Structural Features and Anti-coagulant Activity of the Sulphated Polysaccharide SPS-CF from a Green Alga Capsosiphon fulvescens

Marine Biotechnology

Volumn 17, Issue 6, 2015, Pages 718-735

  Synytsya, Andriy ^a   Choi, Doo Jin ^b   Pohl, Radek ^c   Na, Ye Seul ^b   Capek, Peter ^d   Lattová, Erika ^d   Taubner, Tomáš ^a   Choi, Ji Won ^b   Lee, Chang Won ^b   Park, Jae Kweon ^e   Kim, Woo Jung ^b   Kim, Sung Min ^b   Lee, Jisun ^b   Park, Yong Il ^b  

^a INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^b The Catholic University of Korea   (South Korea)

^c INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^d INSTITUTE OF CHEMISTRY   (Slovakia)

^e Gachon University   (South Korea)

Author keywords

Alga Maesaengi (Capsosiphon fulvescens); Anti coagulant activity; Monosaccharide composition; Structure; Ulvan

Indexed keywords

COAGULATION; DESORPTION; ELECTRODEPOSITION; ELECTROSPRAY IONIZATION; GALLIUM ALLOYS; GAS CHROMATOGRAPHY; GLUCOSE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IONIZATION OF GASES; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE; SPECTROMETRY; STRUCTURE (COMPOSITION); SUGARS; SULFUR COMPOUNDS; THIN LAYER CHROMATOGRAPHY; XYLOSE;

ACTIVATED PARTIAL THROMBOPLASTIN TIME; ANTICOAGULANT ACTIVITIES; ELECTROSPRAY IONIZATION MASS SPECTROMETRY; HIGH-PERFORMANCE ANION-EXCHANGE CHROMATOGRAPHY; MATRIX-ASSISTED LASER DESORPTION/IONIZATION MASS SPECTROMETRY; MONOSACCHARIDE COMPOSITION; NUCLEAR MAGNETIC RESONANCE(NMR); ULVAN;

CHROMATOGRAPHY;

ANTICOAGULANT; BIOCHEMICAL COMPOSITION; GREEN ALGA; ION EXCHANGE; IONIZATION; POLYSACCHARIDE; SULFATE;

KOREA;

ALGAE; CAPSOSIPHON FULVESCENS; CHLOROPHYTA;

ANTICOAGULANT AGENT; MANNAN; MONOSACCHARIDE;

CHEMISTRY; FLAME IONIZATION DETECTION; GAS CHROMATOGRAPHY; GREEN ALGA; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARTIAL THROMBOPLASTIN TIME; THIN LAYER CHROMATOGRAPHY; THROMBIN TIME;

ANTICOAGULANTS; CHLOROPHYTA; CHROMATOGRAPHY, GAS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, THIN LAYER; FLAME IONIZATION; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MANNANS; MONOSACCHARIDES; PARTIAL THROMBOPLASTIN TIME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; THROMBIN TIME;

EID: 84946495405     PISSN: 14362228     EISSN: 14362236     Source Type: Journal    
DOI: 10.1007/s10126-015-9643-y     Document Type: Article

References (71)

