Berberine protects against glutamate-induced oxidative stress and apoptosis in PC12 and N2a cells

Iranian Journal of Basic Medical Sciences

Volumn 20, Issue 5, 2017, Pages 594-603

  Sadeghnia, Hamid Reza ^a,b   Kolangikhah, Monireh ^b   Asadpour, Elham ^c   Forouzanfar, Fatemeh ^b   Hosseinzadeh, Hossein ^d,e  

^a MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Apoptosis; Berberine; Glutamate cytotoxicity; Neuroprotection; Oxidative injury

Indexed keywords

BERBERINE; CASPASE 3; GLUTAMIC ACID; GLUTATHIONE; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ALZHEIMER DISEASE; ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CELL DAMAGE; CELL PROLIFERATION ASSAY; CELL VIABILITY ASSAY; COMET ASSAY; CONTROLLED STUDY; DEGENERATIVE DISEASE; DEMENTIA; DNA FRAGMENTATION ASSAY; EXPOSURE; GENE EXPRESSION; GENE OVEREXPRESSION; LIPID PEROXIDATION ASSAY; MTT ASSAY; NEURO-2A CELL LINE; NONHUMAN; OXIDATIVE STRESS; PC12 CELL LINE; WESTERN BLOTTING;

EID: 85043354971     PISSN: 20083866     EISSN: 20083874     Source Type: Journal    
DOI: 10.22038/IJBMS.2017.8847     Document Type: Article

References (57)

