Korean Journal of Agricultural Science (농업과학연구)

Institute of Agricultural Science, CNU (충남대학교 농업과학연구소)
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Antioxidant effects of Cirsium japonicum var. maackii on oxidative stress in C6 glial cells and mice

  • Min Jeong, Kim (Department of Food Science and Nutrition, Pusan National University) ;
  • Byeong Wook, Noh (Department of Food Science and Nutrition, Pusan National University) ;
  • Qi Qi, Pang (Department of Food Science and Nutrition, Pusan National University) ;
  • Sanghyun, Lee (Department of Plant Science and Technology, Chung-Ang University) ;
  • Ji-Hyun, Kim (Department of Food Science and Nutrition, Pusan National University) ;
  • Eun Ju, Cho (Department of Food Science and Nutrition, Pusan National University)
  • Received : 2022.01.27
  • Accepted : 2022.02.28
  • Published : 2022.03.01
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Abstract

We investigated the effects of Cirsium japonicum var. maackii (CJM) against oxidative stress-induced C6 glial cells and cognitive impairment in mice. To evaluate the anti-oxidative effect of the extract and fractions from CJM, 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT), reactive oxygen species (ROS), and nitric oxide (NO) assays were conducted in H2O2-treated C6 glial cells. Furthermore, we identified the protective mechanisms of CJM with a scopolamine-treated mice model. The results revealed that H2O2 decreased the cell viability in C6 glial cells, indicating that H2O2 induced oxidative stress in glial cells. However, CJM fractions significantly increased cell viability in H2O2-treated C6 glial cells, which suggested that CJM protected against oxidative stress. CJM extract and fractions also reduced ROS and NO production, which were increased by H2O2 in C6 glial cells. In particular, the EtOAc fraction from CJM (EACJM) effectively protected against oxidative stress by increasing the cell viability and decreasing ROS and NO. Therefore, we carried out further in vivo experiments with EACJM. Scopolamine caused increases of ROS, thiobarbituric acid reactive substances (TBARS), and NO production. However, EACJM effectively alleviated ROS, TBARS, and NO levels compared to scopolamine-injected mice. In addition, EACJM up-regulated protein expressions of superoxide dismutase and glutathione peroxidase, indicating that EACJM enhanced the antioxidative system. Our results demonstrated that CJM had protective effects against oxidative stress in glial cells and memory dysfunction in mice. Based on these results, we propose that CJM could be a potential AD preventive and therapeutic agent.

Keywords

Acknowledgement

본 연구는 보건장학회의 지원으로 수행되었으며 이에 감사드립니다.