1. Alekseyenko TV, Zhanayeva SY, Venediktova AA, Zvyagintseva TN, Kuznetsova TA, Besednova NN, Korolenko TA (2007) Antitumor and antimetastatic activity of fucoidan, a sulphated polysaccharide isolated from the Okhotsk Sea Fucus evanescens brown alga. Bull Exp Biol Med 143:730–732
2. Andersson LO (1976) Anticoagulant properties of heparin fractionated by affinity chromatography on matrix-bound antithrombin III and by gel filtration. Thromb Res 9:575–580
3. Bai X, Esko JD (1996) An animal cell mutant defective in heparan sulphate hexuronic acid 2-O-sulphation. J Biol Chem 271:17711–17717
4. BeMiller JN (1967) Acid-catalized hydrolisis of glycosides. Adv Carbohydr Chem 22:25–108
5. Berteau O, Mulloy B (2003) Sulphated fucans, fresh perspectives: structures, functions, and biological properties of sulphated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology 13:29R–40R
6. Blumenkrantz N, Asboe-Hansen O (1973) A new method for quantitative determination of uronic acid. Anal Biochem 54:484–489
7. Boisson-Vidal FC, Chevolot L, Sinquin C, Theveniaux JM, Sternberg C, Mulloy B, Fischer AM (2000) Relationship between antithrombotic activities of fucans and their structure. Drug Delivery Res 51:216–224
8. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
9. Chambers RE, Clamp JR (1971) An assessment of methanolysis and other factors used in the analysis of carbohydrate-containing materials. Biochem J 125:1009–1018
10. Chevolot L, Foucault A, Chaubet F, Kervarec N, Sinquin C, Fisher AM, Boisson-Vidal C (1999) Further data on the structure of brown seaweed fucans: relationships with anticoagulant activity. Carbohydr Res 319:154–165
11. Choi JI, Raghavendran HR, Sung NY, Kim JH, Chun BS, Ahn DH, Choi HS, Kang KW, Lee JW (2010) Effect of fucoidan on aspirin-induced stomach ulceration in rats. Chem Biol Interact 183:249–254
12. Collén PN, Sassi JF, Rogniaux H, Marfaing H, Helbert W (2011) Ulvan lyases isolated from the flavobacteria Persicivirga ulvanivorans are the first members of a new polysaccharide lyase family. J Biol Chem 286:42063–42071
13. Combo AMM, Aguedo M, Goffin D, Wathelet B, Paquot M (2012) Enzymatic production of pectic oligosaccharides from polygalacturonic acid with commercial pectinase preparations. Food Bioprod Proces 90:588–596
14. Dantas L, Courtois J, Courtois B, Seguin JP, Gey C, Heyraud A (1994) NMR spectroscopic investigation of oligoglucuronates prepared by enzymic hydrolysis of a (1 → 4)-β-d-glucuronan. Carbohydr Res 265:303–310
15. Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, Ulvskov P, Willats WGT (2012) The cell walls of green algae: a journey through evolution and diversity. Front Plant Sci 3:1–7
16. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
17. Fan JQ, Namiki Y, Matsuoka K, Lee YC (1994) Comparison of acid hydrolytic conditions for Asn-linked oligosaccharides. Anal Biochem 219:375–378
18. Fischer KG (2007) Essentials of anticoagulation in hemodialysis. Hemodial Int 11:178–189
19. Fukuyama Y, Ciancia M, Nonami H, Cerezo AS, Erra-Balsells R, Matulewicz MC (2002) Matrix-assisted ultraviolet-laser desorption/ionization and electrospray ion ionization time-of-flight mass spectrometry of sulfated neocarrabiose oligosaccharides. Carbohydr Res 337:1553–1562
20. Go H, Hwang HJ, Nam TJ (2011) Polysaccharides from Capsosiphon fulvescens stimulate the growth of IEC-6 cells by activating the MAPK signaling pathway. Mar Biotechnol (NY) 13:433–440
21. Gomes AM, Kozlowski EO, Pomin VH, de Barros CM, Zaganeli JL, Pavão MSG (2010) Unique extracellular matrix heparan sulphate from the bivalve Nodipecten nodosus (Linnaeus, 1758) safely inhibits arterial thrombosis after photochemically induced endothelial lesion. J Biol Chem 285:7312–7323
22. Hahnenberger R, Jakobson AM (1991) Antiangiogenic effect of sulphated and non-sulphated glycosaminoglycans and polysaccharides in the chick-embryo chorioallantoic membrane. Glycoconjugate J 8:350–353
23. Honda S, Akao E, Suzuki S, Okuda M, Kakehi K, Nakamura J (1989) High-performance liquid chromatography of reducing carbohydrates as strongly ultraviolet-absorbing and electrochemically sensitive 1-phenyl-3-methyl-5-pyrazolone derivatives. Anal Biochem 180:351–357
24. Hwang EK, Amano H, Park CS (2008a) Assessment of the nutritional value of Capsosiphon fulvescens (Chlorophyta): developing a new species of marine macroalgae for cultivation in Korea. J Appl Phycol 20:147–151
25. Hwang HJ, Kwon MJ, Kim IH, Nam TJ (2008b) The effect of polysaccharide extracted from the marine alga Capsosiphon fulvescens on ethanol administration. Food Chem Toxicol 46:2653–2657
