Ginsenoside Rb1 attenuates oxygen-glucose deprivation-induced apoptosis in SH-SY5Y cells via protection of mitochondria and inhibition of AIF and cytochrome c release

Molecules

Volumn 18, Issue 10, 2013, Pages 12777-12792

  Liang, Jianmin ^a   Yu, Ying ^a   Wang, Boyu ^a   Lu, Bin ^a   Zhang, Jizhou ^b   Zhang, Hongbo ^a   Ge, Pengfei ^a  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b Basic Medical College   (China)

Author keywords

Apoptosis inducing factor; Cytochrome c; Ginsenoside Rb1; Mitochondria; Oxygen glucose deprivation

Indexed keywords

AIFM1 PROTEIN, HUMAN; APOPTOSIS INDUCING FACTOR; CYTOCHROME C; GINSENOSIDE; GINSENOSIDE RB 1; GLUCOSE; NEUROPROTECTIVE AGENT; REACTIVE OXYGEN METABOLITE;

ANTAGONISTS AND INHIBITORS; APOPTOSIS; CELL HYPOXIA; CELL SURVIVAL; DRUG EFFECTS; DRUG SCREENING; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PHYSIOLOGY; TUMOR CELL LINE; ARTICLE; DRUG ANTAGONISM; DRUG EFFECT;

APOPTOSIS; APOPTOSIS INDUCING FACTOR; CELL HYPOXIA; CELL LINE, TUMOR; CELL SURVIVAL; CYTOCHROMES C; DRUG EVALUATION, PRECLINICAL; GINSENOSIDES; GLUCOSE; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NEUROPROTECTIVE AGENTS; REACTIVE OXYGEN SPECIES;

EID: 84886628627     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules181012777     Document Type: Article

References (48)

