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Comparative Study of Bang-poong (root of Saposhnikovia divaricata Schischkin) and Related Species on Neuroprotective and Acetylcholinesterase Inhibitory Effects

방풍류(防風類) 약재(藥材)의 신경세포보호효과 및 아세틸콜린에스터라제 저해 효과 비교

  • Ju, In Gyoung (Department of Life and Nanopharmaceutical Sciences, Graduate School, Kyung Hee University) ;
  • Lee, Seungmin (Department of Oriental pharmaceutical Science, College of Pharmacy, Kyung Hee University) ;
  • Choi, Jin Gyu (Department of Oriental pharmaceutical Science, College of Pharmacy, Kyung Hee University) ;
  • Oh, Myung Sook (Department of Life and Nanopharmaceutical Sciences, Graduate School, Kyung Hee University)
  • 주인경 (경희대학교 일반대학원 나노의약생명과학과) ;
  • 이승민 (경희대학교 약학대학 한약학과) ;
  • 최진규 (경희대학교 약학대학 한약학과) ;
  • 오명숙 (경희대학교 일반대학원 나노의약생명과학과)
  • Received : 2019.08.28
  • Accepted : 2019.09.25
  • Published : 2019.09.30

Abstract

Objectives : Bang-poong (Saposhnikovia divaricata; SD) was traditionally used to treat inflammatory disorders. In this study, we aimed to investigate whether Bang-poong and related species including SD, Glehnia littoralis (GL), and Peucedanum japonicum (PJ) possess neuroprotective effects and acetylcholinesterase (AChE) inhibitory activities. Methods : Roots of SD, GL and PJ were extracted with distilled water (DW) or 70% ethanol (EtOH). We assessed 2,2-diphenyl-1-picrylhydrazyl (DPPH) free radical scavenging activities of the extracts. To examine neuroprotective effects, we measured cell viability in PC12 or HT22 cells after treatment of the extracts with $H_2O_2$ or amyloid-beta ($A{\beta}$). To assess anti-neuroinflammatory effects, we measured the nitric oxide (NO) levels after treatment with the extracts and lipopolysaccharide (LPS) in BV2 microglial cells. In addition, we performed AChE inhibition assay to explore effects of the extracts on the cholinergic system. Results : DW and EtOH extracts of SD, GL and PJ showed mild DPPH free radical scavenging activities. Also, DW extracts of GL and PJ showed protective effects against $H_2O_2$-induced toxicity in PC12 cells. In LPS-activated BV2 cells, EtOH extracts of SD, GL and PJ exerted inhibitory effects on NO production. Meanwhile, DW extracts of SD, GL and PJ inhibited the $A{\beta}$-induced cell death in HT22 cells. In addition, DW and EtOH extracts of GL exhibited remarkable inhibitory activities on AChE. Conclusions : We demonstrated that SD, GL and PJ exert anti-oxidative, anti-neuroinflammatory and AChE inhibitory activities. These results indicate that SD, GL and PJ could be potential candidates for neurological disorders.

Keywords

Saposhnikovia divaricata;Glehnia littoralis;Peucedanum japonicum;neuroprotection;neuroinflammation;acetylcholinesterase inhibition