26. Jing W, Quanbin Z, Zhongshan Z, Zhien L (2008) Antioxidant activity of sulphated polysaccharide fractions extracted from Laminaria japonica. Int J Biol Macromol 42:127–132
27. Karnjanapratum S, You SG (2011) The effects of chemical modifications on water extractable polysaccharides from Capsosiphon fulvescens on biological activities. 12th ASEAN Food Conf, 16–18 June, 2011. BITEC Bangna, Bangkok, Thailand, PA-312
28. Karnjanapratum S, Tabarsa M, Cho ML, You SG (2012) Characterization and immunomodulatory activities of sulfated polysaccharides from Capsosiphon fulvescens. Int J Biol Macromol 51:720–729
29. Kim WJ, Kim SM, Kim HG, Oh HR, Lee KB, Lee YK, Park YI (2007) Purification and anticoagulant activity of a fucoidan from Korean Undaria pinnatifida sporophyll. Algae 22:247–252
30. Kim WJ, Koo YK, Jung MK, Moon HR, Kim SM, Synytsya A, Yun-Choi HS, Kim YS, Park JK, Park YI (2010) Anticoagulating activities of low-molecular weight fuco-oligosaccharides prepared by enzymatic digestion of fucoidan from the sporophyll of Korean Undaria pinnatifida. Arch Pharmac Res 33:125–131
31. Kinoshita-Toyoda A, Yamada S, Haslam SM, Khoo KH, Sugiura M, Morris HR, Dell A, Sugahara K (2004) Structural determination of five novel tetrasaccharides containing 3-O-sulphated d-glucuronic acid and two rare oligosaccharides containing a β-d-glucose branch isolated from squid cartilage chondroitin sulphate E. Biochemistry 43:11063–11074
32. Kusche M, Lindahl U (1990) Biosynthesis of heparin. O-Sulphation of d-glucuronic acid units. J Biol Chem 265:15403–15409
33. Kwon MJ, Nam TJ (2007) A polysaccharide of the marine alga Capsosiphon fulvescens induces apoptosis in AGS gastric cancer cells via an IGF-IR-mediated PI3K/Akt pathway. Cell Biol Int 31:768–775
34. Lahaye M (1998) NMR spectroscopic characterisation of oligosaccharides from two Ulva rigida ulvan samples (Ulvales, Chlorophyta) degraded by a lyase. Carbohydr Res 314:1–12
35. Lahaye M, Ray B (1996) Cell-wall polysaccharides from the marine green alga Ulva “rigida” (Ulvales, Chlorophyta)—NMR analysis of ulvan oligosaccharides. Carbohydr Res 283:161–173
36. Lahaye M, Robic A (2007) Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765–1774
37. Lahaye M, Brunel M, Bonnin E (1997) Fine chemical structure analysis of oligosaccharides produced by an ulvan-lyase degradation of the water-soluble cell-wall polysaccharides from Ulva sp. (Ulvales, Chlorophyta). Carbohydr Res 304:325–333
38. Lahaye M, Inizan F, Vigouroux J (1998) NMR analysis of the chemical structure of ulvan and of ulvan-boron complex formation. Carbohydr Polym 36:239–249
39. 13C NMR spectroscopic characterisation of ulvans from Ulva (Ulvales, Chlorophyta). J Appl Phycol 11:1–7
40. Lee HG, Cowman MK (1994) An agarose gel electrophoretic method for analysis of hyaluronan molecular weight distribution. Anal Biochem 219:278–287
41. Lee JB, Hayashi K, Hashimoto M, Nakano T, Hayashi T (2004) Novel antiviral fucoidan from sporophyll of Undaria pinnatifida (Mekabu). Chem Pharm Bull 52:1091–1094
42. Li B, Lu F, Wei X, Zhao R (2008) Fucoidan: structure and bioactivity. Molecules 13:1671–1695
43. Maraganore JM, Chao B, Joseph ML, Jablonski J, Ramachandran KL (1989) Anticoagulant activity of synthetic hirudin peptides. J Biol Chem 264:8692–8698
44. Matsubara K, Matsuura Y, Bacic A, Liao M, Hori K, Miyazawa K (2001) Anticoagulant properties of a sulphated galactan preparation from a marine green alga, Codium cylindricum. Int J Biol Macromol 28:395–399
45. Mourao PA, Pereira MS (1999) Searching for alternatives to heparin: sulphated fucans from marine invertebrates. Trends Cardiovascul Med 9:225–232
46. Na YS, Kim WJ, Kim SM, Park JK, Lee SM, Kim SO, Synytsya A, Park YI (2010) Purification, characterization and immunostimulating activity of water-soluble polysaccharide isolated from Capsosiphon fulvescens. Int Immunopharmacol 10:364–370
47. Nam TJ, Kwon MJ (2007a) Hot-water extracting matter of Capsosiphon fulvescens and anticancer drugs. Pukyong National University Industry, Academic Cooperation Foundation. March 2007, WO 2007/035030
48. Nam TJ, Kwon MJ (2007b) Anticancer food edible at any season comprising crude polysaccharides extracted from Capsosiphon fulvescens capable of inhibiting growth of cancer cells, especially stomach cancer cells and large intestine cancer cells without toxicity. Pukyong National University Industry, University Cooperation Foundation. April 2007, KR 1020050088623