1. Lau A, Tymianski M. Glutamate receptors, neurotoxicity and neurodegeneration. Pflügers Arch 2010; 460:525-542.
2. Mehta A, Prabhakar M, Kumar P, Deshmukh R, Sharma PL. Excitotoxicity: bridge to various triggers in neurodegenerative disorders. Eur J Pharmacol 2013; 698:6-18.
3. Bridges RJ, Natale NR, Patel SA. System xc(-) cystine/glutamate antiporter: an update on molecular pharmacology and roles within the CNS. Br J Pharmacol 2012; 165:20-34.
4. Ha JS, Lim HM, Park SS. Extracellular hydrogen peroxide contributes to oxidative glutamate toxicity. Brain Research 2010; 1359:291-297.
5. Froissard P, Monrocq H, Duval D. Role of glutathione metabolism in the glutamate-induced programmed cell death of neuronal-like PC12 cells. Eur J Pharmacol 1997; 326:93-99.
6. Ahmed T, Abdollahi M, Daglia M, Nabavi SF, Nabavi SM. Berberine and neurodegeneration: A review of literature. Pharmacological Reports 2015; 67: 970-979.
7. Imenshahidi M, Hosseinzadeh H. Berberis vulgaris and berberine: an update review. Phytother Res 2016; 30:1745-1764.
8. Imanshahidi M, Hosseinzadeh H. Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine. Phytother Res 2008; 22:999-1012.
9. Tabeshpour J, Imenshahidi M, Hosseinzadeh H. A review of the effects of Berberis vulgaris and its major component, berberine, in metabolic syndrome Iran J Basic Med Sci 2017; 20:557-568.
10. Bhutada P, Mundhada Y, Bansod K, Dixit P, Umathe S, Mundhada D. Anticonvulsant activity of berberine, an isoquinoline alkaloid in mice. Epilepsy Behav 2010; 18:207-210.
11. Wang F, Zhao G, Cheng L, Zhou H-Y, Fu L-Y, Yao W-X. Effects of berberine on potassium currents in acutely isolated CA1 pyramidal neurons of rat hippocampus. Brain Res 2004; 999:91-97.
12. Sarma B, Pandey V, Mishra G, Singh U. Antifungal activity of berberine iodide, a constituent of Fumaria indica. Folia Microbiol 1999; 44:164-166.
13. Hayashi K, Minoda K, Nagaoka Y, Hayashi T, Uesato S. Antiviral activity of berberine and related compounds against human cytomegalovirus. Bioorg Med Chem Lett 2007; 17:1562-1564.
14. Kuo C-L, Chi C-W, Liu T-Y. The anti-inflammatory potential of berberine in vitro and in vivo. Cancer Lett 2004; 203:127-137.
15. Katiyar SK, Meeran SM, Katiyar N, Akhtar S. p53 cooperates berberine‐induced growth inhibition and apoptosis of non‐small cell human lung cancer cells in vitro and tumor xenograft growth in vivo. Mol Carcinog 2009; 48:24-37.
16. Punitha ISR, Shirwaikar A, Shirwaikar A. Antidiabetic activity of benzyl tetra isoquinoline alkaloid berberine in streptozotocin-nicotinamide induced type 2 diabetic rats. Diabetol Croat 2005; 34, 117-128.
17. Kysenius K, Brunello CA, Huttunen HJ. Mitochondria and NMDA receptor-dependent toxicity of berberine sensitizes neurons to glutamate and rotenone injury. PloS one 2014; 9:e107129.
18. Al-Snafi AE. Therapeutic properties of medicinal plants: a review of medicinal plants with central nervous effects (part 1). Int J Pharmacol Toxicol 2015; 5:177-192.
19. Ma S, Liu H, Jiao H, Wang L, Chen L, Liang J, et al. Neuroprotective effect of ginkgolide K on glutamate-induced cytotoxicity in PC 12 cells via inhibition of ROS generation and Ca 2+ influx. Neurotoxicology 2012; 33:59-69.
20. Zhang Y, Wang W, Hao C, Mao X, Zhang L. Astaxanthin protects PC12 cells from glutamate-induced neurotoxicity through multiple signaling pathways. J Func Foods 2015; 16:137-151.
21. Lee SM, Yang EJ, Choi S-M, Kim SH, Baek MG, Jiang JH. Effects of bee venom on glutamate-induced toxicity in neuronal and glial cells. Evid Based Complement Alternat Med 2011; 2012: 368196.
22. Forouzanfar F, Afkhami Goli A, Asadpour E, Ghorbani A, Sadeghnia HR. Protective effect of Punica granatum L. against serum/glucose deprivation-induced PC12 cells injury. Evid Based Complement Alternat Med 2013; 2013: 3716730.
23. Wang H, Joseph JA. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Rad Biol Med 1999; 27:612-616.
24. Ghorbani A, Sadeghnia HR, Asadpour E. Mechanism of protective effect of lettuce against glucose/serum deprivation-induced neurotoxicity. Nutr Neurosci 2015; 18:103-109.
25. Sebastia J, Cristofol R, Martin M, Rodriguez-Farre E, Sanfeliu C. Evaluation of fluorescent dyes for measuring intracellular glutathione content in primary cultures of human neurons and neuroblastoma SH-SY5Y. Cytometry A 2003; 51:16-25.
26. Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 1974; 47:469-474.
27. Percival SS. Cu/Zn superoxide dismutase activity does not parallel copper levels in copper supplemented HL-60 cells. Biol Trace Elem Res 1993; 38:63-72.
28. Ghorbani A, Sadeghnia HR, Asadpour E. Mechanism of protective effect of lettuce against glucose/serum deprivation-induced neurotoxicity. Nutr Neurosci 2015; 18:103-109.
29. Peng WH, Wu CR, Chen CS, Chen CF, Leu ZC, Hsieh MT. Anxiolytic effect of berberine on exploratory activity of the mouse in two experimental anxiety models: interaction with drugs acting at 5-HT receptors. Life Sci 2004; 75:2451-2462.
30. Peng WH, Lo KL, Lee YH, Hung TH, Lin YC. Berberine produces antidepressant-like effects in the forced swim test and in the tail suspension test in mice. Life Sci 2007; 81:933-938.
31. Vaziri Z, Abbassian H, Sheibani V, Haghani M, Nazeri M, Aghaei I, et al. The therapeutic potential of Berberine chloride hydrate against harmaline-induced motor impairments in a rat model of tremor. Neurosci Lett 2015; 590:84-90.
