Optimized and standardized isolation and structural characterization of anti-inflammatory sulfated polysaccharides from the red alga Delesseria sanguinea (Hudson) Lamouroux (Ceramiales, Delesseriaceae)

Biomacromolecules

Volumn 10, Issue 11, 2009, Pages 2998-3008

  Grünewald, Niels ^a   Alban, Susanne ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORIES; ARTIFICIAL REEFS; AVERAGE YIELD; BALTIC SEA; COEXTRACTION; EXTRACTION PROCEDURE; HIGH QUALITY; PHARMACOLOGICAL PROFILES; RED ALGAE; SEASONAL VARIABILITY; STRUCTURAL CHARACTERIZATION; SULFATED POLYSACCHARIDES;

BIOPOLYMERS; FISHERIES; PHYTOPLANKTON; POLYMER BLENDS; POLYSACCHARIDES; REEFS;

SOLVENT EXTRACTION;

ELASTASE; MONOSACCHARIDE; POLYSACCHARIDE;

ARTICLE; CONTROLLED STUDY; DELESERIA SANGUINEA; NONHUMAN; PRIORITY JOURNAL; RED ALGA; SULFATION; THROMBOPLASTIN TIME;

ALGAE, RED; ANIMALS; ANTI-INFLAMMATORY AGENTS; POLYSACCHARIDES; REPRODUCIBILITY OF RESULTS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SULFATES; SWINE;

ALGAE; CERAMIALES; DELESSERIA SANGUINEA; DELESSERIACEAE; RHODOPHYTA;

EID: 70449464611     PISSN: 15257797     EISSN: None     Source Type: Journal    
DOI: 10.1021/bm900501g     Document Type: Article

References (64)

