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The Korean Society of Phycology (한국조류학회(藻類))
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Antioxidant activity and cell protective effect of loliolide isolated from Sargassum ringgoldianum subsp. coreanum

  • Yang, Xiudong (Department of Marine Life Science, Jeju National University) ;
  • Kang, Min-Cheol (Department of Marine Life Science, Jeju National University) ;
  • Lee, Ki-Wan (Department of Marine Life Science, Jeju National University) ;
  • Kang, Sung-Myung (Department of Marine Life Science, Jeju National University) ;
  • Lee, Won-Woo (Department of Marine Life Science, Jeju National University) ;
  • Jeon, You-Jin (Department of Marine Life Science, Jeju National University)
  • Received : 2011.03.08
  • Accepted : 2011.05.25
  • Published : 2011.06.15
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Abstract

A monoterpene lactone, loliolide was successively isolated from brown seaweed, Sargassum ringgoldianum subsp. coreanum using column chromatography and high-performance liquid chromatography. The structure of the isolated compound was determined by comparison of EIMS and NMR spectral data with the previously published data. The antioxidant activities of loliolide were also evaluated by DPPH and $H_2O_2$ radical and intracellular reactive oxygen species scavenging assays, and it showed moderate activities in all antioxidant assays. Furthermore, loliolide was found to exert positive dose-dependent effects in the protective effects against $H_2O_2$-induced cell damage which were determined via MTT, Hoechst staining assays and cell cycle analysis. This is the first study on chemical constituent of this seaweed according to our best knowledge. These results clearly indicated that loliolide isolated from Sargassum ringgoldianum subsp. coreanum can protect the cells against $H_2O_2$-induced cell damage or apoptosis.