Acknowledgement

Supported by : 농림식품기술기획평가원

References

  1. Seo BI, Kwon DY, Choi HY, Lee JH, Oh MS, Bu YM. Medicinal Herbology. 8th rev. ed. Seoul : Younglim-Sa. 2012 : 144-5.
  2. Gu YR, Kim SW, Son YW, Hong JH. Antioxidant activities of solvent extracts from different Glehnia Radix parts and their inhibitory effect against nitric oxide production in Raw 264.7 cell. Korean journal of food preservation. 2017 ; 24(1) : 116-24. https://doi.org/10.11002/kjfp.2017.24.1.116
  3. Kang SY, Oh TW, Kim JW, Park YK. Effect of the water extract of Peucedani Japonici Radix on ovalbumin-induced allergic asthma in mice. Kor J Herbology 2013 ; 28(6) : 1-7. https://doi.org/10.6116/kjh.2013.28.6.1
  4. Korea Food and Drug Administration. The Guideline on the Visual and Organoleptic Examination of Herbal Medicine. Seoul : Korea Food and Drug Administration. 2009 : 1 : 49, 103, 72.
  5. Seo UM, Zhao BT, Kim YH, Kang JS, Son JK, Woo MH. Simultaneous analysis of seven marker compounds from Saposhnikoviae Radix, Glehniae Radix and Peucedani Japonici Radix by HPLC/PDA. Arch Pharm Res. 2016 ; 39(5) : 695-704. https://doi.org/10.1007/s12272-016-0740-x
  6. Kreiner J, Pang E, Lenon GB, Yang AWH. Saposhnikoviae divaricata: a phytochemical, pharmacological, and pharmacokinetic review Chin J Nat Med. 2017 ; 15(4) : 255-64.
  7. Yuan Z, Tezuka Y, Fan W, Kadota S, Li X. Constituents of the underground parts of Glehnia littoralis. Chem Pharm Bull. 2002 ; 50(1) ; 73-7. https://doi.org/10.1248/cpb.50.73
  8. WK Whang, SJ Lee, HH Kim, HK Cho, KS Lee, IH Kang, IH Ham. Standardization of Peucedani Radix. Kor J Pharmacogn. 2001 ; 32(4) : 292-6.
  9. Tai J, Cheung S. Anti-proliferative and antioxidant activities of Saposhnikovia divaricata. Oncol Rep. 2007 ; 18(1) : 227-34.
  10. Chun JM, Kim HS, Lee AY, Kim SH, Kim HK. Anti-Inflammatory and Antiosteoarthritis Effects of Saposhnikovia divaricata ethanol Extract: In Vitro and In Vivo Studies. Evid Based Complement Alternat Med. 2016 ; 2016 : 1984238.
  11. Okuyama E, Hasegawa T, Matsushita T, Fujimoto H, Ishibashi M, Yamazaki M. Analgesic components of saposhnikovia root (Saposhnikovia divaricata). Chem Pharm Bull (Tokyo). 2001 ; 49(2) : 154-60. https://doi.org/10.1248/cpb.49.154
  12. Wang X, Jiang X, Yu X, Liu H, Tao Y, Jiang G, Hong M. Cimifugin suppresses allergic inflammation by reducing epithelial derived initiative key factors via regulating tight junctions. J Cell Mol Med. 2017 ; 21(11) : 2926-36. https://doi.org/10.1111/jcmm.13204
  13. Kuo YC, Lin YL, Huang CP, Shu JW, Tsai WJ. A tumor cell growth inhibitor from Saposhnikovae divaricata. Cancer Invest. 2002 ; 20(7-8) : 955-64. https://doi.org/10.1081/CNV-120005911
  14. Chang CZ, Wu SC, Kwan AL, Lin CL. 4'-O-$\beta$-D-glucosyl-5-O-methylvisamminol, an active ingredient of Saposhnikovia divaricata, attenuates high-mobility group box 1 and subarachnoid hemorrhage-induced vasospasm in a rat model. Behav Brain Funct. 2015 ; 11(1) : 28. https://doi.org/10.1186/s12993-015-0074-8
  15. Ng TB, Liu F, Wang HX. The antioxidant effects of aqueous and organic extracts of Panax quinquefolium, Panax notoginseng, Codonopsis pilosula, Pseudostellaria heterophylla and Glehnia littoralis. J Ethnopharmacol. 2004 ; 93 (2-3) : 285-8. https://doi.org/10.1016/j.jep.2004.03.040
  16. Lee JW, Lee C, Jin Q, Yeon ET, Lee D, Kim SY, Han SB, Hong JT, Lee MK, Hwang BY. Pyranocoumarins from Glehnia littoralis inhibit the LPS-induced NO production in macrophage RAW 264.7 cells. Bioorg Med Chem Lett. 2014 ; 24(12) : 2717-9. https://doi.org/10.1016/j.bmcl.2014.04.046
  17. McCutcheon AR, Ellis SM, Hancock RE, Towers GH. Antifungal screening of medicinal plants of British Columbian native peoples. J Ethnopharmacol. 1994 ; 44(3) : 157-69. https://doi.org/10.1016/0378-8741(94)01183-4