1. Berteau, O.; Mulloy, B. Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology 2003, 13 (6), 29R-40R. (Pubitemid 36665414)
2. Mourao, P. A. S. Use of sulfated fucans as anticoagulant and antithrombotic agents: future perspectives. Curr. Pharm. Des. 2004, 10 (9), 967-981.
3. Medeiros, V. P.; Queiroz, K. C. S.; Cardoso, M. L.; Monteiro, G. R. G.; Oliveira, F. W.; Chavante, S. F.; Guimaraes, L. A.; Rocha, H. A. O.; Leite, E. L. Sulfated galactofucan from Lobophora variegata: Anticoagulant and anti-inflammatory properties. Biochemistry (Moscow) 2008, 73 (9), 1018-1024.
4. Preobrazhenskaya, M. E.; Berman, A. E.; Mikhailov, V. I.; Ushakova, N. A.; Mazurov, A. V.; Semenov, A. V.; Usov, A. I.; Nifantev, N. E.; Bovin, N. V. Fucoidan inhibits leukocyte recruitment in a model peritoneal inflammation in rat and blocks interaction of P-selectin with its carbohydrate ligand. Biochem. Mol. Biol. Int. 1997, 43 (2), 443-451.
5. Alban, S.; Bourgougnon, N.; Franz, G. Anticoagulant activity of an antiviral sulfated glucuronogalactan from Schizymenia dubyi (Rhodophyta, Gigartinales). Thromb. Haemostasis 1997, 78, PS 2836 Suppl.
6. Bourgougnon, N.; Roussakis, C.; Kornprobst, J.-M.; Lahaye, M. Effects in vitro of sulfated polysaccharide from Schizymenia dubyi (Rhodophyta, Gigartinales) on a non-small-cell bronchopulmonary carcinoma line (NSCLC-N6). Cancer Lett. 1994, 85 (1), 87-92. (Pubitemid 24280167)
7. Mandal, P.; Pujol Carlos, A.; Carlucci Maria, J.; Chattopadhyay, K.; Damonte Elsa, B.; Ray, B. Anti-herpetic activity of a sulfated xylomannan from Scinaia hatei. Phytochemistry 2008, 69 (11), 2193-2199.
8. Duarte, M. E. R.; Cauduro, J. P.; Noseda, D. G.; Noseda, M. D.; Goncalves, 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. 2004, 339 (2), 335-347.
9. Damonte, E. B.; Matulewicz, M. C.; Cerezo, A. S.; Coto, C. E. Herpes simplex virus-inhibitory sulfated xylogalactans from the red seaweed Nothogenia fastigiata. Chemotherapy 1996, 42 (1), 57-64.
10. Haslin, C.; Lahaye, M.; Pellegrini, M.; Chermann, J. C. In vitro anti-HIV activity of sulfated cell-wall polysaccharides from gametic, carposporic and tetrasporic stages of the Mediterranean red alga Asparagopsis armata. Planta Med. 2001, 67 (4), 301-305.
11. SCADPlus website, Activities of the European Union - Summaries of legislation, http://europa.eu/scadplus/index.htm, accessed 02/10/2009.
12. Landesforschungsanstalt für Landwirtschaft und Fischerei, Mecklenburg-Vorpommern, Institut für Fischerei, Riff Nienhagen, http://www.riff-nienhagen.de, accessed 03/19/2009.
13. Schygula, C. Colonisation strategies and benthic community development on artificial reef structures in the south-western Baltic Sea, Ph.D. Thesis, University of Rostock, Rostock, Germany, 2007.
14. Nielsen, R.; Kristiansen, A.; Mathiesen, L.; Mathiesen, H. Distributional index of the benthic macroalgae of the Baltic Sea area. Acta Bot. Fenn. 1995, 155, 1-51. (Pubitemid 26453150)
15. Rietema, H. Ecotopic Differences between Baltic and North Sea Populations of Delesseria sanguinea and Membranoptera alata. Bot. Mar. 1993, 36, 15-21.
16. Lüning, K.; Schmitz, K. Dark growth of the red alga Delesseria sanguinea (Ceramiales): lack of chlorophyll, photosynthetic capability and phycobilisomes. Phycologia 1988, 27, 72-77.
17. Nabil, S.; Cosson, J. Seasonal variations in sterol composition of Delesseria sanguinea (Ceramiales, Rhodophyta). Hydrobiologia 1996, 326/327, 511-514. (Pubitemid 26353630)
18. Yvin, J. C.; Chevolot-Magueur, A. M.; Chevolot, L.; Lallemand, J. Y.; Potier, P.; Guilhem, J. Delesserine, a new metabolite of mixed biogenesis from the red marine alga Delesseria sanguinea (Lamouroux). J. Am. Chem. Soc. 1982, 104 (16), 4497-4498.
19. Yvin, J. C.; Chevolot, L.; Chevolot-Magueur, A. M.; Cochard, J. C. First isolation of jacaranone from an alga, Delesseria sanguinea. A metamorphosis inducer of Pecten larvae. J. Nat. Prod. 1985, 48 (5), 814-816.
20. Gervais, M. J. Glucosides of the red alga Delesseria sanguinea. Rev. Gen. Bot. 1959, 66 (7), 395-401.
