Korean Journal of Agricultural Science (농업과학연구)

Institute of Agricultural Science, CNU (충남대학교 농업과학연구소)
권호 표지
DOI QR코드

DOI QR Code

Protective effect of Cirsium japonicum var. maackii against oxidative stress in C6 glial cells

  • Lee, Ah Young (Department of Food Science and Nutrition, Pusan National University) ;
  • Kim, Min Jeong (Department of Food Science and Nutrition, Pusan National University) ;
  • Lee, Sanghyun (Department of Integrative Plant Science, Chung-Ang University) ;
  • Shim, Jae Suk (Imsil Herbal Medicine Association) ;
  • Cho, Eun Ju (Department of Food Science and Nutrition, Pusan National University)
  • Received : 2018.04.10
  • Accepted : 2018.05.11
  • Published : 2018.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

This study was investigated the anti-oxidant property and neuro-protective effect of Cirsium japonicum var. maackii (CJM) against oxidative stress in hydrogen peroxide ($H_2O_2$)-induced C6 glial cells. We measured the 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical, hydroxyl radical (${\cdot}OH$), and superoxide ($O_2{^-}$) radical scavenging activities of an ethanol extract and four fractions [n-Butanol, ethyl acetate (EtOAc), $CHCl_3$, and n-Hexane] from CJM. The results of this study show that the extract and all fractions from CJM had a dose-dependent DPPH radical scavenging activity. In particular, the EtOAc fraction exhibited the strongest scavenging effect with 88.23% at a concentration of $500{\mu}g/mL$. In addition, the EtOAc fraction from CJM also effectively scavenged ${\cdot}OH$ radicals and $O_2{^-}$ radicals, compared to other extract and fractions. In C6 glial cells, $H_2O_2$ markedly decreased the cell viability as well as increased lactate dehydrogenase (LDH) release and reactive oxygen species (ROS) production. However, the EtOAc fraction of CJM attenuated the cellular damage from the oxidative stress by elevating the cell viability and inhibiting the LDH release and ROS over-production compared with the $H_2O_2$-treated control group. Our findings indicate that the EtOAc fraction from CJM has antioxidant effect and neuro-protective effect against oxidative stress, suggesting that it can be used as a natural antioxidant and therapeutic agent for the prevention of neurodegenerative disorders.

