Protective Effect of Arctigenin against MPP⁺ and MPTP-induced Neurotoxicity

Abstract

The potential protective effects of arctigenin on 1-methyl-4-phenylpyridinium ion and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyride-induced neurotoxicity were examined, and the results indicated that arctigenin could improve the movement behaviors and upregulate dopamine and γ-aminobutyric acid levels in a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyride-induced neurotoxicity mouse model. A further in vitro experiment showed that the pretreatment with arctigenin on cultured human neuroblastoma SH-SY5Y cells could obviously attenuate the decrease of cell survival rates caused by treatment with 1-methyl-4-phenylpyridinium ion by way of acting against cell apoptosis through the decrease of Bax/Bcl-2 and caspase-3, and by antioxidative action through reduction of the surplus reactive oxygen species production and downregulation of mitochondrial membrane potential. It is for the first time that a neuroprotective activity of arctigenin in both in vitro and in vivo experiments was reported, enlightening that arctigenin could be useful as a potential therapeutic agent for Parkinsonʼs disease.

Key words

arctigenin - oxidative stress - anti-apoptosis - neuroprotective effect - Parkinsonʼs disease

• References

• 1 Aarsland D, Londos E, Ballard C. Parkinsonʼs disease dementia and dementia with Lewy bodies: different aspects of one entity. Int Psychogeriatr 2009; 2: 216-219
• 2 Mattson MP. Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol 1990; 1: 120-129
• 3 Jomova K, Vondrakova D, Lawson M, Valko MM. Oxidative stress and neurodegenerative disorders. Mol Cell Biochem 2010; 345: 91-104
• 4 Swarup V, Ghosh J, Mishra MK, Basu A. Novel strategy for treatment of Japanese encephalitis using arctigenin, a plant lignan. J Antimicrob Chemother 2008; 3: 679-688
• 5 Zhao H, Wang J, Yang SS. Chemical composition and pharmacological activity of medicinal plants Arctium lappa L. Summary. J Liaoning Coll TCM 2005; 7: 128-129
• 6 Krantz JC, Cair CJ. A physicochemical study of the carbohydrate occurring in the root of Arctium lappa . J Pharm 1897; 72: 416-424
• 7 Nose M, Fujimoto T, Nishibe S, Ogihara Y. Structural transformation of lignan compounds in rat gastrointestinal tract; II. Serum concentration of lignans and their metabolites. Planta Med 1993; 2: 131-134
• 8 Chinese Pharmacopoeia Commission. The Pharmacopoeia of the Peopleʼs Republic of China, Vol. 1. Beijing: China Medical Science Press; 2010: 66-67
• 9 Young PJ, Kim SR, Choi YH, Kim J, Kim SG, Markelonis GJ, Oh TH, Kim YC. Arctigenin protects cultured cortical neurons from glutamate-induced neurodegeneration by binding to kainate receptor. J Neurosci Res 2002; 68: 233-240
• 10 Jang YP, Kim SR, Choi YH, Kim J, Kim SG, Markelonis GJ, Oh TH, Kim YC. Arctigenin protects cultured cortical neurons from glutamate-induced neurodegeneration by binding to kainate receptor. J Neurosci Res 2002; 2: 233-240
• 11 Lee JY, Kim CJ. Arctigenin, a phenylpropanoid dibenzylbutyrolactone lignan, inhibits type I–IV allergic inflammation and pro-inflammatory enzymes. Arch Pharm Res 2010; 33: 947-957
• 12 Chung YC, Ko HW, Bok E, Park ES, Huh SH, Nam JH, Jin BK. The role of neuroinflammation on the pathogenesis of Parkinsonʼs disease. BMB Rep 2010; 43: 225-232
• 13 Wilms H, Zecca L, Rosenstiel P, Sievers J, Deuschl G, Lucius R. Inflammation in Parkinsonʼs diseases and other neurodegenerative diseases: cause and therapeutic implications. Curr Pharm Des 2007; 18: 1925-1928