21. Elsner, H.; Liedmann, A.; Oppers, K. Tierversuche mit einem gerinnungshemmenden Algenstoff aus Delesseria sanguinea (L.) Lam. Naunyn-Schmiedeberg's Arch. Pharmacol. 1938, 190 (3-5), 510-514.
22. Potin, P.; Patier, P.; Floc'h, J. Y.; Yvin, J. C.; Rochas, C.; Kloareg, B. Chemical characterization of cell-wall polysaccharides from tank-cultivated and wild plants of Delesseria sanguinea (Hudson) Lamouroux (Ceramiales, Delesseriaceae): Culture patterns and potent anticoagulant activity. J. Appl. Phycol. 1992, 4 (2), 119-128.
23. Groth, I.; Grünewald, N.; Alban, S. Pharmacological profiles of animal- and nonanimal-derived sulfated polysaccharides-comparison of unfractionated heparin, the semisynthetic glucan sulfate PS3, and the sulfated polysaccharide fraction isolated from Delesseria sanguinea. Glycobiology 2009, 19 (4), 408-417.
24. Grünewald, N.; Groth, I.; Alban, S. Evaluation of seasonal variations of the structure and anti-inflammatory activity of sulfated polysaccharides extracted from the red alga Delesseria sanguinea (Hudson) Lamouroux (Ceramiales, Delesseriaceae). Biomacromolecules 2009, 10, 1155-1162.
25. Kain, J. M.; Bates, M. J. The reproductive phenology of Delesseria sanguinea and Odonthalia dentata off the Isle of Man. Eur. J. Phycol. 1993, 28, 173-182.
26. Navarro, D. A.; Stortz, C. A. Isolation of xylogalactans from the Corallinales: influence of the extraction method on yields and compositions. Carbohydr. Polym. 2002, 49 (1), 57-62.
27. European Pharmacopoeia 6.0, Monograph: Heparins, low-molecularmass. Ph. Eur. 6.0/01/2008:0828, 2008.
28. Dreywood, R. Qualitative test for carbohydrate material. J. Ind. Eng. Chem. 1946, 18, 499.
29. Yaphe, W.; Arsenault, G. P. Improved resorcinol reagent for the determination of fructose and of 3,6-anhydrogalactose in polysaccharides. Anal. Biochem. 1965, 13 (1), 143-148.
30. Blumenkrantz, N.; Asboe-Hansen, G. New method for quantitative determination of uronic acids. Anal. Biochem. 1973, 54 (2), 484-489.
31. van den Hoogen, B. M.; van Weeren, P. R.; Lopes-Cardozo, M.; van Golde, L. M.; Barneveld, A.; van de Lest, C. H. A microtiter plate assay for the determination of uronic acids. Anal. Biochem. 1998, 257 (2), 107-111. (Pubitemid 28128971)
32. McComb, E. A.; McCready, R. M. Determination of acetyl in pectin and in acetylated carbohydrate polymers. Hydroxamic acid reaction. Anal. Chem. 1957, 29, 819-821.
33. Legler, G.; Muller-Platz, C. M.; Mentges-Hettkamp, M.; Pflieger, G.; Julich, E. On the chemical basis of the Lowry protein determination. Anal. Biochem. 1985, 150 (2), 278-287.
34. Zor, T.; Selinger, Z. Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Anal. Biochem. 1996, 236 (2), 302-308. (Pubitemid 26136110)
35. Ogden, G.; Foldi, P. Amino acid analysis: An overview of current methods. LCGC North Am. 1987, 5 (1), 28-40.
36. Heukeshoven, J.; Dernick, R. Improved silver staining procedure for fast staining in PhastSystem Development Unit. I. Staining of sodium dodecyl sulfate gels. Electrophoresis 1988, 9 (1), 28-32.
37. Albersheim, P.; Nevins, D. J.; English, P. D.; Karr, A. Analysis of sugars in plant cell-wall polysaccharides by gas-liquid chromatography. Carbohydr. Res. 1967, 5 (3), 340-345.
38. Blakeney, A. B.; Harris, P. J.; Henry, R. J.; Stone, B. A. A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydr. Res. 1983, 113 (2), 291-299.
39. Harris, P. J.; Henry, R. J.; Blakeney, A. B.; Stone, B. A. An improved procedure for the methylation analysis of oligosaccharides and polysaccharides. Carbohydr. Res. 1984, 127 (1), 59-73.
40. Nagasawa, K.; Inoue, Y.; Kamata, T. Solvolytic desulfation of glycosaminoglycuronan sulfates with dimethyl sulfoxide containing water or methanol. Carbohydr. Res. 1977, 58 (1), 47-55.
41. Taylor, R. L.; Conrad, H. E. Stoichiometric depolymerization of polyuronides and glycosaminoglycuronans to monosaccharides following reduction of their carbodiimide-activated carboxyl group. Biochemistry 1972, 12 (8), 1383-1388.
42. Wyatt, P. J. Light scattering and the absolute characterization of macromolecules. Anal. Chim. Acta 1993, 272 (1), 1-40. (Pubitemid 23026256)
43. Yvin, J.-C.; Alban, S.; Franz, G. Anti-inflammatory and healing medicine based on laminarin sulphate. U.S. Patent 7008931, 2002.
