Antioxidant activity, α-amylase and α-glucosidase inhibition properties of sulfated-polysaccharides purified from freshwater plant Myriophyllum spicatum L.

Authors
Tarbiat Modares University
Abstract
Sulfated polysaccharides presenting in the cell wall of seaweeds and aquatic plants exhibit a diverse range of biological functions mainly due to their particular structural and molecular properties. The aim of the current study was to evaluate the inhibition of oxidation reactions and activities of digestive enzymes including α-amylase and α-glucosidase by sulfated polysaccharides from aquatic plant Myriophyllum spicatum. After the removal of pigments and low molecular weight compounds, polysaccharides were extracted by distilled water at 60°C for 2 hours. Polysaccharide purification using DEAE Sepharose FF led to production of two fractions including F1 and F2. Obtained polysaccharides were considerably capable of scavenging DPPH free radicals (20.62-64.81%) and reducing Fe3+ ions (0.24-0.50 Abs) with F1 fraction exhibiting the greatest activity. Polysaccharides inhibitions against α-amylase activity were greatly different (22.50-63.20%) with the lowest IC50 being 1.31 mg/mL for F2 fraction. α-glucosidase activity was reduced to various levels (1.30-89.5%) and the lowest IC50 of 10.0 mg/mL was observed for crude polysaccharide. Overall, these findings indicated that sulfated polysaccharides from M. spicatum L. possess promising antioxidant, α-amylase and α-glucosidase inhibition potentials depending on their chemical and molecular structure and thus could be considered as antioxidant and anti-diabetic agents.
Keywords

