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A comparative study of Sargassum horneri Korea and China strains collected along the coast of Jeju Island South Korea: its components and bioactive properties

  • Kim, Hyun-Soo (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University) ;
  • Sanjeewa, K.K. Asanka (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University) ;
  • Fernando, I.P. Shanura (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University) ;
  • Ryu, BoMi (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University) ;
  • Yang, Hey-Won (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University) ;
  • Ahn, Ginnae (Department of Marine Bio-Food Sciences, Chonnam National University) ;
  • Kang, Min Cheol (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University) ;
  • Heo, Soo-Jin (Jeju International Marine Science Center for Research & Education, Korea Institute of Ocean Science and Technology) ;
  • Je, Jun-Geon (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University) ;
  • Jeon, You-Jin (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University)
  • Received : 2018.02.13
  • Accepted : 2018.11.15
  • Published : 2018.12.15

Abstract

Sargassum horneri is edible brown seaweed abundant along the coasts of Jeju Island, South Korea. In addition to the native S. horneri population, a large amount of S. horneri has been found to invade Jeju Island from the east coast of China. Thus, S. horneri of both Korea (SK) and China (SC) strains now inhabits along with the shore of Jeju Island and have become a threat to the coastal biodiversity. However, they could be used in obtaining functional ingredients for industrial level applications provided an optimized cost effective strategy. In the present study, we compared SK and SC strains for the extraction efficiency, components, antioxidant, and anti-inflammatory properties of 80% methanolic extracts and their partially purified fractions. According to the results, two strains indicated similar bioactive properties such as DPPH and alkyl radical scavenging activity as well as anti-inflammatory activities on lipopolysaccharide-stimulated RAW 264.7 cells. The yield of 80% methanol extract from SC was higher than SK. However, the yields of the ethyl acetate and chloroform fractions from SK were higher than those of SC strain. The major peaks in the high-performance liquid chromatography chromatograms, which was identified as Apo-9 fucoxanthinone, indicated that both methanolic extracts of SK and SC contains major target peaks but with different amounts. This study might be useful for developing functional materials from SC and SK in future.