• 14 Wang W, Pan Q, Han XY, Wang J, Tan RQ, He F, Dou DQ, Kang TG. Simultaneous determination of arctiin and its metabolites in rat urine and feces by HPLC. Fitoterapia 2013; 86: 6-12
• 15 Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, Steele jr. GD, Chen LB. Intracellular-heterogeneity in mitochondrial membrane potential revealed by J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci U S A 1991; 9: 3671-3675
• 16 Morizane A, Li JY, Brundin P. From bench to bed: the potential of stem cells for the treatment of Parkinsonʼs disease. Cell Tissue Res 2008; 331: 323-336
• 17 Jenner P. Oxidative stress in Parkinsonʼs disease. Ann Neurol 2003; 53: 26-38
• 18 Lev N, Melamed E, Offen D. Apoptosis and Parkinsonʼs disease. Prog Neuropsychopharmacol Biol Psychiatry 2003; 27: 245-250
• 19 Ishihara K, Yamagishi N, Saito Y, Takasaki M, Konoshima T, Htayama T. Arctigenin from Fructus Arctii is a novel suppressor of heat shock response in mammalian cells. Cell Stress Chaperones 2006; 11: 154-161
• 20 Kang HS, Lee JY, Kim CJ. Anti-inflammatory activity of arctigenin from Forsythiae Fructus. J Ethnopharmacol 2008; 116: 305-312
• 21 Jang YP, Kim SR, Kim YC. Neuroprotective dibenzylbutyrolactone lignans of Torreya nucifera . Planta Med 2001; 67: 470-472
• 22 Ma CJ, Sung SH, Kim YC. New neuroprotective dibenzylbutane lignans isolated from Machilus thunbergii . Nat Prod Res 2010; 6: 562-568
• 23 Solano RM, Menéndez J, Casarejos MJ, Rodríguez-Navarro JA, García de Yébenes J, Mena MA. Midbrain neuronal cultures from parkin mutant mice are resistant to nitric oxide-induced toxicity. Neuropharmacology 2006; 51: 327-340
• 24 Boulet S, Mounayar S, Poupard A, Bertrand A, Jan C, Pessiglione M, Hirsch EC, Feuerstein C, Francois C, Feger J, Savasta M, Tremblay L. Behavioral recovery in MPTP-treated monkeys: neurochemical mechanisms studied by intrastriatal microdialysis. J Neurosci 2008; 38: 9575-9584
• 25 Winkler C, Bentlage C, Nikkhah G, Samii M, Björklund A. Intranigral transplants of GABA-rich striatal tissue induce behavioral recovery in the rat Parkinson model and promote the effects obtained by intrastriatal dopaminergic transplants. Exp Neurol 1999; 2: 165-186
• 26 Tatton NA, Kish SJ. In situ detection of apoptotic nuclei in the substantia nigra pars compacta of 1-methyl-4-phenyl-1,2,3,6-tetrahydrophenylpyridine – treated mice using terminal deoxynucleotidyl transferase labeling and acridine orange. Neuroscience 1997; 77: 1037-1048
• 27 Namura I, Douillet P, Sun CJ, Pert A, Cohen RM, Chiueh CC. MPP⁺ (1-methyl-4-phenylpyridine) is a neurotoxin to dopamine-, norepinephrine- and serotonin-containing neurons. Eur J Pharmacol 1987; 136: 31-37
• 28 Greenamyre JT, Shere TB, Betarbet R, Panov AV. Complex I and Parkinsonʼs disease. IUBMB Life 2001; 52: 135-141
• 29 Xie HR, Hu LS, Li GY. SH-SY5Y human neuroblastoma cell line: in vitro cell model of dopaminergic neurons in Parkinsonʼs disease. Chin Med J 2010; 123: 1086-1092
• 30 Fall CP, Bennett JP. Characterization and time course of MPP⁺-induced apoptosis in human SH-SY5Y neuroblastoma cells. J Neurosci Res 1999; 55: 620-628
• 31 Bruno D, Marini AM, Youle RJ. Apoptosis and DNA degradation induced by 1-methyl-4-phenylpyridinium in neurons. Biochem Biophys Res Commun 1991; 181: 1442-1448
• 32 Cory S, Adams JM. The Bcl-2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002; 2: 647-656