Subjects


[1] Burtin, P. (2003). Nutritional value of seaweeds. Electronic journal of Environmental, Agricultural and Food Chemistry, 2(4), 498-503.
[2] Wijesekara, I., Pangestuti, R., & Kim, S. K. (2011). Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydrate Polymers, 84(1), 14-21.
[3] McHugh, D. J. (2003). A guide to the seaweed industry FAO Fisheries Technical Paper 441. Food and Agriculture Organization of the United Nations, Rome.
[4] Tseng, C. K. (2001). Algal biotechnology industries and research activities in China. Journal of Applied Phycology, 13, 375–380.
[5] Tabarsa, M., You, S., Dabaghian, E. H., & Surayot, U. (2018). Water-soluble polysaccharides from Ulva intestinalis: Molecular properties, structural elucidation and immunomodulatory activities. Journal of Food and Drug Analysis, 26(2), 599-608.
[6] Masarin, F., Cedeno, F. R. P., Chavez, E. G. S., De Oliveira, L. E., Gelli, V. C., & Monti, R. (2016). Chemical analysis and biorefinery of red algae Kappaphycus alvarezii for efficient production of glucose from residue of carrageenan extraction process. Biotechnology for Biofuels, 9(1), 1-12.
[7] Borazjani, N. J., Tabarsa, M., You, S., & Rezaei, M. (2018). Purification, molecular properties, structural characterization, and immunomodulatory activities of water soluble polysaccharides from Sargassum angustifolium. International Journal of Biological Macromolecules, 109, 793-802.
[8] Costa, L. S., Fidelis, G. P., Cordeiro, S. L., Oliveira, R. M., Sabry, D. D. A., Câmara, R. B. G., ... & Rocha, H. A. O. (2010). Biological activities of sulfated polysaccharides from tropical seaweeds. Biomedicine & Pharmacotherapy, 64(1), 21-28.
[9] Miyashita, K., & Takagi, T. (1987). Tocopherol content of Japanese algae and its seasonal variation. Agricultural and Biological Chemistry, 51(11), 3115-3118.
[10] Hosokawa, M., Okada, T., Mikami, N., Konishi, I., & Miyashita, K. (2009). Bio-functions of marine carotenoids. Food Science and Biotechnology, 18(1), 1-11.
[11] Parys, S., Rosenbaum, A., Kehraus, S., Reher, G., Glombitza, K. W., & König, G. M. (2007). Evaluation of quantitative methods for the determination of polyphenols in algal extracts. Journal of Natural Products, 70(12), 1865-1870.
[12] Borazjani, N. J., Tabarsa, M., You, S., & Rezaei, M. (2017). Effects of extraction methods on molecular characteristics, antioxidant properties and immunomodulation of alginates from Sargassum angustifolium. International Journal of Biological Macromolecules, 101, 703-711.
[13] Borazjani, N. J., Tabarsa, M., You, S., & Rezaei, M. (2017). Improved immunomodulatory and antioxidant properties of unrefined fucoidans from Sargassum angustifolium by hydrolysis. Journal of Food Science and Technology, 54(12), 4016-4025.
[14] Rahimi, F., Tabarsa, M., & Rezaei, M. (2016). Ulvan from green algae Ulva intestinalis: optimization of ultrasound-assisted extraction and antioxidant activity. Journal of Applied Phycology, 28(5), 2979-2990.
[15] DeFronzo, R. A., & Tripathy, D. (2009). Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care, 32(suppl 2), S157-S163.
[16] Sugiwati, S., Kardono, L., & Bintang, M. (2006). a-Glucosidase inhibitory activity and hypoglycemic effect of Phaleria macrocarpa fruit pericarp extracts by oral administration to rats. Journal of Applied Sciences, 6(10), 2312-2316.
[17] Wang, Y., Wang, J., Zhao, Y., Hu, S., Shi, D., & Xue, C. (2016). Fucoidan from sea cucumber Cucumaria frondosa exhibits anti-hyperglycemic effects in insulin resistant mice via activating the PI3K/PKB pathway and GLUT4. Journal of Bioscience and Bioengineering, 121(1), 36-42.
[18] Koh, H. S. A., Lu, J., & Zhou, W. (2020). Structural dependence of sulfated polysaccharide for diabetes management: Fucoidan from Undaria pinnatifida inhibiting α-glucosidase more strongly than α-amylase and amyloglucosidase. Frontiers in Pharmacology, 11, 831.
[19] Hu, S., Xia, G., Wang, J., Wang, Y., Li, Z., & Xue, C. (2014). Fucoidan from sea cucumber protects against high-fat high-sucrose diet-induced hyperglycaemia and insulin resistance in mice. Journal of Functional Foods, 10, 128-138.
[20] Kolsi, R. B. A., Fakhfakh, J., Sassi, S., Elleuch, M., & Gargouri, L. (2018). Physico-chemical characterization and beneficial effects of seaweed sulfated polysaccharide against oxydatif and cellular damages caused by alloxan in diabetic rats. International Journal of Biological Macromolecules, 117, 407-417.
[21] Zarkami, R., & Khazaie, H. (2020). Assessment of habitat suitability of watermilfoil (Myriophyllum spicatum L.) in some aquatic ecosystems of Mazandaran and Guilan provinces. Journal of Plant Research (Iranian Journal of Biology), 33(3), 705-717.
[22] Alavi, M., Tabarsa, M., You, S., & Gavlighi, H. A. (2020). Structural characteristics, molecular properties and immunostimulatory effects of sulfated polysaccharide from freshwater Myriophyllum spicatum L. International Journal of Biological Macromolecules, 153, 951-961.
[23] Brand-Williams, W., Cuvelier, M. E., & Berset, C. L. W. T. (1995). Use of a free radical method to evaluate antioxidant activity. LWT-Food Science and Technology, 28(1), 25-30.
[24] Oyaizu, M. (1986). Studies on products of browning reaction antioxidative activities of products of browning reaction prepared from glucosamine. The Japanese Journal of Nutrition and Dietetics, 44(6), 307-315.
[25] Apostolidis, E., Kwon, Y. I., & Shetty, K. (2007). Inhibitory potential of herb, fruit, and
fungal-enriched cheese against key enzymes linked to type 2 diabetes and hypertension. Innovative Food Science and Emerging Technologies, 8(1), 46–54.
[26] Kumar, S. P., Kekuda, T. P., Vinayaka, K. S., & Sudharshan, S. J. (2009). Anthelmintic and antioxidant efficacy of two macrolichens of Ramalinaceae. Pharmacognosy Journal, 1(4), 238-242.
[27] Molyneux, P. (2004). The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin Journal of Science and Technology, 26(2), 211-219.
[28] Chandini, S. K., Ganesan, P., & Bhaskar, N. (2008). In vitro antioxidant activities of three selected brown seaweeds of India. Food Chemistry, 107(2), 707-713.
[29] Luo, H., Wang, B., Yu, C., Qu, Y., & Su, C. (2010). Evaluation of antioxidant activities of five selected brown seaweeds from China. Journal of Medicinal Plants Research, 4(23), 2557-2565.
[30] Ye, H., Zhou, C., Sun, Y., Zhang, X., Liu, J., Hu, Q., & Zeng, X. (2009). Antioxidant activities in vitro of ethanol extract from brown seaweed Sargassum pallidum. European Food Research and Technology, 230(1), 101-109.
[31] Brayer, G. D., Sidhu, G., Maurus, R., Rydberg, E. H., Braun, C., Wang, Y., ... & Withers, S. G. (2000). Subsite mapping of the human pancreatic α-amylase active site through structural, kinetic, and mutagenesis techniques. Biochemistry, 39(16), 4778-4791
[32] de Melo, E. B., da Silveira Gomes, A., & Carvalho, I. (2006). α-and β-Glucosidase inhibitors: chemical structure and biological activity. Tetrahedron, 62(44), 10277-10302.
[33] Yuan, Y., & Macquarrie D. (2015). Microwave assisted extraction of sulfated polysaccharides (fucoidan) from Ascophyllum nodosum and its antioxidant activity. Carbohydrate Polymers,129, 101-107.
[34] Hou, Y,, Wang, J., Jin, W., Zhang, H., & Zhang Q. (2012). Degradation of Laminaria japonica fucoidan by hydrogen peroxide and antioxidant activities of the degradation products of different molecular weights. Carbohydrate Polymers, 87(1), 153-9.
[35] Kim, K. T., Rioux, L. E., & Turgeon, S. L. (2014). Alpha-amylase and alpha-glucosidase inhibition is differentially modulated by fucoidan obtained from Fucus vesiculosus and Ascophyllum nodosum. Phytochemistry, 98, 27-33.
[36] Nahoum, V., Roux, G., Anton, V., Rougé, P., Puigserver, A., Bischoff, H., ... & Payan, F. (2000). Crystal structures of human pancreatic α-amylase in complex with carbohydrate and proteinaceous inhibitors. Biochemical Journal, 346(1), 201-208.
[37] Maki, K. C., Galant, R., Samuel, P., Tesser, J., Witchger, M. S., Ribaya-Mercado, J. D., ... & Geohas, J. (2007). Effects of consuming foods containing oat β-glucan on blood pressure, carbohydrate metabolism and biomarkers of oxidative stress in men and women with elevated blood pressure. European Journal of Clinical Nutrition, 61(6), 786-795.
[38] L. Zhang, S. Hogan, J. Li, S. Sun, C. Canning, S.J. Zheng, K. Zhou Grape skin extract inhibits mammalian intestinal α-glucosidase activity and suppresses postprandial glycemic response in streptozocin-treated mice Food Chemistry, 126 (2) (2011), pp. 466-470.