1. Donnan, G.A.; Fisher, M.; Macleod, M.; Davis, S.M. Stroke. Lancet 2008, 371, 1612-1623.
2. Kirino, T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 1982, 239, 57-69.
3. Albers, G.W.; Caplan, L.R.; Coull, B.; Fayad, P.B.; Mohr, J.P.; Saver, J.L.; Sherman, D.G.; TIA Working Group. Transient ischemic attatck-Proposal for a new definition. N. Engl. J. Med. 2002, 347, 1713-1716.
4. Li, Y.; Sharov, V.G.; Jiang, N.; Zaloga, C.; Sabbah, H.N.; Chopp, M. Ultrastructural and light microscopic evidence of apoptosis after middle cerebral artery occlusion in the rat. Am. J. Pathol. 1995, 146, 1045-1051.
5. Malagelada, C.; Xifró, X.; Miñano, A.; Sabriá, J.; Rodríguez-Alvarez, J. Contribution of caspase-mediated apoptosis to the cell death caused by oxygen-glucose deprivation in cortical cell cultures. Neurobiol. Dis. 2005, 20, 27-37.
6. Shah, P.T.; Yoon, K.W.; Xu, X.M.; Broder, L.D. Apoptosis mediates cell death following traumatic injury in rat hippocampal neurons. Neuroscience 1997, 79, 999-1004.
7. Friedlander, R.M. Apoptosis and caspases in neurodegenerative diseases. N. Engl. J. Med. 2003, 348, 1365-1375.
8. Genovese, T.; Mazzon, E.; Paterniti, I.; Esposito, E.; Cuzzocrea, S. Neuroprotective effects of olprinone after cerebral ischemia/reperfusion injury in rats. Neurosci. Lett. 2011, 503, 93-99.
9. Yao, R.Q.; Qi, D.S.; Yu, H.L.; Liu, J.; Yang, L.H.; Wu, X.X. Quercetin attenuates cell apoptosis in focal cerebral ischemia rat brain via activation of BDNF-TrkB-PI3K/Akt signaling pathway. Neurochem. Res. 2012, 37, 2777-2786.
10. Ding, Z.M.; Wu, B.; Zhang, W.Q.; Lu, X.J.; Lin, Y.C.; Geng, Y.J.; Miao, Y.F. Neuroprotective effects of ischemic preconditioning and postconditioning on global brain ischemia in rats through the same effect on inhibition of apoptosis. Int. J. Mol. Sci. 2012, 13, 6089-6101.
11. Yuan, Q.L.; Yang, C.X.; Xu, P.; Gao, X.Q.; Deng, L.; Chen, P.; Sun, Z.L.; Chen, Q.Y. Neuroprotective effects of ginsenoside Rb1 on transient cerebral ischemia in rats. Brain Res. 2007, 1167, 1-12.
12. Zhu, J.; Jiang, Y.; Wu, L.; Lu, T.; Xu, G.; Liu, X. Suppression of local inflammation contributes to the neuroprotective effect of ginsenoside Rb1 in rats with cerebral ischemia. Neuroscience 2012, 202, 342-351.
13. Liang, Y.Y.; Wang, B.; Qian, D.M.; Li, L.; Wang, Z.H.; Hu, M.; Song, X.X. Inhibitory effects of Ginsenoside Rb1 on apoptosis caused by HSV-1 in human glioma cells. Virol. Sin. 2012, 27, 19-25.
14. Gao, X.Q.; Yang, C.X.; Chen, G.J.; Wang, G.Y.; Chen, B.; Tan, S.K.; Liu, J.; Yuan, Q.L. Ginsenoside Rb1 regulates the expressions of brain-derived neurotrophic factor and caspase-3 and induces neurogenesis in rats with experimental cerebral ischemia. J. Ethnopharmacol. 2010, 132, 393-399.
15. Wu, Y.; Xia, Z.Y.; Dou, J.; Zhang, L.; Xu, J.J.; Zhao, B.; Lei, S.; Liu, H.M. Protective effect of ginsenoside Rb1 against myocardial ischemia/reperfusion injury in streptozotocin-induced diabetic rats. Mol. Biol. Rep. 2011, 38, 4327-4335.
16. Guo, Y.; Yang, T.; Lu, J.; Li, S.; Wan, L.; Long, D.; Li, Q.; Feng, L.; Li, Y. Rb1 postconditioning attenuates liver warm ischemia-reperfusion injury through ROS-NO-HIF pathway. Life Sci. 2011, 88, 598-605.
17. Lim, J.H.; Wen, T.C.; Matsuda, S.; Tanaka, J.; Maeda, N.; Peng, H.; Aburaya, J.; Ishihara, K.; Sakanaka, M. Protection of ischemic hippocampal neurons by ginsenoside Rb1, a main ingredient of ginseng root. Neurosci. Res. 1997, 28, 191-200.
18. Manzanero, S.; Santro, T.; Arumugam, T.V. Neuronal oxidative stress in acute ischemic stroke: Sources and contribution to cell injury. Neurochem. Int. 2013, 62, 712-718.
19. Choi, A.Y.; Choi, J.H.; Lee, J.Y.; Yoon, K.S.; Choe, W.; Ha, J.; Yeo, E.J.; Kang, I. Apigenin protects HT22 murine hippocampal neuronal cells against endoplasmic reticulum stress-induced apoptosis. Neurochem. Int. 2010, 57, 143-152.
20. Guo, R.B.; Wang, G.F.; Zhao, A.P.; Gu, J.; Sun, X.L.; Hu, G. Paeoniflorin protects against ischemia-induced brain damages in rats via inhibiting MAPKs/NF-κB-mediated inflammatory responses. PLoS One 2012, 7, e49701.
21. Zhang, T.L.; Fu, J.L.; Geng, Z.; Yang, J.J.; Sun, X.J. The neuroprotective effect of losartan through inhibiting AT1/ASK1/MKK4/JNK3 pathway following cerebral I/R in rat hippocampal CA1 region. CNS Neurosci. Ther. 2012, 18, 981-987.
22. Jordan, J.; de Groot, P.W.; Galindo, M.F. Mitochondria: The headquarters in ischemia-induced neuronal death. Cent. Nerv. Syst. Agents Med. Chem. 2011, 11, 98-106.
