Chemical characterization of sulfated polysaccharides from Gracilaria gracilis and Ulva lactuca and their radical scavenging, metal chelating, and cholinesterase inhibitory activities

References

• Wells, M. L.; Potin, P.; Craigie, J. S.; Raven, J. A.; Merchant, S. S.; Helliwell, K. E.; Smith, A. G.; Camire, M. E.; Brawley, S. H. Algae as Nutritional and Functional Food Sources: Revisiting Our Understanding. J. Appl. Phycol. 2017, 29, 949–982.
   PubMed Web of Science ®Google Scholar
• Murray, M.; Dordevic, A. L.; Bonham, M. P.; Ryan, L. Do Marine Algal Polyphenols Have Antidiabetic, Antihyperlipidemic or Anti-Inflammatory Effects in Humans? A Systematic Review. Crit. Rev. Food Sci. Nutr. 2018, 58, 2039–2054. DOI: 10.1080/10408398.2017.1301876.
   PubMed Web of Science ®Google Scholar
• Murray, M.; Dordevic, A. L.; Ryan, L.; Bonham, M. P. An Emerging Trend in Functional Foods for the Prevention of Cardiovascular Disease and Diabetes: Marine Algal Polyphenols. Crit. Rev. Food Sci. Nutr. 2018, 58, 1342–1358. DOI: 10.1080/10408398.2016.1259209.
   PubMed Web of Science ®Google Scholar
• Thomas, N. V.; Kim, S. K. Potential Pharmacological Applications of Polyphenolic Derivatives from Marine Brown Algae. Environ. Toxicol. Pharmacol. 2011, 32, 325–335. DOI: 10.1016/j.etap.2011.09.004.
   PubMed Web of Science ®Google Scholar
• Pereira, H.; Barreira, L.; Figueiredo, F.; Custódio, L.; Vizetto-Duarte, C.; Polo, C.; Rešek, E.; Engelen, A.; Varela, J. Polyunsaturated Fatty Acids of Marine Macroalgae: Potential for Nutritional and Pharmaceutical Applications. Mar. Drugs. 2012, 10, 1920–1935. DOI: 10.3390/md10091920.
   PubMed Web of Science ®Google Scholar
• Borowitzka, M.;. Dunaliella: Biology, Production, and Markets. In Handbook of Microalgal Culture; Richmond, A., Hu, Q., Eds.; John Wiley & Sons, Ltd: Chichester, 2013; pp 359–368.
   Google Scholar
• Tibbetts, S. M.; Milley, J. E.; Lall, S. P. Nutritional Quality of Some Wild and Cultivated Seaweeds: Nutrient Composition, Total Phenolic Content and in Vitro Digestibility. J. Appl. Phycol. 2016, 26, 3575–3585. DOI: 10.1007/s10811-016-0863-y.
   Google Scholar
• Raposo, M. F. J.; Morais, A. M. B.; Morais, R. M. S. Marine Polysaccharides from Algae with Potential Biomedical Applications. Mar. Drugs. 2015, 13, 2967–3028. DOI: 10.3390/md13052967.
   PubMed Web of Science ®Google Scholar
• Wang, J.; Hu, S.; Nie, S.; Yu, Q.; Xie, M. Reviews on Mechanisms of in Vitro Antioxidant Activity of Polysaccharides. Oxid. Med. Cell. Longev. 2016, 5692852, 13.
   Google Scholar
• Shao, P.; Ma, H.; Qiu, Q.; Jing, W. Physical Stability of R-(+)-Limonene Emulsions Stabilized by Ulva Fasciata Algae Polysaccharide. Int. J. Biol. Macromol. 2016, 92, 926–934. DOI: 10.1016/j.ijbiomac.2016.08.009.
   PubMed Web of Science ®Google Scholar
• Shao, P.; Zhang, H.; Niu, B.; Jiang, L. Antibacterial Activities of R- (+)-Limonene Emulsion Stabilized by Ulva Fasciata Polysaccharide for Fruit Preservation. Int. J. Biol. Macromol. 2018, 111, 1273–1280. DOI: 10.1016/j.ijbiomac.2018.01.126.
   PubMed Web of Science ®Google Scholar
• Fleita, D.; El-Sayed, M.; Rifaat, D. Evaluation of the Antioxidant Activity of Enzymatically-Hydrolyzed Sulfated Polysaccharides Extracted from Red Algae; Pterocladia Capillace. LWT - Food Sci. Technol. 2015, 63, 1236–1244. DOI: 10.1016/j.lwt.2015.04.024.
   Web of Science ®Google Scholar
• Ahn, G.; Lee, W.; Kim, K.; Lee, J.; Heo, S.; Kang, N.; Lee, S.; Ahn, C.; Jeon, Y. A Sulfated Polysaccharide of Ecklonia Cava Inhibits the Growth of Colon Cancer Cells by Inducing Apoptosis. Excli J. 2015, 14, 294–306. DOI: 10.17179/excli2015-565.
