fischer, A.M. (1999) Antithrombotic and anticoagulant activities of a low molecular weight fucoidan by the subcutaneous route. Thromb Haemost 81(3): 391-395.
Molho, D., Cotte, J. (1951) Blood coagulation and anticoagulants. II. Sulfuric esters of alginates: preparation and action in vitro on the factors involved in coagulation. Bull Soc Chim Biol 33(3-4): 312-320.
Mookerjea, S., Hawkins, W.W. (1958) The antilipaemic activity of laminarin sulphate. Can J Biochem Physiol 36(3): 261-268.
Mourao, P.A. (2004) Use of sulfated fucans as anticoagulant and antithrombotic agents: future perspectives. Curr Pharm Des 10(9): 967-981.
Murata, K. (1961) Effects of carrageenin on serum lipids and atherosclerosis in rabbits. Nature 191: 189-190.
Murata, K. (1962) The effects of sulfated polysaccharides obtained from seaweeds on experimental atherosclerosis. J Gerontol 17: 30-36.
Nardella, A., Chaubet, F., Boisson-Vidal, C., Blondin, C., Durand, P., Jozefonvicz, J. (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. Carbohydr Res 289: 201-208.
Nishino, T., Fukuda, A., Nagumo, T., Fujihara, M., Kaji, E. (1999) Inhibition of the generation of thrombin and factor xa by a fucoidan from the brown seaweed Ecklonia kurome. Thromb Res 96(1): 37-49.
Nishino, T., Nishioka, C., Ura, H., Nagumo, T. (1994) Isolation and partial characterization of a noval amino sugar-containing fucan sulfate from commercial Fucus vesiculosus fucoidan. Carbohydr Res 255: 213-224.
Nishino, T., Yokoyama, G., Dobashi, K., Fujihara, M., Nagumo, T. (1989) Isolation, purification, and characterization of fucose-containing sulfated polysaccharides from the brown seaweed Ecklonia kurome and their bloodanticoagulant activities. Carbohydr Res 186(1): 119-129.
O’Neill, A.N. (1955) Sulphated derivatives of laminarin. Can J Chem 33(6): 1097-1101.
Pengzhan, Y., Ning, L., Xiguang, L., Gefei, Z., Quanbin, Z., Pengcheng, L. (2003) Antihyperlipidemic effects of different molecular weight sulfated polysaccharides from Ulva pertusa (Chlorophyta). Pharmacol Res 48(6): 543-549.
Percival, E., McDowell, R. (1967) Chemistry and Enzymology of Marine Algal Polysaccharides. Academic Press London, New York.
Pereira, M.G., Benevides, N.M., Melo, M.R., Valente, A.P., Melo, F.R., Mourao, P.A. (2005) 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(12): 2015-2023.
Pereira, M.S., Mulloy, B., Mourao, P.A. (1999) Structure and anticoagulant activity of sulfated fucans. Comparison between the regular, repetitive, and linear fucans from echinoderms with the more heterogeneous and branched polymers from brown algae. J Biol Chem 274(12): 7656-7667.
Pereira, M.S., Melo, F.R., Mourão, P.A.S. (2002a) Is there a correlation between structure and anticoagulant action of sulfated galactans and sulfated fucans? Glycobiology 12(10): 573-580.
Pereira, M.S., Vilela-Silva, A.-C.E.S., Valente, A.-P., Mourão, P.A.S. (2002b) A 2-sulfated, 3-linked α-l-galactan is an anticoagulant polysaccharide. Carbohydr Res 337(21-23): 2231-2238.
Pitney, W.R., Dacie, J.V. (1953) A simple method of studying the generation of thrombin in recalcified plasma: Application in the investigation of haemophilia. J Clin Pathol 6(1): 9-14.
Pulsawat, W., Tongmalee, S. (2014) Synthesis and Anticoagulant activity of Sulfated alginate. KKU Res J 19(Suppl): 60-66.
