Radical Scavenging Effect and Neuroprotective Activity from Oxidative Stress of Engelhardtia chrysolepis Leaf

Engelhardtia chrysolepis의 라디칼 소거능 및 신경세포의 산화 스트레스 보호효과

  • Kim, Eun Jung (Department of Food Science and Nutrition & Research Institute of Ecology for the Elderly, Pusan National University) ;
  • Lee, Ah Young (Department of Food Science and Nutrition & Research Institute of Ecology for the Elderly, Pusan National University) ;
  • Choi, Soo Yeon (Department of Food Science and Nutrition & Research Institute of Ecology for the Elderly, Pusan National University) ;
  • Seo, Hye Rin (Department of Food Science and Nutrition & Research Institute of Ecology for the Elderly, Pusan National University) ;
  • Lee, Young A (Department of Food Science and Nutrition, Catholic University of Daegu) ;
  • Cho, Eun Ju (Department of Food Science and Nutrition & Research Institute of Ecology for the Elderly, Pusan National University)
  • 김은정 (부산대학교 식품영양학과 & 노인생활환경연구소) ;
  • 이아영 (부산대학교 식품영양학과 & 노인생활환경연구소) ;
  • 최수연 (부산대학교 식품영양학과 & 노인생활환경연구소) ;
  • 서혜린 (부산대학교 식품영양학과 & 노인생활환경연구소) ;
  • 이영아 (대구가톨릭대학교 식품영양학과) ;
  • 조은주 (부산대학교 식품영양학과 & 노인생활환경연구소)
  • Received : 2016.05.24
  • Accepted : 2016.07.11
  • Published : 2016.09.30

Abstract

In this study, the radical scavenging activity and protective effect of ethanol extract from leaf of Engelhardtia chrysolepis HANCE (ECE) against oxidative stress were investigated under in vitro and cellular system. ECE showed strong radical scavenging activities in 1,1-diphenyl-2-picrylhydrazyl, hydroxyl(${\cdot}OH$) and nitric oxide(NO) radical as a concentration-dependent manner. Particularly, strong scavenging activity against the ${\cdot}OH$ and NO radical were observed with the $IC_{50}$ value of $1.30{\mu}g/ml$ and $12.61{\mu}g/ml$, respectively. Furthermore, the cellular oxidative stress was induced by amyloid beta($A{\beta}_{25-35}$) in C6 glial cells. The treatment of $A{\beta}_{25-35}$ to C6 glial cells generated high levels of reactive oxygen species(ROS) and declined cell viability. However, production of ROS was decreased by the treatment of ECE. In addition, the cell viability was significantly increased at each concentration(10, 25, $50{\mu}g/ml$) as dose-dependent manner. The Alzheimer's disease-related protein expressions in $A{\beta}_{25-35}$-treated C6 glial cells were analyzed. The ECE treatment inhibited expression of amyloid precursor protein(APP), C-terminal fragment-${\beta}(CTF-{\beta})$, ${\beta}$-site APP cleaving enzyme(BACE), phosphorylated tau(p-tau) proteins in C6 glial cells induced by $A{\beta}_{25-35}$. The present study indicated that ECE has strong radical scavenging activity and neuroprotective effect through attenuating oxidative stress.