  18. de la Cruz JF, Vergara EJ, Cho Y, Hong HO, Oyungerel B, Hwang SG. Glehnia littoralis Root Extract Induces G0/G1 Phase Cell Cycle Arrest in the MCF-7 Human Breast Cancer Cell Line. Asian Pac J Cancer Prev. 2015 ; 16(18) : 8113-7. https://doi.org/10.7314/APJCP.2015.16.18.8113
  19. Yoon T, Lee do Y, Lee AY, Choi G, Choo BK, Kim HK. Anti-inflammatory effects of Glehnia littoralis extract in acute and chronic cutaneous inflammation. Immunopharmacol Immunotoxicol. 2010 ; 32(4) : 663-70. https://doi.org/10.3109/08923971003671108
  20. Huang GJ, Deng JS, Liao JC, Hou WC, Wang SY, Sung PJ, Kuo YH. Inducible nitric oxide synthase and cyclooxygenase-2 participate in anti-inflammatory activity of imperatorin from Glehnia littoralis. J Agric Food Chem. 2012 ; 60(7) : 1673-81. https://doi.org/10.1021/jf204297e
  21. Yoon T, Cheon MS, Lee AY, Lee do Y, Moon BC, Chun JM, Choo BK, Kim HK. Anti-inflammatory activity of methylene chloride fraction from Glehnia littoralis extract via suppression of NF-kappa B and mitogen-activated protein kinase activity. J Pharmacol Sci. 2010 ; 112(1) : 46-55. https://doi.org/10.1254/jphs.09168FP
  22. Matsuura H, Saxena G, Farmer SW, Hancock RE, Towers GH. Antibacterial and antifungal polyine compounds from Glehnia littoralis ssp. leiocarpa. Planta Med. 1996 ; 62(3) : 256-9. https://doi.org/10.1055/s-2006-957872
  23. Nugara RN, Inafuku M, Iwasaki H, Oku H. Partially purified Peucedanum japonicum Thunb extracts exert anti-obesity effects in vitro. Nutrition. 2014 ; 30(5) : 575-83. https://doi.org/10.1016/j.nut.2013.09.017
  24. Nukitrangsan N, Okabe T, Toda T, Inafuku M, Iwasaki H, Oku H. Effect of Peucedanum japonicum Thunb extract on high-fat diet-induced obesity and gene expression in mice. J Oleo Sci. 2012 ; 61(2) : 89-101. https://doi.org/10.5650/jos.61.89
  25. Kim JM, Noh EM, Kim HR, Kim MS, Song HK, Lee M, Yang SH, Lee GS, Moon HC, Kwon KB, Lee YR. Suppression of TPA-induced cancer cell invasion by Peucedanum japonicum Thunb. extract through the inhibition of $PKC{\alpha}$/NF-${\kappa}B$-dependent MMP-9 expression in MCF-7 cells. Int J Mol Med. 2016 ; 37(1) : 108-14. https://doi.org/10.3892/ijmm.2015.2417
  26. Chun JM, Lee AR, Kim HS, Lee AY, Gu GJ, Moon BC, Kwon BI. Peucedanum japonicum extract attenuates allergic airway inflammation by inhibiting Th2 cell activation and production of pro-inflammatory mediators. J Ethnopharmacol. 2018 ; 211 : 78-88. https://doi.org/10.1016/j.jep.2017.09.006
  27. Kim JM, Erkhembaatar M, Lee GS, Lee JH, Noh EM, Lee M, Song HK, Lee CH, Kwon KB, Kim MS, Lee YR. Peucedanum japonicum Thunb. ethanol extract suppresses RANKL-mediated osteoclastogenesis. Exp Ther Med. 2017 ; 14(1) : 410-6. https://doi.org/10.3892/etm.2017.4480
  28. Chun JM, Lee AY, Kim JS, Choi G, Kim SH. Protective Effects of Peucedanum japonicum Extract against Osteoarthritis in an Animal Model Using a Combined Systems Approach for Compound-Target Prediction. Nutrients. 2018 ; 10(6) : E754. https://doi.org/10.3390/nu10060754
  29. Takeuchi N, Kasama T, Aida Y, Oki J, Maruyama I, Watanabe K, Tobinaga S. Pharmacological activities of the prenylcoumarins, developed from folk usage as a medicine of Peucedanum japonicum THUNB. Chem Pharm Bull (Tokyo). 1991 ; 39(6) : 1415-21. https://doi.org/10.1248/cpb.39.1415
  30. Chen IS, Chang CT, Sheen WS, Teng CM, Tsai IL, Duh CY, Ko FN. Coumarins and antiplatelet aggregation constituents from Formosan Peucedanum japonicum. Phytochemistry. 1996 ; 41(2) : 525-30. https://doi.org/10.1016/0031-9422(95)00625-7
  31. Nugara RN, Inafuku M, Takara K, Iwasaki H, Oku H. Pteryxin: a coumarin in Peucedanum japonicum Thunb leaves exerts antiobesity activity through modulation of adipogenic gene network. Nutrition. 2014 ; 30(10) : 1177-84. https://doi.org/10.1016/j.nut.2014.01.015