Keywords

References

  1. Ahn, G. -N., Kim, K. -N., Cha, S. -H., Song, C. -B., Lee, J., Heo, M. -S., Yeo, I. -K., Lee, N. -H., Jee, Y. -H., Kim, J. -S., Heu, M. -S. & Jeon, Y. -J. 2007. Antioxidant activities of phlorotannins purified from Ecklonia cava on free radical scavenging using ESR and $H_2O_2$-mediated DNA damage. Eur. Food Res. Technol. 226:71-79. https://doi.org/10.1007/s00217-006-0510-y
  2. Association of Official Analytical Chemists. 1998. Official methods of analysis of AOAC international. 16th ed. Vol. 2. Association of Official Analytical Chemists, Washington, DC, 1018 pp.
  3. Chandler, S. F. & Dodds, J. H. 1983. The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasodine in callus cultures of solanum laciniatum. Plant Cell Rep. 2:205-208. https://doi.org/10.1007/BF00270105
  4. Cho, J. Y. 2013. Antifouling chromanols isolated from brown alga Sargassum horneri. J. Appl. Phycol. 25:299-309. https://doi.org/10.1007/s10811-012-9864-7
  5. Choi, W. -C., Reid, S. N. S., Ryu, J. -K., Kim, Y., Jo, Y. -H. & Jeon, B. H. 2016. Effects of ${\gamma}$-aminobutyric acid-enriched fermented sea tangle (Laminaria japonica) on brain derived neurotrophic factor-related muscle growth and lipolysis in middle aged women. Algae 31:175-187. https://doi.org/10.4490/algae.2016.31.6.12
  6. DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A. & Smith, F. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28:350-356. https://doi.org/10.1021/ac60111a017
  7. Esser, N., Legrand-Poels, S., Piette, J., Scheen, A. J. & Paquot, N. 2014. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res. Clin. Pract. 105:141-150. https://doi.org/10.1016/j.diabres.2014.04.006
  8. Fenical, W. & McConnell, O. 1975. Chromazonarol and isochromazonarol, new chromanols from the brown seaweed Dictyopteris undulata (zonarioides). Experientia 31:1004-1005. https://doi.org/10.1007/BF02326923
  9. Fernando, I. P. S., Kim, H. -S., Sanjeewa, K. K. A., Oh, J. -Y., Jeon, Y. -J. & Lee, W. W. 2017a. Inhibition of inflammatory responses elicited by urban fine dust particles in keratinocytes and macrophages by diphlorethohydroxycarmalol isolated from a brown alga Ishige okamurae. Algae 32:261-273. https://doi.org/10.4490/algae.2017.32.8.14
  10. Fernando, I. P. S., Kim, M., Son, K. -T., Jeong, Y. & Jeon, Y. -J. 2016. Antioxidant activity of marine algal polyphenolic compounds: a mechanistic approach. J. Med. Food 19:615-628. https://doi.org/10.1089/jmf.2016.3706
  11. Fernando, I. P. S., Sanjeewa, K. K. A., Samarakoon, K. W., Lee, W. W., Kim, H. -S., Kim, E. -A., Gunasekara, U. K. D. S. S., Abeytunga, D. T. U., Nanayakkara, C., de Silva, E. D., Lee, H. -S. & Jeon, Y. -J. 2017b. FTIR characterization and antioxidant activity of water soluble crude polysaccharides of Sri Lankan marine algae. Algae 32:75-86. https://doi.org/10.4490/algae.2017.32.12.1
  12. Heo, S. -J., Cha, S. -H., Lee, K. -W., Cho, S. K. & Jeon, Y. -J. 2005. Antioxidant activities of chlorophyta and phaeophyta from Jeju Island. Algae 20:251-260. https://doi.org/10.4490/ALGAE.2005.20.3.251
  13. Heo, S. -J., Yoon, W. -J., Kim, K. -N., Ahn, G. -N., Kang, S. -M., Kang, D. -H., Affan, A., Oh, C., Jung, W. -K. & Jeon, Y. -J. 2010. Evaluation of anti-inflammatory effect of fucoxanthin isolated from brown algae in lipopolysaccharide- stimulated RAW 264.7 macrophages. Food Chem. Toxicol. 48:2045-2051. https://doi.org/10.1016/j.fct.2010.05.003
  14. Hiramoto, K., Johkoh, H., Sako, K. -I. & Kikugawa, K. 1993. DNA breaking activity of the carbon-centered radical generated from 2,2'-azobis(2-amidinopropane) hydrochloride (AAPH). Free Radic. Res. Commun. 19:323-332. https://doi.org/10.3109/10715769309056521
  15. Jang, J. -H., Lee, J. -H., Chand, H. S., Lee, J. -S., Lin, Y., Weathington, N., Mallampalli, R., Jeon, Y. -J. & Nyunoya, T. 2016. Apo-9′-fucoxanthinone extracted from Undariopsis peteseniana protects oxidative stress-mediated apoptosis in cigarette smoke-exposed human airwat epithelial cells. Mar. Drugs 14:140. https://doi.org/10.3390/md14070140
  16. Kim, E. -A., Kim, S. -Y., Ye, B. -R., Kim, J., Ko, S. -C., Lee, W. W., Kim, K. -N., Choi, I. -W., Jung, W. -K. & Heo, S. -J. 2018. Anti-inflammatory effect of Apo-9'-fucoxanthinone via inhibition of MAPKs and NF-kB signaling pathway in LPS-stimulated RAW 264.7 macrophges and zebrafish model. Int. Immunopharmacol. 59:339-346. https://doi.org/10.1016/j.intimp.2018.03.034
  17. Ko, S. -C., Lee, M., Lee, J. -H., Lee, S. -H., Lim, Y. & Jeon, Y. -J. 2013. Dieckol, a phlorotannin isolated from a brown seaweed, Ecklonia cava, inhibits adipogenesis through AMP-activated protein kinase (AMPK) activation in 3T3-L1 preadipocytes. Environ. Toxicol. Pharmacol. 36:1253-1260. https://doi.org/10.1016/j.etap.2013.10.011
  18. Kubo, N., Douke, A., Nishigaki, T. & Tsuji, G. 2016. Development and characterization of simple sequence repeat markers for genetic analyses of Sargassum horneri (Sargassaceae, Phaeophyta) populations in Kyoto, Japan. J. Appl. Phycol. 29:1729-1733.