Keywords

References

  1. Bamham KJ, Masters CL, Bush AI. 2004. Neurodegenerative diseases and oxidative stress. Nature Reviews Drugs Discovery 3:205-214. https://doi.org/10.1038/nrd1330
  2. Behl C. 1999. Alzheimer's disease and oxidative stress: Implications for novel therapeutic approaches. Progress in Neurobiology 57:301-323. https://doi.org/10.1016/S0301-0082(98)00055-0
  3. Block ML, Hong JS. 2005. Microglia and inflammation-mediated neurodegeneration: Multiple triggers with a common mechanism. Progress in Neurobiology 76:77-98. https://doi.org/10.1016/j.pneurobio.2005.06.004
  4. Cathcart R, Schwiers E, Ames BN. 1983. Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Analytical Biochemisry 134:111-116. https://doi.org/10.1016/0003-2697(83)90270-1
  5. Choi CH, Song ES, Kim JS, Kang MH. 2003. Antioxidative activities of Castanea crenata Flos. methanol extracts. Korean Journal of Food Science and Technology 35:1216-1220. [in Korean]
  6. Chung SK, Osawa T, Kawakishi S. 1997. Hydroxyl radical-scavenging effects of spices and scavengers from brown mustard (Brassicanigra). Bioscience, Biotechnology and Biochemistry 61:118-123. https://doi.org/10.1271/bbb.61.118
  7. Dabaghi-Barbosa P, Mariante Rocha A, Franco da Cruz Lima A, Heleno de Oliveira B, Benigna Martinelli de Oliveira M, Gunilla Skare Carnieri E, Cadena SM, Eliane Merlin Rocha M. 2015. Hispidulin: Antioxidant properties and effect on mitochondrial energy metabolism. Free Radical Research 39:1305-1315.
  8. De Deyn PP, Hiramatsu M, Borggree F, Goeman J, D'Hooge R, Saerens J, Mori A. 1998. Superoxide dismutase activity in cerebrospinal fluid of patients with dementia and some other neurological disorders. Alzheimer Disease and Associated Disorders 12:26-32. https://doi.org/10.1097/00002093-199803000-00004
  9. Fleury C, Mignotte B, Vayssiere JL. 2002. Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84:131-141. https://doi.org/10.1016/S0300-9084(02)01369-X
  10. Ganzera M, Pocher P, Stuppner H. 2005. Differentiation of Cirsium japonicum and C. setosum by TLC and HPLC-M. Phytochemical Analysis 16:205-209. https://doi.org/10.1002/pca.846
  11. Hatano T, Edamatsu R, Hiramatsu M, Mori A, Fujita Y, Yasuhara T, Yoshida T, Okuda Y. 1989. Effects of the interaction of tannins with co-existing substances, effects of tannins and related polyphenols on superoxide VI anion radical, and on 1,1-diphenyl-2-picrylhydrazyl radical. Chemical and Pharmaceutical Bulletin 37:2016-2021. https://doi.org/10.1248/cpb.37.2016
  12. Hong J, Wei MJ, Leem DG, Park KS, Yoon TH, No KM, Jeong JY. 2010. Evaluation of antioxidants activity through the chemical assay. Journal of Biomedical Research 11:1-8.
  13. Jang MR, Park HJ, Hong EY, Kim GH. 2014. Comparison of the anti-bacterial activity of domestic Cirsium japonicum collected from different regions. The Korean Journal of Food and Cookery Science 30:278-283. [in Korean] https://doi.org/10.9724/kfcs.2014.30.3.278
  14. Jenner P. 2003. Oxidative stress in Parkinson's disease. Annals of Neurology 53:S26-S38. https://doi.org/10.1002/ana.10483
  15. Jung HA, Jin SE, Min BS, Kim BW, Choi JS. 2012. Anti-inflammatory activity of Korean thistle Cirsium Maackii and its major flavonoid, luteolin 5-O-glucoside. Food and Chemical Toxicology 50:2171-2179. https://doi.org/10.1016/j.fct.2012.04.011
  16. Jung HA, Park JJ, Min BS, Jung HJ, Islam MN, Choi JS. 2015. Inhibition of advanced glycation endproducts formation by Korean thistle, Cirsium maackii. Asian Pacific Journal of Tropical Medicine 8:1-5. https://doi.org/10.1016/S1995-7645(14)60178-4
  17. Jung HA, Roy A, Abdul QA, Kim HR, park HJ, Choi JS. 2017. Luteolin 5-O-glucoside from Korean milk thistle, Cirsium maackii, exhibits anti-inflammatory activity via activation of the Nrf2/HO-1 pathway. Natural Product Science 23:183-191. https://doi.org/10.20307/nps.2017.23.3.183