Pushpamali, W.A., Nikapitiya, C., Zoysa, M.D., Whang, I., Kim, S. J., Lee, J. (2008) Isolation and purification of an anticoagulant from fermented red seaweed Lomentaria catenata. Carbohydr Polym 73(2): 274-279.
Qi, X., Mao, W., Chen, Y., Chen, Y., Zhao, C., Li, N., Wang, C. (2013) Chemical characteristics and anticoagulant activities of two sulfated polysaccharides from Enteromorpha linza (Chlorophyta). J Ocean Uni China 12(1): 175-182.
Qi, X., Mao, W., Gao, Y., Chen, Y., Chen, Y., Zhao, C., Li, N., Wang, C., Yan, M., Lin, C., Shan, J. (2012) Chemical characteristic of an anticoagulant-active sulfated polysaccharide from Enteromorpha clathrata. Carbohydr Polym 90(4): 1804-1810.
Quick, A.J. (1945) On the quantitative estimation of prothrombin. Am J Clin Pathol 15(12): 560-566.
Ren, D.L., Noda, H., Amano, H., Nishino, T., Nishizawa, K. (1994) Study on antihypertensive and antihyperlipidemic effects of marine-algae. Fish Sci 60(1): 83-88.
Rocha, H.A., Moraes, F.A., Trindade, E.S., Franco, C.R., Torquato, R.J., Veiga, S.S., Valente, A.P., Mourao, P.A., Leite, E.L., Nader, H.B., Dietrich, C.P. (2005) Structural and hemostatic activities of a sulfated galactofucan from the brown alga Spatoglossum schroederi. An ideal antithrombotic agent? J Biol Chem 280(50): 41278-41288.
Rodrigues, J.A.G., Vanderlei, E.D.S.O., Bessa, É.F., Magalhães, F.D.A., Paula, R.C.M.D., Lima, V., Benevides, N.M.B. (2011) Anticoagulant activity of a sulfated polysaccharide isolated from the green seaweed Caulerpa cupressoides. Braz Arch Biol Techn 54: 691-700.
Rogers, D.J., Jurd, K.M., Blunden, G., Paoletti, S., Zanetti, F. (1990) Anticoagulant activity of a proteoglycan in extracts of Codium fragile ssp. atlanticum. J Appl Phycol 2(4): 357-361.
Schimpf, K., Lenhard, J., Schaaf, G. (1969) The influence of the polysaccharide carrageenin on the clotting mechanism of the blood in the rabbit in vitro and in vivo. Thromb Diath Haemorrh 21(3): 524-33.
Schuler, W., Springer, G.F. (1957) Experimentelle antilipämiewirkung von fucoidin. Naturwissenschaften 44(8): 265-265.
Schwartz, H.J., Kellermeyer, R.W. (1969) Carrageenan and delayed hypersensitivity. II. Activation of Hageman factor by carrageenan and its possible significance. Proc Soc Exp Biol Med 132(3): 1021-1024.
Selim, S., Amin, A., Hassan, S., Hagazey, M. (2015) Antibacterial, cytotoxicity and anticoagulant activities from Hypnea esperi and Caulerpa prolifera marine algae. Pak J Pharm Sci 28(2): 525-530.
Sen, A.K., Das, A.K., Banerji, N., Siddhanta, A.K., Mody, K.H., Ramavat, B. K., Chauhan, V. D., Vedasiromoni, J. R., Ganguly, D. K. (1994) A new sulfated polysaccharide with potent blood anti-coagulant activity from the red seaweed Grateloupia indica. Int J Biol Macromol 16(5): 279-280.
Shanmugam, M., Mody, K.H., Oza, R.M., Ramavat, B.K. (2001a) Blood anticoagulant activity of a green marine alga Codium dwarkense (Codiaceae, Chlorophyta) in relation to its growth stages. Ind J Geo-Mar Sci 30(1): 49-52.