   PubMed Web of Science ®Google Scholar
• Faggio, C.; Pagano, M.; Dottore, A.; Genovese, G.; Morabito, M. Evaluation of Anticoagulant Activity of Two Algal Polysaccharides. Nat. Prod. Res. 2016, 30, 1934–1937. DOI: 10.1080/14786419.2015.1086347.
   PubMed Web of Science ®Google Scholar
• Grossberg, G. T.;. Cholinesterase Inhibitors for the Treatment of Alzheimer’s Disease. Curr. Ther. Res. Clin. Exp. 2003, 64, 216–235. DOI: 10.1016/S0011-393X(03)00059-6.
   PubMed Web of Science ®Google Scholar
• Gara, A. B.; Kolsi, R. B.; Jardak, N.; Chaaben, R.; El-Feki, A.; Fki, L.; Belghith, H.; Belghith, K. Inhibitory Activities of Cystoseira Crinita Sulfated Polysaccharide on Key Enzymes Related to Diabetes and Hypertension: In Vitro and Animal Study. Arch. Physiol. Biochem. 2016, 123(1), 31–42. DOI: 10.1080/13813455.2016.1232737.
   PubMed Web of Science ®Google Scholar
• Chaplin, M. F.; Kennedy, J. F. Carbohydrate Analysis, 2nd ed.; Oxford University Press: New York, NY, USA, 1994.
   Google Scholar
• 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. DOI: 10.1016/0003-2697(76)90527-3.
   PubMed Web of Science ®Google Scholar
• Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Antioxidant Activity Applying an Improved ABTS Radical Cation Decolorisation Assay. Free Radical Biol. Med. 1999, 26, 1231–1237.
   PubMed Web of Science ®Google Scholar
• Gyamfi, M. A.; Yonamine, M.; Aniya, Y. Free Radical Scavenging Action of Medicinal Herbs from Ghana: Thonningia Sanguinea on Experimentally Induced Liver Injuries. Gen. Pharmacol. 1999, 32, 661–667.
   PubMedGoogle Scholar
• Halliwell, B.; Gutteridge, J. M. C. Formation of Thiobarbituric-Acid-Reactive Substance from Deoxyribose in the Presence of Iron Salts: The Role of Superoxide and Hydroxyl Radicals. FEBS Lett. 1981, 128, 347–352.
   PubMed Web of Science ®Google Scholar
• Puntel, R. L.; Nogueira, C. W.; Rocha, J. B. T. Krebs Cycle Intermediates Modulate Thiobarbituric Acid Reactive Species (TBARS) Production in Rat Brain in Vitro. Neurochem. Res. 2005, 30, 225–235.
   PubMed Web of Science ®Google Scholar
• Perry, N. S.; Houghton, P. J.; Theobald, A.; Jenner, P.; Perry, E. K. In Vitro Activity of Slavandula Efolia (Spanish Sage) Relevant to Treatment of Alzheimer’s Disease. J. Pharm. Pharmacol. 2000, 52, 895–902.
   PubMed Web of Science ®Google Scholar
• Hernández-Garibay, H.; Zertuche-González, J. A.; Pacheco-Ruíz, I. Isolation and Chemical Characterization of Algal Polysaccharides from the Green Seaweed Ulva Clathrata (Roth) C. Agardh. J. Appl. Phycol. 2011, 23, 537–542. DOI: 10.1007/s10811-010-9629-0.
   Web of Science ®Google Scholar
• Zayed, A.; Muffler, K.; Hahn, T.; Rupp, S.; Finkelmeier, D.; Burger-Kentischer, A.; Ulber, R. Physicochemical and Biological Characterization of Fucoidan from Fucus Vesiculosus Purified by Dye Affinity Chromatography. Mar. Drugs. 2016, 14, 79. DOI: 10.3390/md14040075.
   PubMed Web of Science ®Google Scholar
• McCandless, E.; Craigie, J. Sulfated Polysaccharides in Red and Brown Algae. Annu. Rev. Plant Biol. 1979, 30, 41–53. DOI: 10.1146/annurev.pp.30.060179.000353.
   Web of Science ®Google Scholar
• Barahonaa, T.; Encinasa, M. V.; Imaraib, M.; Mansillac, A.; Matsuhiroa, N. B.; Torresa, R.; Valenzuela, B. Bioactive Polysaccharides from Marine Algae. Bioact. Carbohydr. Diet. Fibre. 2014, 125–138. DOI: 10.1016/j.bcdf.2014.09.002.
   Google Scholar
• Cong, Q.; Chen, H.; Liao, W.; Xiao, F.; Wang, P.; Qin, Y.; Dong, Q.; Ding, K. Structural Characterization and Effect on Anti-Angiogenic Activity of a Fucoidan from Sargassum Fusiforme. Carbohydr. Polym. 2016, 136, 899–907. DOI: 10.1016/j.carbpol.2015.09.087.
   PubMed Web of Science ®Google Scholar
• Raguraman, V.; Abraham, S.; Jyotsna, J.; Palaniappan, S.; Gopal, S.; Thirugnanasambandam, R.; Kirubagaran, R. Sulfated Polysaccharide from Sargassum Tenerrimum Attenuates Oxidative Stress Induced Reactive Oxygen Species Production in In Vitro and in Zebrafish Model. Carbohydr. Polym. 2019, 203, 441–449. DOI: 10.1016/j.carbpol.2018.09.056.