  18. Kamat JP. 2006. Peroxynitrite: A potent oxidizing and nitrating agent. Indian Journal of Experimental Biology 44:436-447.
  19. Kim SJ, Kim GH. 2003. Identification for flavones in different parts of Cirsium japonicum. Journal of Food Science and Nutrition 8:330-335.
  20. Kirkinezos IG, Moraes CT. 2001. Reactive oxygen species and mitochondrial diseases. Seminars in Cell and Developmental Biology 12:449-457. https://doi.org/10.1006/scdb.2001.0282
  21. Lee HK, Kim JS, Kim NY, Kim MJ, Park SU, Yu CY. 2003. Antioxidant, antimutagenicity and anticancer activities of extracts from Cirsium japonicum var. ussuriense KITA-MURA. Korean Journal of Medicinal Crop Science 11:53-61. [in Korean]
  22. Lee J, Rodriguez JP, Lee KH, Park JY, Kang KS, Hahm DH, Huh CK, Lee SC, Lee S. 2017. Determination of flavonoids from Cirsium japonicum var. maackii and their inhibitory activities against aldose reductase. Applied Biological Chemistry 60:487-496. https://doi.org/10.1007/s13765-017-0302-z
  23. Lee JH, Choi SI, Lee YS, Kim GH. 2008. Antioxidant and anti-inflammatory activities of ethanol extract from leaves of Cirsium japonicum. Food Science and Biotechnology 1:38-45.
  24. Lim SS, Kim MH, Lee JH. 1997. Effect of Artemisia princeps var. orientalis and Cirsium japonicum var. ussuriense on liver function, body lipid, and bile acid of hyperlipiemic rat. Korean Journal of Nutrition 30:797-802. [in Korean]
  25. Lin P, Tian XH, Yi YS, Jiang WS, Zhou YJ, Cheng WJ. 2015. Luteolin-induced protection of $H_2O_2$-induced apoptosis in PC12 cells and the associated pathway. Molecular Medicine Reports 12:7699-7704. https://doi.org/10.3892/mmr.2015.4400
  26. Lipinski B. 2011. Hydroxyl radical and its scavengers in health and disease. Oxidative medicine and Cellular Longevity 2011:809696.
  27. Liu S, Luo X, Li D, Zhang J, Qui D, Liu W, She L, Yang Z. 2006. Tumor inhibition and improved immunity in mice treated with flavone from Cirsium japonicum DC. International Immunopharmacology 6:1387-1393. https://doi.org/10.1016/j.intimp.2006.02.002
  28. Liu Y, Tia X, Gou L, Sun L, Ling X, Yin X. 2013. Luteolin attenuates diabetes-associated cognitive decline in rats. Brain Research Bulletin 94:23-29. https://doi.org/10.1016/j.brainresbull.2013.02.001
  29. Liu R, Zhang T, Yang H, Lan X, Ying J, Du G. 2011. The flavonoid apigenin protects brain neurovascular coupling against amyloid-${\beta}_{25-35}$-induced toxicity in mice. Journal of Alzheimer's Disease 24:85-100. https://doi.org/10.3233/JAD-2010-101593
  30. Meda L, Cassatella MA, Szendrei GI, Otcos L, Jr Baron P, Villalba M, Ferrari D, Rossi F. 1995. Activation of microglial cells by beta-amyloid protein and interferon-${\gamma}$. Nature 374:647-650. https://doi.org/10.1038/374647a0
  31. Montine TJ, Diana NM, Quinn JF, Beal MF, Markesbery WR, Roberts LJ, Morrow JD. 2002. Lipid peroxidation in aging brain and Alzheimer's disease. Free Radical Biology & Medicine 33:620-626. https://doi.org/10.1016/S0891-5849(02)00807-9
  32. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods 65:55-63. https://doi.org/10.1016/0022-1759(83)90303-4
  33. Narayanan S, Ruma D, Gitika B, Sharma SK, Pauline T, Sai Ram M, Ilavazhagan G, Sawhney RC, Kumar D, Banerjee PK. 2005. Antioxidant activities of seabuckthorn (Hippophae rhamnoides) during hypoxia induced oxidative stress in glial cells. Molecular and Cellular Biochemistry 278:9-14. https://doi.org/10.1007/s11010-005-7636-2
  34. Nishikimi N, Rao NA, Yagi K. 1972. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygenin. Biochemical and Biophysical Research Communications 46:849-854. https://doi.org/10.1016/S0006-291X(72)80218-3
