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

Volumn 10, Issue 5, 2009, Pages 1155-1162

  Grünewald, Niels ^a   Groth, Inken ^a   Alban, Susanne ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORY ACTIVITY; ANTI-INFLAMMATORY EFFECTS; AQUEOUS EXTRACTION; ARTIFICIAL REEFS; BALTIC SEA; COEXTRACTION; ELASTASE; GLUCANS; GLUCOSE CONTENT; INHIBITORY ACTIVITY; MACRO ALGAE; PHARMACOLOGICAL CHARACTERIZATION; RED ALGAE; SEASONAL VARIABILITY; SEASONAL VARIATION; SULFATED POLYSACCHARIDES;

BIOPOLYMERS; FISHERIES; GLUCOSE; HARVESTING; PHYTOPLANKTON; POLYSACCHARIDES; REEFS;

SOLVENT EXTRACTION;

ELASTASE; HYALURONIDASE; POLYSACCHARIDE SULFATE;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; BALTIC SEA; DELESSERIA SANGUINEA; DRUG ISOLATION; ENZYME ACTIVITY; PRIORITY JOURNAL; RED ALGA; SEASONAL VARIATION;

ALGAE, RED; ANTI-INFLAMMATORY AGENTS; ANTICOAGULANTS; ENZYME INHIBITORS; HUMANS; HYALURONOGLUCOSAMINIDASE; LEUKOCYTE ELASTASE; MOLECULAR WEIGHT; NEUTROPHILS; POLYSACCHARIDES; SEASONS; SULFURIC ACID ESTERS;

ALGAE; CERAMIALES; DELESSERIA SANGUINEA; DELESSERIACEAE; RHODOPHYTA;

EID: 66149087712     PISSN: 15257797     EISSN: None     Source Type: Journal    
DOI: 10.1021/bm8014158     Document Type: Article

References (56)