Shanmugam, M., Mody, K. H., Ramavat, B. K., Murthy, A. S. K., Siddhanta, A. K. (2002) Screening of Codiacean algae (Chlorophyta) of the Indian coasts for blood anticoagulant activity. Ind J Geo-Mar Sci 31(1): 33-38.
Shanmugam, M., Mody, K.H., Siddhanta, A.K. (2001b) Blood anticoagulant sulphated polysaccharides of the marine green algae Codium dwarkense (Boergs.) and C. tomentosum (Huds.) Stackh. Ind J Exp Biol 39: 365-370.
Shanmugam, M., Ramavat, B. K., Mody, K. H., Oza, R. M., Tewari, A. (2001c) Distribution of heparinoid-active sulphated polysaccharides in some Indian marine green algae. Ind J Geo-Mar Sci 30(4): 222-227.
Shonima, G. M., Jiji, T., Pratheesh, P. T., Kurup, G. M. (2012) Ex vivo anticoagulant activity of the polysaccharide isolated form Ulva fasciata. Int J LifeSc Bt and Pharm Res 1(2): 194-197.
Shore, B., Nichols, A.V., Freeman, N.K. (1953) Evidence for lipolytic action by human plasma obtained after intravenous administration of heparin. Proc Soc Exp Biol Med 83(2): 216-220.
Siddhanta, A.K., Shanmugam, M., Mody, K.H., Goswami, A.M., Ramavat, B.K. (1999) Sulphated polysaccharides of Codium dwarkense Boergs. from the west coast of India: chemical composition and blood anticoagulant activity. Int J Biol Macromol 26(2-3): 151-154.
Silva, T.M., Alves, L.G., de Queiroz, K.C., Santos, M.G., Marques, C.T., Chavante, S.F., Rocha, H.A., Leite, E.L. (2005) Partial characterization and anticoagulant activity of a heterofucan from the brown seaweed Padina gymnospora. Braz J Med Biol Res 38(4): 523-533.
Soeda, S., Sakaguchi, S., Shimeno, H., Nagamatsu, A. (1992) Fibrinolytic and anticoagulant activities of highly sulfated fucoidan. Biochem Pharmacol 43(8): 1853-1858.
Springer, G.F., Wurzel, H.A., McNeal, G.M., Ansell, N. J., Doughty, M.F. (1957) Isolation of anticoagulant fractions from crude fucoidin. Exp Biol Med 94(2): 404-409.
Sun, Y., Chen, X., Liu, S., Yu, H., Li, R., Wang, X., Qin, Y., Li, P. (2018) Preparation of low molecular weight Sargassum fusiforme polysaccharide and its anticoagulant activity. Chin J Oceanol Limn 36(3): 882-891.
Takemori, S. (1957a) Isolation and composition of some seaweed polysaccharide sulfates and their anticoagulant activity I. Hirasaki Igaku 8: 749-759.
Takemori, S. (1957b) Isolation and composition of some seaweed polysaccharide sulfates and their anticoagulant activity II. Hirasaki Igaku 8: 760-769.
Trento, F., Cattaneo, F., Pescador, R., Porta, R., Ferro, L. (2001) Antithrombin activity of an algal polysaccharide. Thromb Res 102(5): 457-465.
Uehara, T., Takeshita, M., Maeda, M. (1992) Studies on anticoagulant-active arabinan sulfates from the green alga, Codium latum. Carbohydr Res 235: 309-311.
Ushakova, N.A., Morozevich, G.E., Ustyuzhanina, N.E., Bilan, M.I., Usov, A.I., Nifantiev, N.E., Preobrazhenskaya, M.E. (2009) Anticoagulant activity of fucoidans from brown algae. Biochem (Moscow) 3(1): 77-83.
Ustyuzhanina, N.E., Bilan, M.I., Gerbst, A.G., Ushakova, N.A., Tsvetkova, E.A., Dmitrenok, A.S., Usov, A.I., Nifantiev, N.E. (2016) Anticoagulant and antithrombotic activities of modified xylofucan sulfate from the brown alga Punctaria plantaginea. Carbohydr Polym 136: 826-833.