• 33 Kaul S, Kanthasamy A, Kitazawa M, Anantharam V, Kanthasamy AG. Caspase-3 dependent proteolytic activation of protein kinase C delta mediates and regulates 1-methyl-4-phen-ylpyridinium (MPP⁺)-induced apoptotic cell death in dopaminergic cells: relevance to oxidative stress in dopaminergic degeneration. Eur J Neurosci 2003; 18: 1387-1401
• 34 Salvesen GS, Dixit VM. Caspases: intracellular signaling by proteolysis. Cell 1997; 91: 443-446
• 35 Zhang D, Zhang JJ, Liu GT. The novel squamosamide derivative (compound FLZ) attenuated 1-methyl, 4-phenyl-pyridinium ion (MPP⁺)-induced apoptosis and alternations of related signal transduction in SH-SY5Y cells. Neuropharmacology 2007; 52: 423-429
• 36 Lindsay J, Esposti MD, Gilmore AP. Bcl-2 proteins and mitochondria-specificity in membrane targeting for death. Biochem Biophys Acta 2011; 1813: 523-529
• 37 Zhang K, Ma ZG, Wang J, Xie AM, Xie JX. Myricetin attenuated MPP⁺-induced cytotoxicity by anti-oxidation and inhibition of MKK4 and JNK activation in MES23.5 cells. Neuropharmacology 2011; 61: 329-335
• 38 Le DA, Wu Y, Huang Z, Matsushita K, Plesnila N, Augustinack JC, Hyman BT, Yuan J, Kuida K, Flavell RA, Moskowitz MA. Caspase activation and neuroprotection in caspase-3-deficient mice after in vivo cerebral ischemia and in vitro oxygen glucose deprivation. Proc Natl Acad Sci USA 2002; 99: 15188-15193
• 39 Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB. Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species. J Cell Sci 2007; 120: 4155-4166
• 40 Jung TW, Lee JY, Shim WS, Kang ES, Kim SK, Ahn CW, Lee HC, Cha BS. Rosiglitazone protects human neuroblastoma SH-SY5Y cells against MPP⁺ induced cytotoxicity via inhibition of mitochondrial dysfunction and ROS production. J Neurol Sci 2007; 253: 53-60
• 41 Kim SY, Kim MY, Mo JS, Park JW, Park HS. SAG protects human neuroblastoma SH-SY5Y cells against 1-methyl-4-phenylpyridinium ion (MPP⁺) -induced cytotoxicity via the downregulation of ROS generation and JNK signalling. Neurosci Lett 2007; 413: 132-136
• 42 Prehn JH, Bindokas VP, Jordan J, Galindo MF, Ghadge GD, Roos RP, Boise LH, Thompson CB, Krajewski S, Reed JC, Miller RJ. Protective effect of transforming growth factor-beta 1 on beta-amyloid neurotoxicity in rat hippocampal neurons. Mol Pharmacol 1996; 49: 319-328
• 43 Hou Q, He F, Dou DQ, Kang TG, Li HF. New preparation method of arctigenin from Fructus Arctii. Chin J New Drugs 2011; 20: 871-873
• 44 Matsuura K, Kabuto H, Makino H, Ogawa N. Pole test is a useful method for evaluating the mouse movement disorder caused by striatal dopamine depletion. J Neurosci Methods 1997; 73: 45-48
• 45 Donnan GA, Willis GL, Kaczmarczyk SJ, Rowe P. Motor function in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated mouse. J Neurol Sci 1987; 77: 185-191
• 46 Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55-63
• 47 Schneider L, Giordano S, Zelickson BR, Johnson MS, Benavides GA, Ouyang X, Fineberg N, Darley-Usmar VM, Zhang J. Differentiation of SH-SY5Y cells to a neuronal phenotype changes cellular bioenergetics and the response to oxidative stress. Free Radic Biol Med 2011; 51: 2007-2017
• 48 Tzeng YW, Lee LY, Chao PL, Lee HC, Wu RT, Lin AM. Role of autophagy in protection afforded by hypoxic preconditioning against MPP⁺-induced neurotoxicity in SH-SY5Y cells. Free Radic Biol Med 2010; 49: 839-846
• 49 LeBel CP, Ali SF, McKee M, Bondy SC. Organometal-induced increases in oxygen reactive species: the potential of 2′,7′-dichlorofluorescin diacetate as an index of neurotoxic damage. Toxicol Appl Pharmacol 1990; 104: 17-24
• 50 Im JY, Han PL. Nordihydroguaiaretic acid induces astroglial death via glutathione depletion. J Neurosci Res 2007; 85: 3127-3134