Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
권호 표지
DOI QR코드

DOI QR Code

Comparision of antioxidant and anti-inflammatory activities of enzyme assisted hydrolysate from Ecklonia maxima blades and stipe

  • Lee, Hyo-Geun (Department of Marine Life Science, Jeju National University) ;
  • Je, Jun-Geon (Department of Marine Life Science, Jeju National University) ;
  • Hwang, Jin (Department of Marine Life Science, Jeju National University) ;
  • Jayawardena, Thilina U. (Department of Marine Life Science, Jeju National University) ;
  • Nagahawatta, D.P. (Department of Marine Life Science, Jeju National University) ;
  • Lu, Yu An (Department of Marine Life Science, Jeju National University) ;
  • Kim, Hyun-Soo (Marine Biodiversity Institute of Korea) ;
  • Kang, Min-Cheol (Research Group of Food Processing, Korea Food Research Institute) ;
  • Lee, Dae-Sung (Marine Biodiversity Institute of Korea) ;
  • Jeon, You-Jin (Department of Marine Life Science, Jeju National University)
  • Received : 2021.03.20
  • Accepted : 2021.04.26
  • Published : 2021.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

Marine brown seaweeds are a source of functional ingredients with various biological properties. They have been used in the food and functional food industries. Brown seaweeds are divided into three parts of blades, stipe, and root. Normally seaweed blades were used as raw materials for biological research. However, there are limited uses on stipes of Ecklonia maxima (E. maxima) depending on the physicochemical, nutritional, and biological properties. Besides, the comparative studies of two structures of E. maxima, blades and stipe didn't discover previously. This study aimed to compare the potent antioxidant and anti-inflammatory activities of the two structures of E. maxima, blades and stipe in vitro studies to increase the utilization of the two structures of E. maxima. The enzyme-assisted hydrolysate from E. maxima showed significant antioxidant and anti-inflammatory activities. Among them, celluclast-assisted hydrolysate from E. maxima blades (EMBC) and viscozyme-assisted hydrolysate from E. maxima stipe (EMSV) expressed significant protection on hydrogen peroxide-induced oxidative stress. Moreover, EMBC and EMSV treatment remarkably reduced nitric oxide production by downregulation of pro-inflammatory cytokine expressions in lipopolysaccharide-stimulated Raw 264.7 cells. Especially EMBC showed strong inhibition on pro-inflammatory cytokine production compared to EMSV. Taken together research findings suggest that EMBC and EMSV possessed potent antioxidant and anti-inflammatory properties and may be utilized as functional ingredients in the food and functional food sectors.

Keywords

Acknowledgement

This research was financially supported by a grant from the Marine Biotechnology program (20170488) funded by the Ministry of Oceans and Fisheries, Korea.