1. Mayer, A. M. S.; Rodriguez, A. D.; Berlinck, R. G. S.; Hamann, M. T. Marine pharmacology in 2003-4: Marine compounds with anthelmintic, antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiplatelet, antiprotozoal, antituberculosis, and antiviral activities; affecting the cardiovascular, immune and nervous systems, and other miscellaneous mechanisms of action. Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 2007, 145, 553-581. (Pubitemid 46660746)
2. Abad, M. J.; Bedoya, L. M.; Bermejo, P. Natural marine antiinflammatory products. Mini-Rev. Med. Chem. 2008, 8, 740-754.
3. Alban, S.; Bourgougnon, N.; Franz, G. Anticoagulant activity of an antiviral sulfated glucuronogalactan from Schizymenia dubyi (Rhodophyta, Gigartinales). Thromb. Haemostasis 1997, 78, 2836.
4. 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. (Shannon, Irel.) 1994, 85 (1), 87-92. (Pubitemid 24280167)
5. Assreuy, A. M. S.; Gomes, D. M.; Josino da Silva, M. S.; Torres, V. M.; Siqueira, R. C. L.; Pires, A. d. F.; Criddle, D. N.; de Alencar, N. M. N.; Cavada, B. S.; Sampaio, A. H.; Farias, W. R. L. Biological effects of a sulfated-polysaccharide isolated from the marine red algae Champia feldmannii. Biol. Pharm. Bull. 2008, 31 (4), 691-695.
6. Viana, G. S. B.; Freitas, A. L. P.; Lima, M. M. L.; Vieira, L. A. P.; Andrade, M. C. H.; Benevides, N. M. B. Antinociceptive activity of sulfated carbohydrates from the red algae Bryothamnion seaforthii (Turner) Kütz. and B. triquetrum (S. G. Gmel.) M. Howe. Braz. J. Med. Biol. Res. 2002, 35, 719-722.
7. 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)
8. Mourao, P. A. S. Use of sulfated fucans as anticoagulant and antithrombotic agents: future perspectives. Curr. Pharm. Des. 2004, 10 (9), 967-981. (Pubitemid 38380075)
9. 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.
10. 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. (Pubitemid 26373008)
11. 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. A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 2007, 17 (5), 541-552. (Pubitemid 47049941)
12. SCADPlus website, Activities of the European Union - Summaries of legislation. http://europa.eu/scadplus/leg/en/lvb/l60017.htm. (accessed 11/11/2008).
13. Landesforschungsanstalt für Landwirtschaft und Fischerei MV, Institut für Fischerei, Riff Nienhagen. http://www.riff-nienhagen.de (accessed 11/07/2008).
14. 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.
15. 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.
16. 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.
17. Groth, I.; Grünewald, N.; Alban, S. Pharmacological profiles of animal-and non-animal-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.
18. Obluchinskaya, E. D.; Voskoboinikov, G. M.; Galynkin, V. A. Contents of alginic acid and fucoidan in fucus algae of the Barents Sea. Appl. Biochem. Microbiol. 2002, 38 (2), 186-188. (Pubitemid 37115940)
19. Zvyagintseva, T. N.; Shevchenko, N. M.; Chizhov, A. O.; Krupnova, T. N.; Sundukova, E. V.; Isakov, V. V. Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions. J. Exp. Mar. Biol. Ecol. 2003, 294 (1), 1-13. (Pubitemid 36996551)
20. Molenaar, F. J.; Breeman, A. M. Latitudinal trends in the growth and reproductive seasonality of Delesseria sanguinea. Membranoptera alata and Phycodrys rubens (Rhodophyta). J. Phycol. 1997, 33, 330-343.
21. Kain, J. M. Photoperiod and temperature as triggers in the seasonality of Delesseria sanguinea. Helgoland Mar. Res. 1987, 41, 355-370.
22. Grünewald, N.; Alban, S. Optimized and standardized isolation and structural characterization of anti-inflammatory sulfated polysaccharides from the red alga Delesseria sanguinea (Hudson) Lamouroux (Ceramiales, Delesseriaceae), in preparation.
23. European Pharmacopoeia Monograph: Low molecular heparins. European Pharmacopoeia; EDQM Counsil of Europe: Strasbourg, France, 2008; Vol.6.0/0828.
24. Casu, B.; Gennaro, U. Conductimetric method for the determination of sulfate and carboxyl groups in heparin and other mucopolysaccharides. Carbohydr. Res. 1975, 39 (1), 168-176.
25. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
26. 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)
27. Roth, M. Fluorescence reaction for amino acids. Anal. Chem. (Washington, DC, U.S.) 1971, 43 (7), 880-882.
28. Ogden, G.; Foldi, P. Amino acid analysis: An overview of current methods. LCGC North Am. 1987, 5 (1), 28-40.