Keywords

References

  1. Lim, D. G. (2004) Oxidative stress; reactive oxygen species and nitric oxide. Korean J. Crit. Care Med. 19: 81-85.
  2. Bokov, A., Chaundhuri, A. and Richardson, A. (2004) The role of oxidative damage and stress in aging. Mech. Ageing Dev. 125: 811-826. https://doi.org/10.1016/j.mad.2004.07.009
  3. Kim, N. S., Shon, M. S. and Hwang, Y. I. (2014) Anti-obese and antioxidant activities of Spica Prunellae extract in 3T3-L1 and HepG2 cells. Food Eng. Prg. 18: 413-418. https://doi.org/10.13050/foodengprog.2014.18.4.413
  4. Ricci, J. E., Waterhouse, N. and Green, D. R. (2003) Mitochondrial functions during cell death, a complex (IV) dilemma. Cell Death Differ. 10: 488-492. https://doi.org/10.1038/sj.cdd.4401225
  5. Melov, S. (2000) Mitochondrial oxidative stress: Physiologic consequences and potential for a role in aging. Ann. NY Acd. Sci. 908: 219-225.
  6. Lushchak, V. I. (2014) Free radicals, reactive oxygen species, oxidative stress and its classification. Chem. Biol. Interact. 224: 164-175. https://doi.org/10.1016/j.cbi.2014.10.016
  7. Darley-Usmar, V., Wiseman, H. and Halliwell, B. (1995) Nitric oxide and oxygen radicals: a question of balance. FEBS Lett. 369: 131-135. https://doi.org/10.1016/0014-5793(95)00764-Z
  8. Patel, R. P., McAndrew J., Sellak, H., White, C. R., Jo, H., Freeman, B. A. and Darley-Usmar, V. M. (1999) Biological aspects of reactive nitrogen species. BBA-Bioenergetics 1411: 385-400. https://doi.org/10.1016/S0005-2728(99)00028-6
  9. Harman, D. (1995) Free radical theory of aging: Alzheimer's disease pathogenesis. Age 18: 97-119. https://doi.org/10.1007/BF02436085
  10. Barnham, K. J., Masters, C. L. and Bush, A. I. (2004) Neurodegenerative diseases and oxidative stress. Nat. Rev. Drug Discov. 3: 205-214. https://doi.org/10.1038/nrd1330
  11. Albanes, D., Heinonen, O. P., Taylor, P. R., Virtamo, J., Edwards, B. K., Rautalahti, M., Hartman, A. M., Palmgren, J., Freedman, L. S., Haapakoski, J., Barrett, M. J., Pietinen, P., Malila, N., Tala, E., Liippo, K., Salomaa, E. R., Tangrea, J. A., Teppo, L., Askin, F. B., Taskinen, E., Erozan, Y., Greenwald, P. and Huttunen, J. K. (1996) Alpha-tocopherol and beta-carotene supplements and lung cancer incidence in the alpha-tocopherol, beta-carotene cancer prevention study: Effects of base-line characteristics and study compliance. J. Natl. Cancer Inst. 88: 1560-1570. https://doi.org/10.1093/jnci/88.21.1560
  12. Kuhn, M. (2003) Oxygen free radicals and antioxidants. Am. J. Nutr. 103: 58-62.
  13. Kim, J. H., Jeong, C. H., Choi, G. N., Kwak, J. H., Choi, S. G. and Heo, H. J. (2009) Antioxidant and neuronal cell protective effects of methanol extract from Schizandra chinensis using an in vitro system. Korean J. Food Sci. Technol. 41: 712-716.
  14. Kim, H. Y., Hwang, B. R., Wu, T. T. and Cho, E. J. (2012) The protective effect of Perilla frutescens from ONOO--induced oxidative stress and antiaging effect under cellular system. CNU J. Agric. Sci. 39: 467-471
  15. Xiao, P. G. (ed) (1993) A pictorial encyclopaedia of Chinese medical herbs (in Japanese). Chuokoron-Sha, Tokyo, 9: 41.
  16. Kasai, R. (1989) Studies on sweet dihydroflavonol glycosides from leaves of huang-qi (in Japanese). Tech. J. Food Chem. Chemicals (Japan) 1: 69-71.
  17. Haraguchi, H., Mochida, Y., Sakai, S., Masuda, H., Tamura, Y., Mizutani, K., Tanaka, O. and Chou, W. H. (1996) Protection against oxidative damage by dihydroflavonols in Engelhardtia chrysolepis. Biosci. Biotechnol. Biochem. 60: 945-948. https://doi.org/10.1271/bbb.60.945
  18. Kasai, R., Hirono, S., Chou, W. H., Tanaka, O. and Chen, F. H. (1988) Sweet dihydroflavonol rhamnoside from leaves of Engelhardtia chrysolepis, a Chinese folk medicine, Hung-qi. Chem. Pharm. Bull. 36: 4167-4170. https://doi.org/10.1248/cpb.36.4167
  19. Kasai, R., Hirono, S., Chou, W. H., Tanaka, O. and Chen F. H. (1991) An additional sweet dihydroflavonol glycoside from leaves of Engelhardtia chrysolepis, a Chinese folk medicine, Huang-qi. Chem. Pharm. Bull. 39: 1871-1872. https://doi.org/10.1248/cpb.39.1871
  20. Igarashi, K., Uchida, Y., Murakami, N., Mizutani, K. and Masuda, H. (1996) Effect of astilbin in tea processed from leaves of Engelhardtia chrysolepis., on the serum and liver lipid concentrations and on the erythrocyte and liver antioxidative enzyme activities of rats. Biosci. Biotechnol. Biochem. 60: 513-515. https://doi.org/10.1271/bbb.60.513