  19. Kundu, S. & Kawamura, K. 2014. Seasonal variations of stable carbon isotopic composition of bulk aerosol carbon from Gosan site, Jeju Island in the East China Sea. Atmos. Environ. 94:316-322. https://doi.org/10.1016/j.atmosenv.2014.05.045
  20. Lee, J. -H., Ko, J. -Y., Samarakoon, K., Oh, J. -Y., Heo, S. -J., Kim, C. -Y., Nah, J. -W., Jang, M. -K., Lee, J. -S. & Jeon, Y. -J. 2013. Preparative isolation of sargachromanol E from Sargassum siliquastrum by centrifugal partition chromatography and its anti-inflammatory activity. Food Chem. Toxicol. 62:54-60. https://doi.org/10.1016/j.fct.2013.08.010
  21. Leiro, J., Alvarez, E., Garcia, D. & Orallo, F. 2002. Resveratrol modulates rat macrophage functions. Int. Immuno-pharmacol. 2:767-774. https://doi.org/10.1016/S1567-5769(02)00014-0
  22. Lin, M. T. & Beal, M. F. 2006. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787-795. https://doi.org/10.1038/nature05292
  23. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65:55-63. https://doi.org/10.1016/0022-1759(83)90303-4
  24. Nanjo, F., Goto, K., Seto, R., Suzuki, M., Sakai, M. & Hara, Y. 1996. Scavenging effects of tea catechins and their derivatives on 1,1-diphenyl-2-picrylhydrazyl radical. Free Radic. Biol. Med. 21:895-902. https://doi.org/10.1016/0891-5849(96)00237-7
  25. Pang, S. J., Liu, F., Shan, T. F., Gao, S. Q. & Zhang, Z. H. 2009. Cultivation of the brown alga Sargassum horneri: sexual reproduction and seedling production in tank culture under reduced solar irradiance in ambient temperature. J. Appl. Phycol. 21:413-422. https://doi.org/10.1007/s10811-008-9386-5
  26. Park, H. -J., Lee, M. -S., Shim, H. S., Lee, G. -R., Chung, S. Y., Kang, Y. M., Lee, B. -J., Seo, Y. B., Kim, K. S. & Shim, I. 2016. Fermented Saccharina japonica (Phaeophyta) improves neuritogenic activity and TMT-induced cognitive deficits in rats. Algae 31:73-84. https://doi.org/10.4490/algae.2016.31.11.10
  27. Pesic, M. & Greten, F. R. 2016. Inflammation and cancer: tissue regeneration gone awry. Curr. Opin. Cell Biol. 43:55-61. https://doi.org/10.1016/j.ceb.2016.07.010
  28. Preeprame, S., Hayashi, K., Lee, J. -B., Sankawa, U. & Hayashi, T. 2001. A novel antivirally active fucan sulfate derived from an edible brown alga, Sargassum horneri. Chem. Pharm. Bull. (Tokyo) 49:484-485. https://doi.org/10.1248/cpb.49.484
  29. Sanjeewa, K. K. A., Fernando, I. P. S., Kim, E. -A., Ahn, G., Jee, Y. & Jeon, Y. -J. 2017a. Anti-inflammatory activity of a sulfated polysaccharide isolated from an enzymatic digest of brown seaweed Sargassum horneri in RAW 264.7 cells. Nutr. Res. Pract. 11:3-10. https://doi.org/10.4162/nrp.2017.11.1.3
  30. Sanjeewa, K. K. A., Fernando, I. P. S., Kim, S. -Y., Kim, H. -S., Ahn, G., Jee, Y. & Jeon, Y. -J. 2018. In vitro and in vivo anti-inflammatory activities of high molecular weight sulfated polysaccharide: containing fucose separated from Sargassum horneri: short communication. Int. J. Biol. Macromol. 107:803-807. https://doi.org/10.1016/j.ijbiomac.2017.09.050
  31. Sanjeewa, K. K. A., Fernando, I. P. S., Samarakoon, K. W., Lakmal, H. H. C., Kim, E. -A., Kwon, O. -N., Dilshara, M. G., Lee, J. -B. & Jeon, Y. -J. 2016. Anti-inflammatory and anti-cancer activities of sterol rich fraction of cultured marine microalga Nannochloropsis oculata. Algae 31: 277-287. https://doi.org/10.4490/algae.2016.31.6.29
  32. Sanjeewa, K. K. A., Lee, J. -S., Kim, W. -S. & Jeon, Y. -J. 2017b. The potential of brown-algae polysaccharides for the development of anticancer agents: an update on anticancer effects reported for fucoidan and laminaran. Carbohydr. Polym. 177:451-459. https://doi.org/10.1016/j.carbpol.2017.09.005
  33. Su, L., Shan, T., Pang, S. & Li, J. 2018. Analyses of the genetic structure of Sargassum horneri in the Yellow Sea: implications of the temporal and spatial relations among floating and benethic populations. J. Appl. Phycol. 30:1417-1424. https://doi.org/10.1007/s10811-017-1296-y
  34. Wang, G., Sun, J., Liu, G., Wang, L., Yu, J., Liu, T., Chi, S., Liu, C., Guo, H. & Wang, X. 2014. Comparative analysis on transcriptome sequencings of six Sargassum species in China. Acta Oceanol. Sin. 33:37-44.
  35. Wang, T., Jonsdottir, R., Liu, H., Gu, L., Kristinsson, H. G., Raghavan, S. & Olafsdottir, G. 2012. Antioxidant capacities of phlorotannins extracted from the brown algae Fucus vesiculosus. J. Agric. Food Chem. 60:5874-5883. https://doi.org/10.1021/jf3003653
  36. Wijesinghe, W. A. J. P. & Jeon, Y. -J. 2012. Enzyme-assistant extraction (EAE) of bioactive components: a useful approach for recovery of industrially important metabolites from seaweeds: a review. Fitoterapia 83:6-12. https://doi.org/10.1016/j.fitote.2011.10.016
  37. Yoshioka, H., Ishida, M., Nishi, K., Oda, H., Toyohara, H. & Sugahara, T. 2014. Studies on anti-allergic activity of Sargassum horneri extract. J. Funct. Foods 10:154-160. https://doi.org/10.1016/j.jff.2014.06.002
  38. Zhang, L., Zhao, C., Shi, D., Hu, W., Wei, J. & Chang, Y. 2017. Gulfweed Sargassum horneri is an alternative diet for aquaculture of juvenile sea urchins Strongylocentrotus intermedius in summer. Aquac. Int. 25:905-914. https://doi.org/10.1007/s10499-016-0088-8

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