44. Alban, S.; Ludwig, R. J.; Bendas, G.; Schon, M. P.; Oostingh, G. J.; Radeke, H. H.; Fritzsche, J.; Pfeilschifter, J.; Kaufmann, R.; Boehncke, W. H. PS3, a semisynthetic β-1,3-glucan sulfate, diminishes contact hypersensitivity responses through inhibition of L- and P-selectin functions. J. Invest. Dermatol. 2009, 129 (5), 1192-1202.
45. Matsuhiro, B.; Rivas, P. Second-derivative Fourier transform infrared spectra of seaweed galactans. J. Appl. Phycol. 1993, 5 (1), 45-51.
46. Rochas, C.; Lahaye, M.; Yaphe, W. Sulfate content of carrageenan and agar determined by infrared spectroscopy. Bot. Mar. 1986, 29 (4), 335-340.
47. Alban, S.; Franz, G. Partial synthetic glucan sulfates as potential new antithrombotics: A review. Biomacromolecules 2001, 2 (2), 354-361. (Pubitemid 32707511)
48. Navarro, D. A.; Stortz, C. A. Microwave-assisted alkaline modification of red seaweed galactans. Carbohydr. Polym. 2005, 62 (2), 187-191.
49. Viola, R.; Nyvall, P.; Pedersen, M. The unique features of starch metabolism in red algae. Proc. R. Soc. B 2001, 268 (1474), 1417-1422. (Pubitemid 32625608)
50. Groth, I.; Alban, S. Elastase inhibition assay with peptide substratessan example for the limited comparability of in vitro results. Planta Med. 2008, 74 (8), 852-858. (Pubitemid 351991121)
51. Usov, A. I.; Ivanova, E. G.; Shashkov, A. S. Polysaccharides of algae. XXXIII. Isolation and carbon-13 NMR spectral study of some new gel-forming polysaccharides from Japan Sea red seaweeds. Bot. Mar. 1983, 26 (6), 285-294.
52. Miller, I. J. Evaluation of the structures of polysaccharides from three taxa in the genus Hymenena and from Acrosorium decumbens (Rhodophyta, Delesseriaceae). Bot. Mar. 2005, 48 (2), 148-156.
53. Percival, E.; McDowell, R. H. Algal Polysaccharides. In Methods in Plant Biochemistry, 2nd ed.; Dey, P. M., Harborne, J. D., Eds.; Academic Press Ltd.: Oxford, 1990; Chapter 15.
54. Turner, R. D.; Evans, L. V. Structural and physiological aspects of translocation in the red alga Delesseria. Eur. J. Phycol. 1986, 21, 338.
55. Karsten, U.; West, J. A.; Mostaert, A. S.; King, R. J.; Barrow, K. D.; Kirst, G. O. Mannitol in the red algal genus Caloglossa (Harvey) J. Agardh. J. Plant Physiol. 1992, 140 (3), 292-297.
56. Karsten, U.; Michalik, D.; Michalik, M.; West, J. A. A new unusual low molecular weight carbohydrate in the red algal genus Hypoglossum (Delesseriaceae, Ceramiales) and its possible function as an osmolyte. Planta 2005, 222 (2), 319-326.
57. Wingler, A. The function of trehalose biosynthesis in plants. Phytochemistry 2002, 60 (5), 437-440.
58. Ludwig, R. J.; Alban, S.; Boehncke, W. H. Structural requirements of heparin and related molecules to exert a multitude of anti-inflammatory activities. Mini-Rev. Med. Chem. 2006, 6 (9), 1009-1023.
59. Shanmugam, M.; Mody, K. H. Heparinoid-active sulphated polysaccharides from marine algae as potential blood anticoagulant agents. Curr. Sci. India 2000, 79 (12), 1672-1683.
60. Bourgougnon, N.; Lahaye, M.; Quemener, B.; Chermann, J. C.; Rimbert, M.; Cormaci, M.; Furnari, G.; Kornprobst, J. M. Annual variation in composition and in vitro anti-HIV-1 activity of the sulfated glucuronogalactan from Schizymenia dubyi (Rhodophyta, Gigartinales). J. Appl. Phycol. 1996, 8 (2), 155-161.
61. Codif Recherche & Nature Company, Rhodofiltrat Delesseria HG, http://www.in-cosmetics.com/ ExhibitorLibrary/73/RHODOFILTRAT-DELESSERIA-GB.pdf, accessed 01/12/2008.
62. Bourgougnon, N.; Chermann, J. C.; Lahaye, M.; Kornprobst, J. M. Anti-HIV activity and mode of action, in vitro, of the sulfated polysaccharide from Schizymenia dubyi (Rhodophyta). Cell. Pharmacol. 1996, 3 (2), 104-108.
63. Witvrouw, M.; De Clercq, E. Sulfated polysaccharides extracted from sea algae as potential antiviral drugs. Gen. Pharmacol. 1997, 29 (4), 497-511. (Pubitemid 27421412)
64. Keith, J.; Stockwell, S.; Ball, D.; Remillard, K.; Kaplan, D.; Thannhauser, T.; Sherwood, R. Comparative analysis of macromolecules in mollusc shells. Comp. Biochem. Physiol. B 1993, 105 (3-4), 487-496. (Pubitemid 23200095)