References

  1. AOAC. Official methods of analysis. 17th ed. Gaithersburg, MD: Association of Official Analytical Chemists; 1999.
  2. Anderson RJ, Carrick P, Levitt GJ, Share A. Holdfasts of adult kelp Ecklonia maxima provide refuges from grazing for recruitment of juvenile kelps. Mar Ecol Prog Ser. 1997;159:265-73. https://doi.org/10.3354/meps159265
  3. Bolton JJ, Anderson RJ, Smit AJ, Rothman MD. South African kelp moving eastwards: the discovery of Ecklonia maxima (Osbeck) Papenfuss at De Hoop Nature Reserve on the south coast of South Africa. Afr J Mar Sci. 2012;34:147-51. https://doi.org/10.2989/1814232X.2012.675125
  4. Bolton JJ, Levitt GJ. Light and temperature requirements for growth and reproduction in gametophytes of Ecklonia maxima (Alariaceae: Laminariales). Mar Biol. 1985;87:131-5. https://doi.org/10.1007/BF00539420
  5. Cardoso SM, Pereira OR, Seca AML, Pinto DCGA, Silva AMS. Seaweeds as preventive agents for cardiovascular diseases: from nutrients to functional foods. Mar Drugs. 2015;13:6838-65. https://doi.org/10.3390/md13116838
  6. Castro LSEPW, Pinheiro TS, Castro AJG, Dore CMPG, da Silva NB, Alves MGCF, et al. Fucose-containing sulfated polysaccharides from brown macroalgae Lobophora variegata with antioxidant, anti-inflammatory, and antitumoral effects. J Appl Phycol. 2014;26:1783-90. https://doi.org/10.1007/s10811-013-0217-y
  7. Carroll AR, Copp BR, Davis RA, Keyzers RA, Prinsep MR. Marine natural products. Nat Prod Rep. 2020;37:175-223. https://doi.org/10.1039/C9NP00069K
  8. Chandler SF, Dodds JH. The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasodine in callus cultures of Solanum laciniatum. Plant Cell Rep. 1983;2:205-8. https://doi.org/10.1007/BF00270105
  9. Chen Z, Tian R, She Z, Cai J, Li H. Role of oxidative stress in the pathogenesis of nonalcoholic fatty liver disease. Free Radic Biol Med. 2020;152:116-41. https://doi.org/10.1016/j.freeradbiomed.2020.02.025
  10. Ciepiela GA, Godlewska A, Jankowska J. The effect of seaweed Ecklonia maxima extract and mineral nitrogen on fodder grass chemical composition. Environ Sci Pollut Res. 2016;23:2301-7. https://doi.org/10.1007/s11356-015-5417-3
  11. Dodgson KS, Price RG. A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem J. 1962;84:106-10. https://doi.org/10.1042/bj0840106
  12. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem. 1956;28:350-6. https://doi.org/10.1021/ac60111a017
  13. Featonby-Smith BC, Van Staden J. Identification and seasonal variation of endogenous cytokinins in Ecklonia maxima (Osbeck) Papenf. Bot Mar. 1984;27:527-30.
  14. Feng D, Aldrich C. Adsorption of heavy metals by biomaterials derived from the marine alga Ecklonia maxima. Hydrometallurgy. 2004;73:1-10. https://doi.org/10.1016/S0304-386X(03)00138-5
  15. Fernando IPS, Sanjeewa KKA, Samarakoon KW, Lee WW, Kim HS, Kim EA, et al. FTIR characterization and antioxidant activity of water soluble crude polysaccharides of Sri Lankan marine algae. Algae. 2017;32:75-86. https://doi.org/10.4490/algae.2017.32.12.1
  16. Fernando IPS, Kim M, Son KT, Jeong Y, Jeon YJ. Antioxidant activity of marine algal polyphenolic compounds: a mechanistic approach. J Med Food. 2016;19:615-28. https://doi.org/10.1089/jmf.2016.3706
  17. Gyuraszova M, Gurecka R, Babickova J, Tothova L. Oxidative stress in the pathophysiology of kidney disease: implications for noninvasive monitoring and identification of biomarkers. Oxid Med Cell Longev. 2020;2020:5478708.