References

  1. An P, Wu T, Yu H, Fang K, Ren Z, Tang M. 2018. Hispidulin protects against focal cerebral ischemia reperfusion injury in rats. Journal of Molecular Neuroscience 65:203-212. https://doi.org/10.1007/s12031-018-1086-2
  2. Benzi G, Moretti A. 1998. Is there a rationale for the use of acetylcholinesterase inhibitors in the therapy of Alzheimer's disease? European Journal of Pharmacology 346:1-13. https://doi.org/10.1016/S0014-2999(98)00093-4
  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 Biochemistry 134:111-116. https://doi.org/10.1016/0003-2697(83)90270-1
  5. Cho C, Kang LJ, Jang D, Jeon J, Lee H, Choi S, Han SJ, Oh E, Nam J, Kim CS, et al. 2019. Cirsium japonicum var. maackii and apigenin block Hif-2α-induced osteoarthritic cartilage destruction. Journal of Cellular and Molecular Medicine 23:5369-5379. https://doi.org/10.1111/jcmm.14418
  6. Chung WS, Welsh CA, Barres BA, Stevens B. 2015. Do glia drive synaptic and cognitive impairment in disease? Nature Neuroscience 18:1539-1545.
  7. Dawson GR, Iversen SD. 1993. The effects of novel cholinesterase inhibitors and selective muscarinic receptor agonists in tests of reference and working memory. Behavioural Brain Research 57:143-153. https://doi.org/10.1016/0166-4328(93)90130-I
  8. De Bernardo S, Canals S, Casarejos MJ, Solano RM, Menendez J, Mena MA. 2004. Role of extracellular signalregulated protein kinase in neuronal cell death induced by glutathione depletion in neuron/glia mesencephalic cultures. Journal of Neurochemistry 91:667-682. https://doi.org/10.1111/j.1471-4159.2004.02744.x
  9. Dirsch VM, Stuppner H, Vollmar AM. 1998. The Griess assay: Suitable for a bio-guided fractionation of antiinflammatory plant extracts. Planta Medica 64:423-426. https://doi.org/10.1055/s-2006-957473
  10. 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
  11. Galea E, Reis DJ, Fox ES, Xu H, Feinstein DL. 1996. CD 14 mediates endotoxin induction of nitric oxide synthase in cultured brain glial cells. Journal of Neuroimmunology 64:19-28. https://doi.org/10.1016/0165-5728(95)00143-3
  12. Hashioka S, Wu Z, Klegeris A. 2021. Glia-driven neuroinflammation and systemic inflammation in Alzheimer's disease. Current Neuropharmacology 19:908-924. https://doi.org/10.2174/1570159X18666201111104509
  13. Heneka MT, O'Banion MK, Terwel D, Kummer MP. 2010. Neuroinflammatory processes in Alzheimer's disease. Journal of Neural Transmission 117:919-947. https://doi.org/10.1007/s00702-010-0438-z
  14. Ishida H, Umino T, Tsuji K, Kosuge T. 1987. Studies on antihemorrhagic substances in herbs classified as hemostatics in Chinese medicine. VII. On the antihemorrhagic principle in Cirsium japonicum DC. Chemical and Pharmaceutical Bulletin 35:861-864.
  15. Jang M, Kim GH. 2016. Cirsium japonicum extracts show antioxidant activity and PC12 cell protection against oxidative stress. Korean Journal of Food Science and Technology 48:172-177. [in Korean] https://doi.org/10.9721/KJFST.2016.48.2.172
  16. Jang MR, Hong EY, Cheong JH, Kim GH. 2012. Antioxidative components and activity of domestic Cirsium japonicum extract. Journal of the Korean Society of Food Science and Nutrition 41:739-744. [in Korean] https://doi.org/10.3746/JKFN.2012.41.6.739
  17. Jiang T, Chu J, Chen H, Cheng H, Su J, Wang X, Cao Y, Tian S, Li Q. 2020. Gastrodin inhibits H2O2-induced ferroptosis through its antioxidative effect in rat glioma cell line C6. Biological and Pharmaceutical Bulletin 43:480-487. https://doi.org/10.1248/bpb.b19-00824
  18. Jung HA, Abdul QA, Byun JS, Joung EJ, Gwon WG, Lee MS, Kim HS, Choi JS. 2017. Protective effects of flavonoids isolated from Korean milk thistle Cirsium japonicum var. maackii (Maxim.) Matsum on tert-butyl hydroperoxide-induced hepatotoxicity in HepG2 cells. Journal of Ethnopharmacology 209:62-72. https://doi.org/10.1016/j.jep.2017.07.027
  19. Jung TY, Lee HW, Park JH. 2011. Memory enhancing effect of Longanae Arillus against scopolamine-induced amnesia in C57BL/6 mice. Journal of Physiology & Pathology in Korean Medicine 25:406-416. [in Korean]
  20. Kalaria RN. 2018. The pathology and pathophysiology of vascular dementia. Neuropharmacology 134:226-239. https://doi.org/10.1016/j.neuropharm.2017.12.030
  21. Karthivashan G, Park SY, Kweon MH, Kim J, Haque M, Cho DY, Kim IS, Cho EA, Ganesan P, Choi DK. 2018. Ameliorative potential of desalted Salicornia europaea L. extract in multifaceted Alzheimer's-like scopolamine-induced amnesic mice model. Scientific Reports 8:1-16.