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References

  1. Athukorala, Y. & Jeon, Y. -J. 2005. Screening for angiotensin 1-converting enzyme inhibitory activity of Ecklonia cava. J. Food Sci. Nutr. 10:134-139. https://doi.org/10.3746/jfn.2005.10.2.134
  2. Athukorala, Y., Lee, K. -W., Kim, S. -K. & Jeon, Y. -J. 2007. Anticoagulant activity of marine green and brown algae collected from Jeju Island in Korea. Bioresour. Technol. 98:1711-1716. https://doi.org/10.1016/j.biortech.2006.07.034
  3. Blois, M. S. 1958. Antioxidant determination by the use of a stable free radical. Nature 181:1199-1200. https://doi.org/10.1038/1811199a0
  4. Chang, H. W., Jang, K. H., Lee, D., Kang, H. R., Kim, T. -Y., Lee, B. H., Choi, B. W., Kim, S. & Shin, J. 2008. Monoglycerides from the brown alga Sargassum sagamianum: isolation, synthesis, and biological activity. Bioorg. Med. Chem. Lett. 18:3589-3592. https://doi.org/10.1016/j.bmcl.2008.05.008
  5. Gschwind, M. & Huber, G. 1995. Apoptotic cell death induced by β-amyloid 1-42 peptide is cell type dependent. J. Neurochem. 65:292-300.
  6. Heo, S. -J., Cha, S. -H., Lee, K. -W., Cho, S. K. & Jeon, Y. -J. 2005a. Antioxidant activities of chlorophyta and phaeophyta from Jeju Island. Algae 20:251-260. https://doi.org/10.4490/ALGAE.2005.20.3.251
  7. Heo, S. -J., Park, E. -J., Lee, K. -W. & Jeon, Y. -J. 2005b. Antioxidant activities of enzymatic extracts from brown seaweeds. Bioresour. Technol. 96:1613-1623. https://doi.org/10.1016/j.biortech.2004.07.013
  8. Hodges, R. & Porte, A. L. 1964. The structure of loliolide: A terpene from Lolium perenne. Tetrahedron 20:1463-1467. https://doi.org/10.1016/S0040-4020(01)99140-9
  9. Kim, D. -S. & Park, Y. -H. 1985. Uronic acid composition, block structure and some related properties of alginic acid: (3) on alginic acid prepared from Sargassum ringgoldianum. Bull. Korean Fish. Soc. 18:29-36.
  10. Kimura, J. & Maki, N. 2002. New loliolide derivatives from the brown alga Undaria pinnatifida. J. Nat. Prod. 65:57-58. https://doi.org/10.1021/np0103057
  11. Ko, S. -C., Kang, S. -M., Ahn, G., Yang, H. -P., Kim, K. -N. & Jeon, Y. -J. 2010. Antioxidant activity of enzymatic extracts from Sargassum coreanum. J. Korean Soc. Food Sci. Nutr. 39:494-499. https://doi.org/10.3746/jkfn.2010.39.4.494
  12. Kuniyoshi, M. 1985. Germination inhibitors from the brown alga Sargassum crassifolium (Phaeophyta, Sargassaceae). Bot. Mar. 28:501-503. https://doi.org/10.1515/botm.1985.28.11.501
  13. Li, Y., Qian, Z. -J., Ryu, B., Lee, S. -H., Kim, M. -M. & Kim, S. -K. 2009. Chemical components and its antioxidant properties in vitro: an edible marine brown alga, Ecklonia cava. Bioorg. Med. Chem. 17:1963-1973. https://doi.org/10.1016/j.bmc.2009.01.031
  14. Lizard, G., Fournel, S., Genestier, L., Dhedin, N., Chaput,C., Flacher, M., Mutin, M., Panaye, G. & Revillard, J. -P. 1995. Kinetics of plasma membrane and mitochondrial alterations in cells undergoing apoptosis. Cytometry 21:275-283. https://doi.org/10.1002/cyto.990210308
  15. Mosman, 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
  16. Muller, H. E. 1985. Detection of hydrogen peroxide produced by microorganism on ABTS-peroxidase medium. Zentrabl. Bakteriol. Mikrobiol. Hyg. A 259:151-154.
  17. Nicoletti, I., Migliorati, G., Pagliacci, M. C., Grignani, F. & Riccardi, C. 1991. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139:271-279. https://doi.org/10.1016/0022-1759(91)90198-O
  18. Okada, N., Shirata, K., Niwano, M., Koshino, H. & Uramoto, M. 1994. Immunosuppressive activity of a monoterpene from Eucommia ulmoides. Phytochemistry 37:281-282. https://doi.org/10.1016/0031-9422(94)85042-9
  19. Okunade, A. L. & Wiemer, D. F. 1985. (-)-loliolide, an antrepellent compound from Xanthoxyllum setulosum. J. Nat. Prod. 48:472-473. https://doi.org/10.1021/np50039a020
  20. Rosenkranz, A. R., Schmaldienst, S., Stuhlmeier, K. M., Chen, W., Knapp, W. & Zlabinger, G. J. 1992. A microplate assay for the detection of oxidative products using 2′,7′-dichlorefluorescein-diacetate. J. Immunol. Methods 156:39-45. https://doi.org/10.1016/0022-1759(92)90008-H
  21. Valdes, L. J. 3rd. 1986. Loliolide from Salvia divinorum. J. Nat. Prod. 49:171. https://doi.org/10.1021/np50043a031
  22. Wang, X. W., Zhan, Q., Coursen, J. D., Khan, M. A., Kontny, H. U., Yu, L., Hollander, M. C., O'Connor, P. M., Fornace, A. J. J. & Harris, C. C. 1999. GADD45 induction of a G2/M cell cycle checkpoint. Proc. Natl. Acad. Sci. U. S. A. 96:3706-3711. https://doi.org/10.1073/pnas.96.7.3706
  23. Zhang, X. -P., Pei, Y. -H., Liu, M. -S., Kang, S. -L. & Zhang, J. -Q. 2010. Chemical constituents from the leaves of Cerbera manghas. Asian Pac. J. Trop. Med. 3:109-111. https://doi.org/10.1016/S1995-7645(10)60046-6

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