49. Nam TJ, Kwon MJ (2007c) Solid matter of Capsosiphon fulvescens and serum lipid improving and liver protecting agent comprising the same having blood lipid metabolism improving effect and hepatotoxicity protecting effect. Pukyong National University Industry, University Cooperation Foundation. October 2007, KR 1020050088622
50. Nam TJ, Kwon MJ, Hwang HJ (2008) Saccharide with gastric mucous membrane injury inhibiting activity derived from a hot water extract of Capsosiphon fulvescens and a food for inhibiting gastritis or gastric bleeding comprising the same. Pukyong National University, Industry-University Cooperation Foundation. June 2008, KR 1020070043584
51. Park YI, Wood HA, Lee YC (1999) Monosaccharide compositions of Danaus plexippus (monarch butterfly) and Trichoplusia ni (cabbage looper) egg glycoproteins. Glycoconjugate J 16:629–638
52. 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 90:1804–1810
53. Quemener B, Lahaye M, Bobin-Dubigeon C (1997) Sugar determination in ulvans by a chemical-enzymatic method coupled to high performance anion exchange chromatography. J Appl Phycol 9:179–188
54. Ragazzi M, Ferro DR, Provasoli A, Pumilia P, Cassinari A, Torri G, Guerrini M, Casu B, Nader HB, Dietrich CP (1993) Conformation of the unsaturated uronic acid residues of glycosamtnoglycan disaccharides. J Carbohydr Chem 12:523–535
55. Ray B (2006) Polysaccharides from Enteromorpha compressa: isolation, purification and structural features. Carbohydr Polym 66:408–416
56. Ray B, Lahaye M (1995a) Cell-wall polysaccharides from the marine green alga Ulva rigida (Ulvales, Chlorophyta). Extraction and chemical composition. Carbohydr Res 274:251–261
57. Ray B, Lahaye M (1995b) Cell-wall polysaccharides from the marine green alga Ulva rigida (Ulvales, Chlorophyta). Chemical structure of ulvan. Carbohydr Res 274:313–318
58. Razi N, Kreuger J, Lay L, Russo G, Panza L, Lindahl B, Lindahl U (1995) Identification of O-sulphate substituents on d-glucuronic acid units in heparin-related glycosaminoglycans using novel synthetic disaccharide standards. Glycobiology 5:807–811
59. Robic A, Bertrand D, Sassi JF, Lerat Y, Lahaye JM (2009) Determination of the chemical composition of ulvan, a cell wall polysaccharide from Ulva spp. (Ulvales, Chlorophyta) by FT-IR and chemometrics. Appl Phycol 21:451–456
60. Shanmugam M, Mody KH (2000) Heparinoid-active sulphated polysaccharides from marine algae as potential blood anticoagulant agents. Curr Sci 79:1672–1683
61. Shanmugam M, Mody KH, Siddhanta AK (2001) Blood anticoagulant sulphated polysaccharides of the marine green algae Codium dwarkense (Boergs.) and C. tomentosum (Huds.) Stackh. Ind J Exp Biol 39:365–370
62. Shapira J (1969) Identification of sugars as their trifluoroacetylpolyol derivatives. Nature 222:792–793
63. Siddhanta AK, Shanmugam M, Mody KH, Goswami AM, Ramavat BK (1999) Sulphated polysaccharides of Codium dwarkense Boergs. from the west coast of India: chemical composition and blood anticoagulant activity. Int J Biol Macromol 26:151–154
64. Silvestri LJ, Hurst RE, Simpson L, Settine JM (1982) Analysis of sulfate in complex carbohydrates. Anal Biochem 123:303–309
65. Sohn CH (1998) The seaweed resources of Korea. In: Critchley AT, Ohno M (eds) Seaweed resources of the world. Japan International Cooperation Agency, Yokosuka, pp 15–33
66. Sugahara K, Tanaka Y, Yamada S, Seno N, Kitagawa H, Haslam SM, Morris HR, Dell A (1996) Novel sulphated oligosaccharides containing 3-O-sulphated glucuronic acid from king crab cartilage chondroitin sulphate K: unexpected degradation by chondroitinase ABC. J Biol Chem 271:26745–26754
67. Synytsya A, Kim WJ, Kim SM, Pohl R, Synytsya A, Kvasnička F, Čopíková J, Park YI (2010) Structure and antitumour activity of fucoidan isolated from sporophyll of Korean brown seaweed Undaria pinnatifida. Carbohydr Polym 81:41–48
68. Tabarsa M, Lee SJ, You SG (2012) Structural analysis of immunostimulating sulfated polysaccharides from Ulva pertusa. Carbohydr Res 361:141–147
69. Uehara T, Takeshita M, Maeda M (1992) Studies on anticoagulant-active arabinan sulfates from the green alga, Codium latum. Carbohydr Res 235:309–311
70. Yang VC, Linhardt RJ, Bernstein H, Cooney CL, Langer R (1985) Purification and characterization of heparinase from Flavobacterium heparinum. J Biol Chem 260:1849–1857
71. Yoo YC, Kim WJ, Kim SY, Kim SM, Chung MK, Park JW, Suh HH, Lee KB, Park YI (2007) Immunomodulating activity of a fucoidan isolated from Korean Undaria pinnatifida sporophyll. Algae 22:333–338