  18. Kannan RRR, Aderogba MA, Ndhlala AR, Stirk WA, Van Staden J. Acetylcholinesterase inhibitory activity of phlorotannins isolated from the brown alga, Ecklonia maxima (Osbeck) Papenfuss. Food Res Int. 2013;54:1250-4. https://doi.org/10.1016/j.foodres.2012.11.017
  19. Kang MC, Lee HG, Choi HD, Jeon YJ. Antioxidant properties of a sulfated polysaccharide isolated from an enzymatic digest of Sargassum thunbergii. Int J Biol Macromol. 2019;132:142-9. https://doi.org/10.1016/j.ijbiomac.2019.03.178
  20. Kim EA, Lee SH, Ko CI, Cha SH, Kang MC, Kang SM, et al. Protective effect of fucoidan against AAPH-induced oxidative stress in zebrafish model. Carbohydr Polym. 2014;102:185-91. https://doi.org/10.1016/j.carbpol.2013.11.022
  21. Kocira A, Swieca M, Kocira S, Zlotek U, Jakubczyk A. Enhancement of yield, nutritional and nutraceutical properties of two common bean cultivars following the application of seaweed extract (Ecklonia maxima). Saudi J Biol Sci. 2018;25:563-71. https://doi.org/10.1016/j.sjbs.2016.01.039
  22. Kulkarni MG, Rengasamy KRR, Pendota SC, Gruz J, Plackova L, Novak O, et al. Bioactive molecules derived from smoke and seaweed Ecklonia maxima showing phytohormone-like activity in Spinacia oleracea L. New Biotechnol. 2019;48:83-9. https://doi.org/10.1016/j.nbt.2018.08.004
  23. Lee HG, Kim HS, Oh JY, Lee DS, Yang HW, Kang MC, et al. Potential antioxidant properties of enzymatic hydrolysates from Stichopus japonicus against hydrogen peroxide-induced oxidative stress. Antioxidants. 2021;10:110. https://doi.org/10.3390/antiox10010110
  24. Lee YH, Cheng FY, Chiu HW, Tsai JC, Fang CY, Chen CW, et al. Cytotoxicity, oxidative stress, apoptosis and the autophagic effects of silver nanoparticles in mouse embryonic fibroblasts. Biomaterials. 2014;35:4706-15. https://doi.org/10.1016/j.biomaterials.2014.02.021
  25. Libby P. Inflammatory mechanisms: the molecular basis of inflammation and disease. Nutr Rev. 2007;65:S140-6. https://doi.org/10.1111/j.1753-4887.2007.tb00352.x
  26. Lordan S, Ross RP, Stanton C. Marine bioactives as functional food ingredients: potential to reduce the incidence of chronic diseases. Mar Drugs. 2011;9:1056-100. https://doi.org/10.3390/md9061056
  27. Mayombo NAS, Majewska R, Smit AJ. Diatoms associated with two South African kelp species: Ecklonia maxima and Laminaria pallida. Afr J Mar Sci. 2019;41:221-9. https://doi.org/10.2989/1814232X.2019.1592778
  28. Mwangi HM, Van Der Westhuizen J, Marnewick J, Mabusela WT, Kabanda MM, Ebenso EE. Isolation, identification and radical scavenging activity of phlorotannin derivatives from brown algae, Ecklonia maxima: an experimental and theoretical study. Free Radic Antioxid. 2013;3:S1-10.
  29. Newman DJ, Cragg GM. Marine natural products and related compounds in clinical and advanced preclinical trials. J Nat Prod. 2004;67:1216-38. https://doi.org/10.1021/np040031y
  30. Nguyen TT, Heimann K, Zhang W. Protein recovery from underutilised marine bioresources for product development with nutraceutical and pharmaceutical bioactivities. Mar Drugs. 2020;18:391. https://doi.org/10.3390/md18080391
  31. Olasehinde TA, Olaniran AO, Okoh AI. Macroalgae as a valuable source of naturally occurring bioactive compounds for the treatment of Alzheimer's disease. Mar Drugs. 2019;17:609. https://doi.org/10.3390/md17110609
  32. Papenfus HB, Stirk WA, Finnie JF, Van Staden J. Seasonal variation in the polyamines of Ecklonia maxima. Bot Mar. 2012;55:539-46. https://doi.org/10.1515/bot-2012-0150