  32. Park JH, Lee TK, Yan BC, Shin BN, Ahn JH, Kim IH, Cho JH, Lee JC, Hwang IK, Kim JD, Hong S, Lee YJ, Won MH, Kang IJ. Pretreated Glehnia littoralis Extract Prevents Neuronal Death Following Transient Global Cerebral Ischemia through Increases of Superoxide Dismutase 1 and Brainderived Neurotrophic Factor Expressions in the Gerbil Hippocampal Cornu Ammonis 1 Area. Chin Med J (Engl). 2017 ; 130(15) : 1796-803. https://doi.org/10.4103/0366-6999.211554
  33. Park JH, Shin BN, Ahn JH, Cho JH, Lee TK, Lee JC, Jeon YH, Kang IJ, Yoo KY, Hwang IK, Lee CH, Noh YH, Kim SS, Won MH, Kim JD. Glehnia littoralis Extract Promotes Neurogenesis in the Hippocampal Dentate Gyrus of the Adult Mouse through Increasing Expressions of Brain-Derived Neurotrophic Factor and Tropomyosin-Related Kinase B. Chin Med J (Engl). 2018 ; 131(6) : 689-95. https://doi.org/10.4103/0366-6999.226894
  34. Ju IG, Choi JG, Kim N, Kwak C, Lee JK, Oh MS. Peucedani Japonici Radix ameliorates lipopolysaccharideinduced neuroinflammation by regulating microglial responses. Neurosci Lett. 2018 ; 686 : 161-7. https://doi.org/10.1016/j.neulet.2018.09.010
  35. Song HR, Lee HY, Shim SH, Kwon YJ. Neuroinflammation and Psychiatric Illness. Korean J Biol Psychiatry. 2016 ; 23(1) : 12-7.
  36. Islam MT. Oxidative stress and mitochondrial dysfunction-linked neurodegenerative disorders. Neurol Res. 2008 ; 39(1) : 73-82.
  37. Haam J, Yakel JL. Cholinergic modulation of the hippocampal region and memory function. J Neurochem. 2017 ; 142 Suppl 2 : 111-21. https://doi.org/10.1111/jnc.14052
  38. Kim N, Choi JG, Park S, Lee JK, Oh MS. Butterbur Leaves Attenuate Memory Impairment and Neuronal Cell Damage in Amyloid Beta-Induced Alzheimer's Disease Models. Int J Mol Sci. 2018 ; 19(6) : 1644. https://doi.org/10.3390/ijms19061644
  39. Ellman GL, Courtney KD, Andres Jr V, Featherstone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 1961 ; 7 : 88-90. https://doi.org/10.1016/0006-2952(61)90145-9
  40. Ju MS, Kim HG, Choi JG, Ryu JH, Hur J, Kim YJ, Oh MS. Cassiae semen, a seed of Cassia obtusifolia, has neuroprotective effects in Parkinson's disease models. Food Chem Toxicol. 2010 ; 48 : 2037-44. https://doi.org/10.1016/j.fct.2010.05.002
  41. Iqbal J, al-Rashida M, Babar A, Hameed A, Khan MS, Munawar MA, Khan AF. Cholinesterase Inhibitory Activities of N-Phenylthiazol-2-Amine Derivatives and their Molecular Docking Studies. Med Chem. 2015 ; 11(5) : 489-96. https://doi.org/10.2174/1573406411666141230104536
  42. Seo BI, Kwon DY, Choi HY, Lee JH, Oh MS, Bu YM. Medicinal Herbology. 8th rev. ed. Seoul : Younglim-Sa. 2012 : 345.
  43. Lee WC, Jeon WJ, Shin GJ. An Experimental Studies on the alleviation effects of Daebangpoongtang in LPS-induced arthritis. Dongguk Journal of the Institute of Oriental Medicine. 2009 ; 9:35-49.
  44. Sanchez-Moreno C. Methods used to evaluate the free radical scavenging activity in foods and biological systems. Food Science and Technology International. 2002 ; 8 : 121-37. https://doi.org/10.1177/1082013202008003770
  45. Fetler L, Amigorena S. Neuroscience. Brain under surveillance: the microglia patrol. Science. 2005 ; 309 : 392-3. https://doi.org/10.1126/science.1114852
  46. Catorce MN, Gevorkian G. LPS-induced Murine Neuroinflammation Model: Main Features and Suitability for Pre-clinical Assessment of Nutraceuticals. Curr Neuropharmacol. 2016 ; 14(2) : 155-64. https://doi.org/10.2174/1570159X14666151204122017
  47. Kamino T, Shimokura T, Morita Y, Tezuka Y, Nishizawa M, Tanaka K. Comparative analysis of the constituents in Saposhnikoviae Radix and Glehniae Radix cum Rhizoma by monitoring inhibitory activity of nitric oxide production. J Nat Med. 2016 ; 70(2) : 253-9. https://doi.org/10.1007/s11418-016-0969-1
  48. Selkoe DJ. Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J Alzheimers Dis. 2001 ; 3 : 75-80. https://doi.org/10.3233/JAD-2001-3111
  49. Ferreira-Vieira TH, Guimaraes IM, Silva FR, Ribeiro FM. Alzheimer's disease: Targeting the Cholinergic System. Curr Neuropharmacol. 2016 ; 14(1) : 101-15. https://doi.org/10.2174/1570159X13666150716165726