32. Serafim TL, Oliveira PJ, Sardao VA, Perkins E, Parke D, Holy J. Different concentrations of berberine result in distinct cellular localization patterns and cell cycle effects in a melanoma cell line. Cancer Chemother Pharmacol 2008; 61:1007-1018.
33. Tsang CM, Lau EPW, Di K, Cheung PY, Hau PM, Ching YP, et al. Berberine inhibits Rho GTPases and cell migration at low doses but induces G2 arrest and apoptosis at high doses in human cancer cells. Int J Mol Med 2009; 24:131.
34. Shin KS, Choi HS, Zhao TT, Suh KH, Kwon IH, Choi SO, et al. Neurotoxic effects of berberine on long-term L-DOPA administration in 6-hydroxydopamine-lesioned rat model of Parkinson's disease. Arch Pharm Res 2013; 36:759-767.
35. Kwon IH, Choi HS, Shin KS, Lee BK, Lee CK, Hwang BY, et al. Effects of berberine on 6-hydroxydopamine-induced neurotoxicity in PC12 cells and a rat model of Parkinson's disease. Neurosci Lett 2010; 486:29-33.
36. Froissard P, Duval D. Cytotoxic effects of glutamic acid on PC12 cells. Neurochem Int 1994; 24:485-493.
37. Calderon FH, Bonnefont A, Muñoz FJ, Fernández V, Videla LA, Inestrosa NC. PC12 and neuro 2a cells have different susceptibilities to acetylcholinesterase–amyloid complexes, amyloid25–35 fragment, glutamate, and hydrogen peroxide. J Neurosci Res 1999; 56:620-631.
38. Zhang W, Su X, Gao Y, Sun B, Yu Y, Wang X, et al. Berberine protects mesenchymal stem cells against hypoxia-induced apoptosis in vitro. Biol Pharmac Bull 2009; 32:1335-1342.
39. Hsu Y-Y, Chen C-S, Wu S-N, Jong Y-J, Lo Y-C. Berberine activates Nrf2 nuclear translocation and protects against oxidative damage via a phosphatidylinositol 3-kinase/Akt-dependent mecha-nism in NSC34 motor neuron-like cells. Eur J Pharmac Sci 2012; 46:415-425.
40. Zhou X-Q, Zeng X-N, Kong H, Sun X-L. Neuroprotective effects of berberine on stroke models in vitro and in vivo. Neurosci Lett 2008; 447:31-36.
41. Campisi A, Acquaviva R, Mastrojeni S, Raciti G, Vanella A, De Pasquale R, et al. Effect of berberine and Berberis aetnensis C. Presl. alkaloid extract on glutamate‐evoked tissue transglutaminase up‐regula-tion in astroglial cell cultures. Phytother Res 2011; 25:816-820.
42. Liu X, Zhou J, Abid MDN, Yan H, Huang H, Wan L, et al. Berberine attenuates axonal transport impairment and axonopathy induced by calyculin a in N2a cells. PloS one 2014; 9.
43. Kritis AA, Stamoula EG, Paniskaki KA, Vavilis TD. Researching glutamate-induced cytotoxicity in different cell lines: a comparative/collective analysis/study. Front Cell Neurosci 2015; 9:91.
44. Bhutada P, Mundhada Y, Bansod K, Dixit P, Umathe S, Mundhada D. Anticonvulsant activity of berberine, an isoquinoline alkaloid in mice. Epilepsy Behav 2010; 18:207-210.
45. Cui HS, Matsumoto K, Murakami Y, Hori H, Zhao Q, Obi R. Berberine exerts neuroprotective actions against in vitro ischemia-induced neuronal cell damage in organotypic hippocampal slice cultures:involvement of B-cell lymphoma 2 phosphorylation suppression. Biol Pharmac Bull 2009; 32:79-85.
46. Lee T, Heo H, Kim Kwon Y. Effect of berberine on cell survival in the developing rat brain damaged by MK-801. Exp Neurobiol 2010; 19:140-145.
47. Yoo KY, Hwang IK, Lim BO, Kang TC, Kim DW, Kim SM, et al. Berberry extract reduces neuronal damage and N-Methyl-D-aspartate receptor 1 immunoreactivity in the gerbil hippocampus after transient forebrain ischemia. Biol Pharmac Bull 2006; 29:623-628.
48. Yoo JH, Yang EM, Cho JH, Lee JH, Jeong SM, Nah SY, et al. Inhibitory effects of berberine against morphine-induced locomotor sensitization and analgesic tolerance in mice. Neuroscience 2006; 142:953-961.
49. Zhao YM, Sun LN, Zhou HY, Wang XL. Voltage-dependent potassium channels are involved in glutamate-induced apoptosis of rat hippocampal neurons. Neurosci Lett 2006; 398:22-27.
50. Yu SP, Yeh C, Strasser U, Tian M, Choi DW. NMDA receptor-mediated K+ efflux and neuronal apoptosis. Science 1999; 284:336-339.
51. Yu SP. Regulation and critical role of potassium homeostasis in apoptosis. Prog Neurobiol 2003; 70:363-386.
52. Wang F, Zhao G, Cheng L, Zhou HY, Fu LY, Yao WX. Effects of berberine on potassium currents in acutely isolated CA1 pyramidal neurons of rat hippocampus. Brain Res 2004; 999:91-97.
53. Wu J, Jin GZ. Tetrahydroberberine blocks membrane K+ channels underlying its inhibition of intracellular message-mediated outward currents in acutely dissociated CA1 neurons from rat hippocampus. Brain Res 1997; 775:214-218.
54. Vaziri Z, Abbassian H, Sheibani V, Haghani M, Nazeri M, Aghaei I, et al. The therapeutic potential of Berberine chloride hydrate against harmaline-induced motor impairments in a rat model of tremor. Neurosci Lett 2015; 590:84-90.
55. Sendrowski K, Rusak M, Sobaniec P, Ilendo E, Dabrowska M, Bockowski L, et al. Study of the protective effect of calcium channel blockers against neuronal damage induced by glutamate in cultured hippocampal neurons. Pharmacol Rep 2013; 65:730-736.
56. Xu S, Zhang Y, Ren J, Zhou Z. Effects of berberine of L-and T-type calcium channels in guinea pig ventricular myocytes. Zhongguo Yao Li Xue Bao 1997; 18:515-518.
57. Nadjafi S, Ebrahimi S-A, Rahbar-Roshandel N. Protective effects of berberine on oxygen-glucose deprivation/reperfusion on oligodendrocyte cell line (OLN-93). Int J Prevent Med 2014; 5:1153-1160.