Advertisement

Bioactivities of Nizamuddinia zanardinii sulfated polysaccharides extracted by enzyme, ultrasound and enzyme-ultrasound methods

  • Mehdi Alboofetileh
  • Masoud RezaeiEmail author
  • Mehdi Tabarsa
  • SangGuan You
Original Article
  • 9 Downloads

Abstract

Sulfated polysaccharide (fucoidan) was isolated from Nizamuddinia zanardinii by enzyme (alcalase), ultrasonic and enzyme-ultrasonic methods. The extracted fucoidans were assessed for their chemical compositions, molecular characteristics, anticancer and immunomodulatory activities. Enzyme-ultrasonic isolated fucoidan showed the maximum extraction yield (7.87%) while that obtained by ultrasonic had the minimum value (3.6%). fucoidans were composed of different levels of carbohydrates (52.78–58.65%), proteins (6.98–8.91%), sulfates (21.78–29.6%) and uronic acids (0.42–1.08%). The weight mean average molecular weight of fucoidans varied between 443.7 and 1020.85 kDa. The polysaccharide chains were consisted of fucose, galactose, glucose, mannose and xylose. All the recovered fucoidans showed strong growth inhibition against HeLa and Hep-G2 cancer cells. The isolated fucoidans were non-toxic and considerably stimulated the macrophage cells to release nitric oxide. Enzyme extraction produced fucoidan with the most macrophage stimulation capacity (> 42 µmol). These results suggested that enzyme treatment preserved more sulfate groups in fucoidan structure influencing its anticancer and immunostimulatory activities.

Keywords

Nizamuddinia zanardinii Fucoidan Enzyme extraction Molecular weight Sulfate group 

Notes

Acknowledgements

Authors would like to thank the Iran National Science Foundation (INSF) for support of this research.