  22. Kasa P, Papp H, Kasa Jr P, Torok I. 2000. Donepezil dose-dependently inhibits acetylcholinesterase activity in various areas and in the presynaptic cholinergic and the postsynaptic cholinoceptive enzyme-positive structures in the human and rat brain. Neuroscience 101:89-100. https://doi.org/10.1016/S0306-4522(00)00335-3
  23. Kim JH, Cho MJ, Park CH, Cho EJ, Kim HY. 2020a. Free radical scavenging activity and protective effect of three glycyrrhiza varieties against hydrogen peroxide-induced oxidative stress in C6 glial cells. Journal of Applied Biological Chemistry 63:327-334. [in Korean]
  24. Kim JH, He MT, Kim MJ, Park CH, Lee JY, Shin YS, Cho EJ. 2020b. Protective effects of combination of Carthamus tinctorius L. seed and Taraxacum coreanum on scopolamine-induced memory impairment in mice. Korean Journal of Medicinal Crop Science 28:85-94. [in Korean] https://doi.org/10.7783/KJMCS.2020.28.2.85
  25. Kim MJ, Kim JH, Kim JH, Lee S, Cho EJ. 2020c. Amelioration effects of Cirsium japonicum var. maackii extract/fractions on amyloid beta25-35-induced neurotoxicity in SH-SY5Y cells and identification of the main bioactive compound. Food & Function 11:9651-9661. https://doi.org/10.1039/D0FO01041C
  26. Kim MJ, Lee S, Kim HY, Cho EJ. 2021. Cirsium japonicum var. maackii inhibits hydrogen peroxide-induced oxidative stress in SH-SY5Y cells. Korean Journal of Agricultural Science 48:119-131. [in Korean] https://doi.org/10.7744/KJOAS.20210006
  27. Kim S, Kang S, Ko K, Nam S. 2017. Antioxidant activity and protective effects of Cirsium japonicum against damaged mouse liver cell (BNL CL. 2). Journal of Life Science 27:442-449. [in Korean] https://doi.org/10.5352/JLS.2017.27.4.442
  28. Kim SS, Park JY, Lee WC, Park CY, Ko BH, Jeon YA, Park KJ, An HJ, Kang BS, Yun SH, et al. 2000. Memory enhancing activity of extract of new citrus cultivar 'Shinyegam' in mice. Korean Journal of Food Preservation 25:855-862. [in Korean] https://doi.org/10.11002/kjfp.2018.25.7.855
  29. Konar A, Gupta R, Shukla RK, Maloney B, Khanna VK, Wadhwa R, Lahiri DK, Thakur MK. 2019. M1 muscarinic receptor is a key target of neuroprotection, neuroregeneration and memory recovery by i-Extract from Withania somnifera. Scientific Reports 9:1-15. https://doi.org/10.1038/s41598-018-37186-2
  30. Kut K, Bartosz G, Soszynski M, Sadowska-Bartosz I. 2022. Antioxidant properties of hispidulin. Natural Product Research 12:1-4.
  31. Lee AY, Kim MJ, Lee S, Shim JS, Cho EJ. 2018. Protective effect of Cirsium japonicum var. maackii against oxidative stress in C6 glial cells. Korean Journal of Agricultural Science 45:509-519. [in Korean] https://doi.org/10.7744/KJOAS.20180031
  32. 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.
  33. Mates JM, Sanchez-Jimenez F. 1999. Antioxidant enzymes and their implications in pathophysiologic processes. Front Bioscience 4:D339-D345.
  34. 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
  35. Muhammad T, Ali T, Ikram M, Khan A, Alam SI, Kim MO. 2019. Melatonin neuroxidative stress-mediated neuroinflammation/neurodegeneration and memory impairment in scopolamine-induced amnesia mice model. Journal of Neuroimmune Pharmacology 14:278-294. https://doi.org/10.1007/s11481-018-9824-3
  36. Ohkawa H, Ohishi N, Yagi K. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95:351-358.
  37. Penke B, Bogar F, Fulop L. 2017. β-Amyloid and the pathomechanisms of Alzheimer's disease: A comprehensive view. Molecules 22:1692. https://doi.org/10.3390/molecules22101692
  38. Polinsky RJ. 1998. Clinical pharmacology of rivastigmine: A new-generation acetylcholinesterase inhibitor for the treatment of Alzheimer's disease. Clinical Therapeutics 20:634-647. https://doi.org/10.1016/S0149-2918(98)80127-6
  39. Qian Y, Zheng Y, Ramos KS, Tiffany-Castiglioni E. 2005. GRP78 compartmentalized redistribution in Pb-treated glia: Role of GRP78 in lead-induced oxidative stress. Neurotoxicology 26:267-275. https://doi.org/10.1016/j.neuro.2004.09.002
  40. 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
  41. 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 cirsimaritin extracted from Cirsium japonicum var. maackii Maxim. Bioorganic & Medicinal Chemistry Letters 27:3076-3080. https://doi.org/10.1016/j.bmcl.2017.05.051
  42. Sohn E, Kim YJ, Kim JH, Jeong SJ. 2021. Ficus erecta Thunb leaves alleviate memory loss induced by scopolamine in mice via regulation of oxidative stress and cholinergic system. Molecular Neurobiology 58:3665-3676. https://doi.org/10.1007/s12035-021-02358-1
  43. Tsikas D. 2007. Analysis of nitrite and nitrate in biological fluids by assays based on the Griess reaction: Appraisal of the Griess reaction in the L-arginine/nitric oxide area of research. Journal of Chromatography 851:51-70.