  21. Mizutani, K., Kambara, T., Masuda, H., Tamura, Y., Tanaka, O., Tokuda, H., Nishino, H. and Kozuka, M. (1997) Antitumor-promoting activities of dihydroflavonols from Kohki tea, the leaves of Engelhardtia chrysolepis. In Ohigashi, H., Osawa, T., Terao, J., Watanabe, S. and Yoshikawa, T. (Ed.), Food factors for cancer prevention. 607-612. Springer Japan. Tokyo.
  22. Haraguchi, H., Ohmi, I., Fukuda, A., Tamura, Y., Mizutani, K., Tanaka, O. and Chou, W. H. (1997) Inhibition of aldose reductase and sorbitol accumulation by astilbin and taxifolin dihydroflavonols in Engelhardtia chrysolepis. Biosci. Biotechnol. Biochem. 61: 651-654. https://doi.org/10.1271/bbb.61.651
  23. Hatano, T., Edamatsu, R., Hiramatsu, M., Mori, A., Fujita, Y., Yasuhara, T., Yoshida, T. and Okuda T. (1989) Effects of the interaction of tannins with co-existing substances. VI. : Effects of tannins and related polyphenols on superoxide anion radical, and on 1, 1-diphenyl-2-picrylhydrazyl radical. Chem. Pharm. Bull. 37: 2016-2021. https://doi.org/10.1248/cpb.37.2016
  24. Chung, S. K., Osawa, T. and Kawakishi, S. (1997) Hydroxyradical-scavenging effects of spices and scavengers from brown mustard (Brassica nigra). Biosci. Biotech. Biochem. 61: 118-123. https://doi.org/10.1271/bbb.61.118
  25. Marcocci, L., Maguire, J. J., Droxylefaix, M. T. and Packer, L. (1994) The nitric oxide-scavenging properties of Ginkgo biloba extract EGb761. Biochem. Biophys. Res. Commun. 201: 748-755. https://doi.org/10.1006/bbrc.1994.1764
  26. Ma, W. W., Hou, C. C., Zhou, X., Yu, H. L., Xi, Y. D., Ding, J., Zhao, X. and Xiao, R. Genistein alleviates the mitochondria-targeted DNA damage induced by ${\beta}$-amyloid peptides 25-35 in C6 glioma cells. Neurochem. Res. 38: 1315-1323.
  27. Wang, L. F. and Zhang, H. Y. (2003) A theoretical investigation on DPPH radical-scavenging mechanism of edaravone. Bioorg. Med. Chem. Lett. 13: 3789-3792. https://doi.org/10.1016/j.bmcl.2003.07.016
  28. Halliwell, B. and Gutteridge, J. M. C. (1991) Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch. Biochem. Biophys. 246: 501-504.
  29. Xin, W., Huang, H., Yu, L., Shi, H., Sheng, Y., Wang, T. T. Y. and Yu, L. (2012) Three new flavanonol glycosides from leaves of Engelhardtia roxburghiana, and their anti-inflammation, antiproliferative and antioxidant properties. Food Chem. 132: 788-798. https://doi.org/10.1016/j.foodchem.2011.11.038
  30. Wang, Q., Lee, A. Y., Choi, J. M., Lee, D. G., Kim, H. Y., Lee, S. and Cho, E. J. (2014) In vitro radical scavenging effect and neuroprotective activity from oxidative stress of Petasites japonicas. Korean J. Pharmacogn. 45: 147-153.
  31. Horakova, K., Sovcikova, A., Seemannova, Z., Syrova, D., Busanyova, K., Drobna, Z. and Ferencik, M. (2001) Detection of drug-induced, superoxide-mediated cell damage and its prevention by antioxidants. Free Radic. Biol. Med. 30: 650-664. https://doi.org/10.1016/S0891-5849(00)00508-6
  32. Cathcart, R., Schwiers, E. and Ames, B. N. (1983) Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal. Biochem. 134: 111-116. https://doi.org/10.1016/0003-2697(83)90270-1
  33. Jang, J. and Kim, K. (2006) Model mice in Alzheimer's disease. Food Sci. Ind. 39: 50-55.
  34. Zhao-bin, P. A. N., Fei-chao, L. I., Yue-e, L. I. A. O. and Xiao-song, L. I. N. (2011) Protective effect of total flavone of Engelhardtia roxburghiana Folium on experimental cerebral ischemia in rats. Chin. J. Exp. Tradit. Med. Form. 17: 223-226.
  35. Hennigan, A., O'Callaghan, R. M. and Kelly, A. M. (2007) Neurotrophins and their receptors: roles in plasticity, neurodegeneration and neuroprotection. Biochem. Soc. Trans. 35: 424-427. https://doi.org/10.1042/BST0350424
  36. Yamada, K., Mizuno, M. and Nabeshima, T. (2002) Role for brain-derived neurotrophic factor in learning and memory. Life Sci. 70: 735-744. https://doi.org/10.1016/S0024-3205(01)01461-8
  37. Peng, S., Wuu, J., Mufson, E. J. and Fahnestock, M. (2005) Precursor form of brain-derived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer's disease. J. Neurochem. 93: 1412-1421. https://doi.org/10.1111/j.1471-4159.2005.03135.x