References

  1. Bahramzadeh S, Tabarsa M, SangGuan You S, Li C, Bita S (2019) Purification, structural analysis and mechanism of murine macrophage cell activation by sulfated polysaccharides from Cystoseira indica. Carbohydra Polym 205:261–270CrossRefGoogle Scholar
  2. Borazjani NJ, Tabarsa M, You S, Rezaei M (2017) Improved immunomodulatory and antioxidant properties of unrefined fucoidans from Sargassum angustifolium by hydrolysis. J Food Sci Technol 54(12):4016–4025CrossRefGoogle Scholar
  3. Borazjani NJ, Tabarsa M, You S, Rezaei M (2018) Purification, molecular properties, structural characterization, and immunomodulatory activities of water soluble polysaccharides from Sargassum angustifolium. Int J Biol Macromol 109:793–802CrossRefGoogle Scholar
  4. Cheng Z, Song H, Yang Y, Liu Y, Liu Z, Hu H, Zhang Y (2015) Optimization of microwave-assisted enzymatic extraction of polysaccharides from the fruit of Schisandra chinensis Baill. Int J Biol Macromol 76:161–168CrossRefGoogle Scholar
  5. Cho ML, Lee BY, You SG (2011) Relationship between oversulfation and conformation of low and high molecular weight fucoidans and evaluation of their in vitro anticancer activity. Molecules 16(1):291–297CrossRefGoogle Scholar
  6. Cho M, Lee DJ, Kim JK, You S (2014) Molecular characterization and immunomodulatory activity of sulfated fucans from Agarum cribrosum. Carbohydr Polym 113:507–514CrossRefGoogle Scholar
  7. Dodgson KS, Price RG (1962) A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem J 84:106–110CrossRefGoogle Scholar
  8. Dong H, Lin S, Zhang Q, Chen H, Lan W, Li H, He J, Qin W (2016) Effect of extraction methods on the properties and antioxidant activities of Chuanminshen violaceum polysaccharides. Int J Biol Macromol 93:179–185CrossRefGoogle Scholar
  9. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  10. Easson MW, Condon B, Dien BS, Iten L, Slopek R, Yoshioka-Tarver M, Lambert A, Smith J (2011) The application of ultrasound in the enzymatic hydrolysis of switchgrass. Appl Biochem Biotechnol 165:1322–1331CrossRefGoogle Scholar
  11. Fan T, Hu J, Fu L, Zhang L (2015) Optimization of enzymolysis-ultrasonic assisted extraction oF polysaccharides from Momordica charabtia L. by response surface methodology. Carbohydr Polym 115:701–706CrossRefGoogle Scholar
  12. Filisetti-Cozzi TMCC, Carpita NC (1991) Measurement of uronic acids without interference from neutral sugars. Anal Biochem 197:157–162CrossRefGoogle Scholar
  13. Green LC, Wanger DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15 N] nitrate in biological fluids. Anal Biochem 126:131–136CrossRefGoogle Scholar
  14. Guillard CL, Dumay J, Donnay-Moreno C, Bruzac S, Ragon JY, Fleurence J, Bergé JP (2015) Ultrasound-assisted extraction of R-phycoerythrin from Grateloupia turuturu with and without enzyme addition. Algal Res 12:522–528CrossRefGoogle Scholar
  15. Guillard CL, Bergé JP, Donnay-Moreno C, Bruzac S, Ragon JY, Baron R, Fleurence J, Dumay J (2016) Soft liquefaction of the red seaweed Grateloupia turuturu Yamada by ultrasound-assisted enzymatic hydrolysis process. J Appl Phycol 28(4):2575–2585CrossRefGoogle Scholar
  16. Hayashi K, Nakano T, Hashimoto M, Kanekiyo K, Hayashi T (2008) Defensive effects of a fucoidan from brown alga Undaria pinnatifida against herpes simplex virus infection. Int Immunopharm 8(1):109–116CrossRefGoogle Scholar
  17. Huang CY, Wu SJ, Yang WN, Kuan AW, Chen CY (2016) Antioxidant activities of crude extracts of Fucoidan extracted from Sargassum glaucescens by a compressional-puffing-hydrothermal extraction process. Food Chem 197:1121–1129CrossRefGoogle Scholar
  18. Kadam SU, Tiwari BK, Smyth TJ, O’Donnell CP (2015) Optimization of ultrasound assisted extraction of bioactive components from brown seaweed Ascophyllum nodosum using response surface methodology. Ultrason Sonochem 23:308–316CrossRefGoogle Scholar
  19. Kantachumpoo A, Chirapart A (2010) Components and antimicrobial activity of polysaccharides extracted from Thai brown seaweeds. Kasetsart J 44:220–233Google Scholar
  20. Kim KG, Lee BY (2013) Fucoidan from the sporophyll of Undaria pinnatifida suppresses adipocyte differentiation by inhibition of inflammation-related cytokines in 3T3-L1 cells. Nutr Res 32(6):439–447CrossRefGoogle Scholar
  21. Lee SH, Ko CI, Ahn G, You S, Kim JS, Heu MS, Kim J, Jee Y, Jeon YJ (2012) Molecular characteristics and anti-inflammatory activity of the fucoidan extracted from Ecklonia cava. Carbohydr Polym 89(2):599–606CrossRefGoogle Scholar
  22. Lim SJ, Aida WMW, Maskat MY, Mamot S, Ropien J, Mohd DM (2014) Isolation and antioxidant capacity of fucoidan from selected Malaysian seaweeds. Food Hydrocol 42(2):280–288CrossRefGoogle Scholar
  23. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  24. Nishino T, Aizu Y, Nagumo T (1991) The relationship between the molecular weight and the anticoagulant activity of two types of fucan sulfates from the brown seaweed Ecklonia kurome. Agric Biol Chem 55(3):791–796Google Scholar
  25. Quitain AT, Kai T, Sasaki M, Goto M (2013) Microwave − hydrothermal extraction and degradation of fucoidan from supercritical carbon dioxide Deoiled Undaria pinnatida. Ind Eng Chem Res 52(23):7940–7946CrossRefGoogle Scholar
  26. Rostami Z, Tabarsa M, You S, Rezaei M (2017) Relationship between molecular weights and biological properties of alginates extracted under different methods from Colpomenia peregrina. Process Biochem 58:289–297CrossRefGoogle Scholar
  27. Rostami Z, Tabarsa M, You S, Rezaei M (2018) Structural characterization and RAW264.7 murine macrophage stimulating activity of a fucogalactoglucan from Colpomenia peregrina. J Food Sci Technol 55(11):4650–4660CrossRefGoogle Scholar
  28. Shang H, Chen S, Li R, Zhou H, Wu H, Song H (2018) Influences of extraction methods on physicochemical characteristics and activities of Astragalus cicer L. polysaccharides. Process Biochem 73:220–227CrossRefGoogle Scholar
  29. Sumere BR, de Souza MC, dos Santos MP, Bezerra RMN, da Cunha DT, Martinez J, Rostagno MA (2018) Combining pressurized liquids with ultrasound to improve the extraction of phenolic compounds from pomegranate peel (Punica granatum L.). Ultrason Sonochem 48:151–162CrossRefGoogle Scholar
  30. Takeda K, Tomimori K, Kimura R, Ishikawa C, Nowling TK, Mori N (2012) Anti-tumor activity of fucoidan is mediated by nitric oxide released from macrophages. Int J Oncol 40:251–260Google Scholar
  31. Wang J, Zhang Q, Zhang Z, Li Z (2008) Antioxidant activity of sulfated polysaccharide fractions extracted from Laminaria japonica. Int J Biol Macromol 42(2):127–132CrossRefGoogle Scholar
  32. Wang J, Jin W, Zhang W, Hou Y, Zhang H, Zhang Q (2013) Hypoglycemic property of acidic polysaccharide extracted from Saccharina japonica and its potential mechanism. Carbohydr Polym 95(1):143–147CrossRefGoogle Scholar
  33. Wu H, Zhu J, Diao W, Wang C (2014) Ultrasound-assisted enzymatic extraction and antioxidant activity of polysaccharides from pumpkin (Cucurbita moschata). Carbohydr Polym 113:314–324CrossRefGoogle Scholar
  34. Yang C, Chung D, Shin IS, Lee H, Kim J, Lee Y, You S (2008) Effects of molecular weight and hydrolysis conditions on anticancer activity of fucoidans from sporophyll of Undaria pinnatifida. Int J Biol Macromol 43:433–437CrossRefGoogle Scholar
  35. You Q, Yin X, Zhao Y (2013) Enzyme assisted extraction of polysaccharides from the fruit of Cornus officinalis. Carbohydr Polym 98(1):607–610CrossRefGoogle Scholar
  36. Zeng H, Zhang Y, Lin S, Jian Y, Miao S, Zheng B (2015) Ultrasonic–microwave synergistic extraction (UMSE) and molecular weight distribution of polysaccharides from Fortunella margarita (Lour.) Swingle. Sep Purif Technol 144:97–106CrossRefGoogle Scholar
  37. Zhao YM, Wang J, Wu ZG, Yang JM, Li W, Shen LX (2016) Extraction, purification and anti-proliferative activities of polysaccharides from Lentinus edodes. Int J Biol Macromol 93:136–144CrossRefGoogle Scholar

Copyright information

© Association of Food Scientists & Technologists (India) 2019

Authors and Affiliations

  1. 1.Department of Seafood Processing, Faculty of Marine SciencesTarbiat Modares UniversityNoorIran
  2. 2.Department of Marine Food Science and TechnologyGangneung-Wonju National UniversityGangneungRepublic of Korea

Personalised recommendations