Usui, T., Asari, K., Mizuno, T. (1980) Isolation of highly purified “fucoidan” from Eisenia bicyclis and its anticoagulant and antitumor activities. Agric Biol Chem 44(8): 1965-1966.
Wang, X., Zhang, Z., Yao, Z., Zhao, M., Qi, H. (2013) Sulfation, anticoagulant and antioxidant activities of polysaccharide from green algae Enteromorpha linza. Int J Biol Macromol 58: 225-230.
Wang, J., Zhang, Q., Zhang, Z., Song, H., Li, P. (2010) Potential antioxidant and anticoagulant capacity of low molecular weight fucoidan fractions extracted from Laminaria japonica. Int J Biol Macromol 46(1): 6-12.
Wijesinghe, W.A.J.P., Athukorala, Y., Jeon, Y.J. (2011) Effect of anticoagulative sulfated polysaccharide purified from enzyme-assistant extract of a brown seaweed Ecklonia cava on Wistar rats. Carbohydr Res 86(2): 917- 921.
Winter, C.A., Risley, E.A., Nuss, G.W. (1962) Carrageenin-induced edema in hind paw of the rat as an assay for antiinflammatory drugs. Exp Biol Med 111(3): 544-547.
Yoon, S. J., Pyun, Y.R., Hwang, J.K., Mourao, P.A. (2007) A sulfated fucan from the brown alga Laminaria cichorioides has mainly heparin cofactor IIdependent anticoagulant activity. Carbohydr Res 342(15): 2326-2330.
Yu, Y., Li, Y.P., Du, C.Y., Mou, H.J., Wang, P. (2017) Compositional and structural characteristics of sulfated polysaccharide from Enteromorpha prolifera. Carbohydr Polym 165: 221-228.
Yuan, Y., Xu, X., Jing, C., Zou, P., Zhang, C., Li, Y. (2018) Microwave assisted hydrothermal extraction of polysaccharides from Ulva prolifera: Functional properties and bioactivities. Carbohydr Polym 181: 902-910.
Zha, X.Q., Xiao, J.J., Zhang, H.N., Wang, J.H., Pan, L.H., Yang, X.F., Luo, J.P. (2012) Polysaccharides in Laminaria japonica (LP): Extraction, physicochemical properties and their hypolipidemic activities in diet-induced mouse model of atherosclerosis. Food Chem 134: 244-252.
Zhang, H., Mao, W., Fang, F., Li, H., Sun, H., Chen, Y., Qi, X. (2008) Chemical characteristics and anticoagulant activities of a sulfated polysaccharide and its fragments from Monostroma latissimum. Carbohydr Res 71(3): 428-434.
Zhang, Z., Till, S., Jiang, C., Knappe, S., Reutterer, S., Scheiflinger, F., Szabo, C.M., Dockal, M. (2014) Structure-activity relationship of the pro- and anticoagulant effects of Fucus vesiculosus fucoidan. Thromb Haemost 111(3): 429-437.
Zhang, Z., Zhang, Q., Wang, J., Song, H., Zhang, H., Niu, X. (2010) Regioselective syntheses of sulfated porphyrans from Porphyra haitanensis and their antioxidant and anticoagulant activities in vitro. Carbohydr Res 79(4): 1124-1129.
Zhao, T., Zhang, Q., Qi, H., Zhang, H., Niu, X., Xu, Z., Li, Z. (2006) Degradation of porphyran from Porphyra haitanensis and the antioxidant activities of the degraded porphyrans with different molecular weight. Int J Biol Macromol 38(1): 45-50.
Zúñiga, E.A., Matsuhiro, B., Mejías, E. (2006) Preparation of a low-molecular weight fraction by free radical depolymerization of the sulfated galactan from Schizymenia binderi (Gigartinales, Rhodophyta) and its anticoagulant activity. Carbohydr Polym 66(2): 208-215.