  33. Papenfuss GF. Studies of South African Phaeophyceae. I. Ecklonia maxima, Laminaria pallida, Macrocystis pyrifera. Am J Bot. 1942;29:15-24. https://doi.org/10.1002/j.1537-2197.1942.tb13966.x
  34. Penalver R, Lorenzo JM, Ros G, Amarowicz R, Pateiro M, Nieto G. Seaweeds as a functional ingredient for a healthy diet. Mar Drugs. 2020;18:301. https://doi.org/10.3390/md18060301
  35. Pereira F. Have marine natural product drug discovery efforts been productive and how can we improve their efficiency? Expert Opin Drug Discov. 2019;14:717-22. https://doi.org/10.1080/17460441.2019.1604675
  36. Pereira SA, Kimpara JM, Valenti WC. A bioeconomic analysis of the potential of seaweed Hypnea pseudomusciformis farming to different targeted markets. Aquac Econ Manag. 2020;24:507-25. https://doi.org/10.1080/13657305.2020.1803445
  37. Podkowinska A, Formanowicz D. Chronic kidney disease as oxidative stress- and inflammatory-mediated cardiovascular disease. Antioxidants. 2020;9:752. https://doi.org/10.3390/antiox9080752
  38. Rekatsina M, Paladini A, Piroli A, Zis P, Pergolizzi JV, Varrassi G. Pathophysiology and therapeutic perspectives of oxidative stress and neurodegenerative diseases: a narrative review. Adv Ther. 2020;37:113-39.
  39. Rengasamy KRR, Aderogba MA, Amoo SO, Stirk WA, Van Staden J. Potential antiradical and alpha-glucosidase inhibitors from Ecklonia maxima (Osbeck) Papenfuss. Food Chem. 2013;141:1412-5. https://doi.org/10.1016/j.foodchem.2013.04.019
  40. Rothman MD, Anderson RJ, Smit AJ. The effects of harvesting of the South African kelp (Ecklonia maxima) on kelp population structure, growth rate and recruitment. Paper presented at: 18th International Seaweed Symposium; 2004 Jun 20-25; Bergen, Norway.
  41. Rothman MD, Bolton JJ, Stekoll MS, Boothroyd CJT, Kemp FA, Anderson RJ. Geographical variation in morphology of the two dominant kelp species, Ecklonia maxima and Laminaria pallida (Phaeophyceae, Laminariales), on the west coast of Southern Africa. J Appl Phycol. 2017;29:2627-39. https://doi.org/10.1007/s10811-017-1255-7
  42. Rouphael Y, De Micco V, Arena C, Raimondi G, Colla G, De Pascale S. Effect of Ecklonia maxima seaweed extract on yield, mineral composition, gas exchange, and leaf anatomy of zucchini squash grown under saline conditions. J Appl Phycol. 2017;29:459-70. https://doi.org/10.1007/s10811-016-0937-x
  43. Wang L, Jayawardena TU, Yang HW, Lee HG, Jeon YJ. The potential of sulfated polysaccharides isolated from the brown seaweed Ecklonia maxima in cosmetics: antioxidant, anti-melanogenesis, and photoprotective activities. Antioxidants. 2020;9:724. https://doi.org/10.3390/antiox9080724
  44. Wang L, Jeon YJ, Kim JI. In vitro and in vivo anti-inflammatory activities of a sterol-enriched fraction from freshwater green alga, Spirogyra sp. Fish Aquat Sci. 2020;23:1-9. https://doi.org/10.1186/s41240-020-0147-y
  45. Wang J, Zheng J, Huang C, Zhao J, Lin J, Zhou X, et al. Eckmaxol, a phlorotannin extracted from Ecklonia maxima, produces anti-β-amyloid oligomer neuroprotective effects possibly via directly acting on glycogen synthase kinase 3β. ACS Chem Neurosci. 2018;9:1349-56. https://doi.org/10.1021/acschemneuro.7b00527
  46. Waterborg JH. The Lowry method for protein quantitation. In: Walker JM, editor. The protein protocols handbook. New York, NY : Humana Press; 2009. p. 7-10.
  47. Zhou X, Yi M, Ding L, He S, Yan X. Isolation and purification of a neuroprotective phlorotannin from the marine algae Ecklonia maxima by size exclusion and high-speed counter-current chromatography. Mar Drugs. 2019;17:212. https://doi.org/10.3390/md17040212