29. Pons, A.; Roca, P.; Aguilo, C.; Garcia, F. J.; Alemany, M.; Palou, A. A method for the simultaneous determination of total carbohydrate and glycerol in biological samples with the anthrone reagent. J. Biochem. Biophysic. Meth. 1981, 4 (3-4), 227-231. (Pubitemid 11079640)
30. 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.
31. Blumenkrantz, N.; Asboe-Hansen, G. New method for quantitative determination of uronic acids. Anal. Biochem. 1973, 54 (2), 484-489.
32. 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)
33. Wyatt, P. J. Light scattering and the absolute characterization of macromolecules. Anal. Chim. Acta 1993, 272 (1), 1-40. (Pubitemid 23026256)
34. 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.
35. 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.
36. Yvin, J. C.; Alban, S.; Franz, G. Anti-inflammatory and healing medicine based on laminarin sulphate. US Patent 7008931.
37. Alban, S. Natural and synthetic glycosaminoglycans: molecular characteristics as the basis of distinct drug profiles. Haemostaseologie (Stuttgart, Germany) 2008, 28 (1-2), 51-61.
38. Proctor, R. R.; Rapaport, S. I. The partial thromboplastin time with kaolin. A simple screening test for first stage plasma clotting factor deficiencies. Am. J. Clin. Pathol. 1961, 36, 212-219.
39. Alban, S.; Franz, G. Partial synthetic glucan sulfates as potential new antithrombotics: A review. Biomacromolecules 2001, 2 (2), 354-361. (Pubitemid 32707511)
40. Becker, M.; Franz, G.; Alban, S. Inhibition of PMN-elastase activity by semisynthetic glucan sulfates. Thromb. Haemostasis 2003, 89 (5), 915-925. (Pubitemid 36608876)
41. Turner, R. D.; Evans, L. V. Structural and physiological aspects of translocation in the red alga Delesseria. Eur. J. Phycol. 1986, 21, 338.
42. Viola, R.; Nyvall, P.; Pedersen, M. The unique features of starch metabolism in red algae. Proc. R. Soc. London B 2001, 268 (1474), 1417-1422. (Pubitemid 32625608)
43. European Medicines Agency (EMEA). Scientific guidelines for human medicinal products. Quality guidelines for herbal medicinal products. http://www.emea.europa.eu/htms/human/humanguidelines/quality.htm (accessed 12/01/2008).
44. Mao, W.-J.; Fang, F.; Li, H.-Y.; Qi, X.-H.; Sun, H.-H.; Chen, Y.; Guo, S.-D. Heparinoid-active two sulfated polysaccharides isolated from marine green algae Monostroma nitidum. Carbohydr. Polym. 2008, 74, 834-839.
45. 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.
46. Farias, W. R. L.; Valente, A.-P.; Pereira, M. S.; Mourao, P. A. S. Structure and anticoagulant activity of sulfated galactans. J. Biol. Chem. 2000, 275 (38), 29299-29307.
47. CODIF Recherche & Nature company, RHODOFILTRAT DELESSERIA HG. http://www.in-cosmetics.com/ExhibitorLibrary/73/RHODOFILTRAT-DELESSERIA-GB.pdf. (accessed 01/12/2008).
48. Montanari, D.; Guglielmo, M. Cosmetic composition for the treatment and/or prevention of skin stretch marks. Patent No. WO 2008 080443, 2008.
49. Girard, N.; Maingonnat, C.; Bertrand, P.; Tilly, H.; Vannier, J. P.; Delpech, B. Human monocytes synthesize hyaluronidase. Br. J. Haematol. 2002, 119 (1), 199-203. (Pubitemid 35176521)
50. Nelson, A. R.; Fingleton, B.; Rothenberg, M. Matrix metalloproteinases: biologic activity and clinical implications. J. Clin. Oncol. 2000, 18 (5), 1135-1149. (Pubitemid 30123793)
51. Posey, J. T.; Soloway, M. S.; Ekici, S.; Sofer, M.; Civantos, F.; Duncan, R. C.; Lokeshwar, V. B. Evaluation of the prognostic potential of hyaluronic acid and hyaluronidase (HYAL1) for prostate cancer. Cancer Res. 2003, 63 (10), 2638-2644. (Pubitemid 36605207)
52. Sato, T.; Takahashi, S.; Mizumoto, T.; Harao, M.; Akizuki, M.; Takasugi, M.; Fukutomi, T.; Yamashita, J. Neutrophil elastase and cancer. Surg. Oncol. 2006, 15 (4), 217-222. (Pubitemid 46771195)
53. Alban, S.; Franz, G. Gas-liquid chromatography-mass spectrometry analysis of anticoagulant active Curdlan sulfates. Semin. Thromb. Hemostasis 1994, 20 (2), 152-158. (Pubitemid 24263664)
54. Witvrouw, M.; De Clercq, E. Sulfated polysaccharides extracted from sea algae as potential antiviral drugs. Gen. Pharmacol. 1997, 29 (4), 497-511. (Pubitemid 27421412)
55. Damonte, E. B.; Matulewicz, M. C.; Cerezo, A. S.; Coto, C. E. Herpes simplex virus-inhibitory sulphated xylogalactans from the red seaweed Nothogenia fastigiata. Chemotherapy 1996, 42 (1), 57-64. (Pubitemid 126484600)
56. 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)