   PubMed Web of Science ®Google Scholar
• Kim, S.; Choi, D.; Athukorala, Y.; Jeon, Y.; Senevirathne, M.; Rha, C. K. Antioxidant Activity of Sulfated Polysaccharides Isolated from Sargassum Fulvellum. Preventive Nutr. Food Sci. 2007, 12, 65–73. DOI: 10.3746/jfn.2007.12.2.065.
   Google Scholar
• Presa, F. B.; Marques, M. L. M.; Viana, R. L. S.; Nobre, L. T. D. B.; Costa, L. S.; Rocha, H. A. O. The Protective Role of Sulfated Polysaccharides from Green Seaweed Udotea Flabellum in Cells Exposed to Oxidative Damage. Mar. Drugs. 2018, 16, 135. DOI: 10.3390/md16040135.
   PubMed Web of Science ®Google Scholar
• Valko, M.; Lebfritz, D.; Moncol, J.; Cronin, M. T.; Mazur, M.; Telser, J. Free Radicals and Antioxidants in Normal Physiological Functions and Human Disease. Int. J. Biochem. Cell Biol. 2007, 39, 44–84. DOI: 10.1016/j.biocel.2006.07.001.
   PubMed Web of Science ®Google Scholar
• Liu, F.; Ooi, V. E. C.; Chang, S. T. Free Radical Scavenging Activities of Mushroom Polysaccharide Extracts. Life Sci. 1997, 60, 763–771. DOI: 10.1016/S0024-3205(97)00004-0.
   PubMed Web of Science ®Google Scholar
• Liu, D.; Sheng, J.; Li, Z.; Qi, H.; Sun, Y.; Duan, Y.; Zhang, W. Antioxidant Activity of Polysaccharide Fractions Extracted from Athyrium Multidentatum (Doll.) Ching. Int. J. Biol. Macromol. 2013, 56, 1–5. DOI: 10.1016/j.ijbiomac.2013.02.014.
   PubMed Web of Science ®Google Scholar
• Renard, C. M.; Baron, A.; Guyot, S.; Drilleau, J. F. “Interactions between Apple Cell Walls and Native Apple Polyphenols: Quantifcation and Some Consequences. Int. J. Biol. Macromol. 2001, 29, 115–125. DOI: 10.1016/S0141-8130(01)00155-6.
   PubMed Web of Science ®Google Scholar
• García-Ayllón, M.; Riba-Llena, I.; Serra-Basante, C.; Alom, J.; Boopathy, R.; Sáez-Valero, J. Altered Levels of Acetylcholinesterase in Alzheimer Plasma. PLoS One. 2010, 5, e8701. DOI: 10.1371/journal.pone.0008701.
   PubMed Web of Science ®Google Scholar
• Čolović, M. B.; Krstić, D. J.; Lazarević-Pašti, T. D.; Bondžić, A. M.; Vasi, V. M. Acetylcholinesterase Inhibitors: Pharmacology and Toxicology. Curr. Neuropharmacol. 2013, 315–335. DOI: 10.2174/1570159X11311030006.
   PubMed Web of Science ®Google Scholar
• Lin, X.; Huang, Z. S.; Chen, X. Y.; Rong, Y. P.; Zhang, S. J.; Jiao, Y.; Huang, Q. F.; Huang, R. B. Protective Effect of Millettia Pulchra Polysaccharide on Cognitive Impairment Induced by D-Galactose in Mice. Carbohydr. Polym. 2014, 101, 533–543. DOI: 10.1016/j.carbpol.2013.09.037.
   PubMed Web of Science ®Google Scholar
• Park, S. K.; Kang, J. Y.; Kim, J. M.; Park, S. H.; Kwon, B. K.; Kim, G.; Heo, H. J. Protective Effect of Fucoidan Extract from Ecklonia Cava on Hydrogen Peroxide-Induced Neurotoxicity. J. Microbiol. Biotechnol. 2018, 28, 40–49.
   PubMed Web of Science ®Google Scholar
• Greig, N. H.; Lahiri, D. K.; Sambamurti, K. Butyrylcholinesterase: An Important New Target in Alzheimer’s Disease Therapy. Int. Psychogeriatr. 2002, 14, 77–91. DOI: 10.1017/S1041610203008676.
   PubMed Web of Science ®Google Scholar
• Greig, N. H.; Utsuki, T.; Ingram, D. K.; Wang, Y.; Pepeu, G.; Scali, C.; Yu, Q.; Mamczarz, J.; Holloway, H. W.; Giordano, T.; et al. Selective Butyrylcholinesterase Inhibition Elevates Brain Acetylcholine, Augments Learning and Lowers Alzheimer β-amyloid Peptide in Rodent. Proc. Natl. Acad. Sci. U S A. 2005, 102, 17213–17218. DOI: 10.1073/pnas.0508575102.
   PubMed Web of Science ®Google Scholar