  35. Nunomura A, Castellani RJ, Zhu X, Moreira PI, Perry G, Smith MA. 2006. Involvement of oxidative stress in Alzheimer disease. Journal of Neuropathology & Experimental Neurology 65:631-641. https://doi.org/10.1097/01.jnen.0000228136.58062.bf
  36. Omodeo-Sale F, Gramigna D, Campaniello R. 1997. Lipid peroxidation and antioxidant systems in rat brain: effect of chronic alcohol consumption. Neurochemical Research 22:557-582.
  37. Park HK, Yoon SY, Choi JH, Ko HS, Suh YW, Lee YS, Kim GH, Chung MS, Cheon JH. 2006. The antidepressant effects of Cirsium japonicum in ICR mice. Journal of Korean Society of Health 50:429-435. [in Korean]
  38. Park JY, Kim HY, Shibamoto T, Jang TS, lee SC, Shim JS, Hahm DH, Lee HJ, Lee S, Kang KS. 2017. Beneficial effects of a medicinal herb, Cirsium japonicum var. maackii, extract and its major component, cirsimaritin on breast cancer metastasis in MDA-MB-231 breast cancer cells. Bioorganic & Medicinal Chemistry Letters 27:3968-3973. https://doi.org/10.1016/j.bmcl.2017.07.070
  39. Park JY, Yun H, Jo J, Baek JY, Lee SC, Choi YJ, Shim JS, Choi HJ, Lee S, Kang KS. 2018. Beneficial effects of Cirsium japonicum var. maackii on menopausal symptoms in ovariectomized rats. Food and Function 9:2480-2489. https://doi.org/10.1039/C7FO01258F
  40. Racher AJ, Looby D, Griffiths JB. 1990. Use of lactate dehydrogenase release to assess changes in culture viability. Cytotechnology 3:301-307. https://doi.org/10.1007/BF00365494
  41. Rice-Evans CA, Miller N, Paganga G. 1996. Structure antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biology & Medicine 20:933-956. https://doi.org/10.1016/0891-5849(95)02227-9
  42. Rodriguez JP, Lee J, Park JY, Kang KS, Hahm DH, Lee SC, Lee S. 2017. HPLC-UV analysis of sample preparation influence on flavonoid yield from Cirsium japonicum var. maackii. Applied Biological Chemistry 60:519-525. https://doi.org/10.1007/s13765-017-0306-8
  43. Rodriguez JP, Lee YK, Woo DG, Shin JS, Geraldino PJL, Jacinto SD, Lee S. 2018. Flavonoids from Cirsium japonicum var. maackii pappus as inhibitors of aldose reductase and their simultaneous determination. Chemical Papers 72:81-88. https://doi.org/10.1007/s11696-017-0259-8
  44. Shin MS, Park JY, Lee J, Yoo HH, Hahm DH, Lee SC, Lee S, Hwang GS, Jung K, Kang KS. 2017. Anti-inflammatory effects and corresponding mechanisms of cirsimartiin extracted from Cirsium japonicum var. maackii Maxim. Bioorganic & Medicinal Chemistry Letters 27:3076-3080. https://doi.org/10.1016/j.bmcl.2017.05.051
  45. Sies H. 2017. Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: Oxidative eustress. Redox Biology 11:613-619. https://doi.org/10.1016/j.redox.2016.12.035
  46. Touyz RM. 2004. Reactive oxygen species, vascular oxidative stress, and redox signaling in hypertension: What is the clinical significance? Hypertension 44:248-252. https://doi.org/10.1161/01.HYP.0000138070.47616.9d
  47. Wan Y, Liu LY, Hong ZF, Peng J. 2014. Ethanol extract of Cirsium japonicum attenuates hepatic lipid accumulation via AMPK activation in human HepG2 cells. Experimental and Therapeutic Medicine 8:79-84. https://doi.org/10.3892/etm.2014.1698
  48. Waris G, Ahsan H. 2006. Reactive oxygen species: Role in the development of cancer and various chronic conditions. Journal of Carcinogenesis 5:14. https://doi.org/10.1186/1477-3163-5-14
  49. Yin Y, Heo SI, Wang MH. 2008. Antioxidant and antidiabetic activities of extracts from Cirsium japonicum roots. Nutrition Research and Practice 2:247-251. https://doi.org/10.4162/nrp.2008.2.4.247
  50. Zhao L, Wang JL, Liu R, Li XX, Li JF, Zhang L. 2013. Neuroprotective, anti-amyloidogenic and neurotrophic effects of apigenin in an Alzheimer's disease mouse model. Molecules 189:9949-9965.