23. Lee, H.J.; Lyu da, H.; Koo, U.; Lee, S.J.; Hong, S.S.; Kim, K.; Kim, K.H.; Lee, D.; Mar, W. Inhibitory effect of 2-arylbenzofurans from the Mori Cortex Radicis (Moraceae) on oxygen glucose deprivation (OGD)-induced cell death of SH-SY5Y cells. Arch. Pharm. Res. 2011, 34, 1373-1380.
24. Zhao, L.P.; Ji, C.; Lu, P.H.; Li, C.; Xu, B.; Gao, H. Oxygen glucose deprivation (OGD)/re-oxygenation-induced in vitro neuronal cell death involves mitochondrial cyclophilin-D/P53 signaling axis. Neurochem. Res. 2013, 38, 705-713.
25. Du, C.P.; Tan, R.; Hou, X.Y. Fyn kinases play a critical role in neuronal apoptosis induced by oxygen and glucose deprivation or amyloid-β peptide treatment. CNS Neurosci. Ther. 2012, 18, 754-761.
26. Sena, L.A.; Chandel, N.S. Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 2012, 48, 158-167.
27. Rau, T.F.; Lu, Q.; Sharma, S.; Sun, X.; Leary, G.; Beckman, M.L.; Hou, Y.; Wainwright, M.S.; Kavanaugh, M.; Poulsen, D.J.; et al. Oxygen glucose deprivation in rat hippocampal slice cultures results in alterations in carnitine homeostasis and mitochondrial dysfunction. PLoS One 2012, 7, e40881.
28. James, D.; Parone, P.A.; Terradillos, O.; Lucken-Ardjomande, S.; Montessuit, S.; Martinou, J.C. Mechanisms of mitochondrial outer membrane permeabilization. Novartis Found. Symp. 2007, 287, 170-176.
29. Marutani, E.; Kosugi, S.; Tokuda, K.; Khatri, A.; Nguyen, R.; Atochin, D.N.; Kida, K.; van Leyen, K.; Arai, K.; Ichinose, F. A novel hydrogen sulfide-releasing N-methyl-D-aspartate receptor antagonist prevents ischemic neuronal death. J. Biol. Chem. 2012, 287, 32124-32135.
30. Li, Z.; Cui, G.; Wang, J.; Yu, Z.; Zhao, L.; Lv, Z. Nemo-like kinase (NLK) involves in neuronal apoptosis after traumatic brain injury. Cell. Mol. Neurobiol. 2012, 32, 381-389.
31. Hasegawa, Y.; Suzuki, H.; Sozen, T.; Altay, O.; Zhang, J.H. Apoptotic mechanisms for neuronal cells in early brain injury after subarachnoid hemorrhage. Acta Neurochir. Suppl. 2011, 110, 43-48.
32. Nakka, V.P.; Gusain, A.; Mehta, S.L.; Raghubir, R. Molecular mechanisms of apoptosis in cerebral ischemia: Multiple neuroprotective opportunities. Mol. Neurobiol. 2008, 37, 7-38.
33. Chen, F.; Chen, Y.; Kang, X.; Zhou, Z.; Zhang, Z.; Liu, D. Anti-apoptotic function and mechanism of ginseng saponins in Rattus pancreatic β-cells. Biol. Pharm. Bull. 2012, 35, 1568-1573.
34. Cai, B.X.; Jin, S.L.; Luo, D.; Lin, X.F.; Gao, J. Ginsenoside Rb1 suppresses ultraviolet radiation-induced apoptosis by inducing DNA repair. Biol. Pharm. Bull. 2009, 32, 837-841.
35. Liang, J.M.; Xu, H.Y.; Zhang, X.J.; Li, X.; Zhang, H.B.; Ge, P.F. Role of mitochondrial function in the protective effects of ischaemic postconditioning on ischaemia/reperfusion cerebral damage. J. Int. Med. Res. 2013, 41, 618-627.
36. Jiang, J.; Jiang, J.; Zuo, Y.; Gu, Z. Rapamycin protects the mitochondria against oxidative stress and apoptosis in a rat model of Parkinson's disease. Int. J. Mol. Med. 2013, 31, 825-832.
37. Agudo-López, A.; Miguel, B.G.; Fernández, I.; Martínez, A.M. Involvement of mitochondria on neuroprotective effect of sphingosine-1-phosphate in cell death in an in vitro model of brain ischemia. Neurosci. Lett. 2010, 470, 130-133.
38. Suski, J.M.; Lebiedzinska, M.; Bonora, M.; Pinton, P.; Duszynski, J.; Wieckowski, M.R. Relation between mitochondrial membrane potential and ROS formation. Methods Mol. Biol. 2012, 810, 183-205.
39. Lü, J.M.; Weakley, S.M.; Yang, Z.; Hu, M.; Yao, Q.; Chen, C. Ginsenoside Rb1 directly scavenges hydroxyl radical and hypochlorous acid. Curr. Pharm. Des. 2012, 18, 6339-6347.
40. Li, J.; Shao, Z.H.; Xie, J.T.; Wang, C.Z.; Ramachandran, S.; Yin, J.J.; Aung, H.; Li, C.Q.; Qin, G.; Hoek, T.V.; et al. The effects of ginsenoside Rb1 on JNK in oxidative injury in cardiomyocytes. Arch. Pharm. Res. 2012, 35, 1259-1267.
41. Kong, H.L.; Li, Z.Q.; Zhao, Y.J.; Zhao, S.M.; Zhu, L.; Li T, Fu, Y.; Li, H.J. Ginsenoside Rb1 protects cardiomyocytes against CoCl2-induced apoptosis in neonatal rats by inhibiting mitochondria permeability transition pore opening. Acta Pharmacol. Sin. 2010, 31, 687-695.
42. Kim, G.S.; Jung, J.E.; Narasimhan, P.; Sakata, H.; Yoshioka, H.; Song, Y.S.; Okami, N.; Chan, P.H. Release of mitochondrial apoptogenic factors and cell death are mediated by CK2 and NADPH oxidase. J. Cereb. Blood Flow Metab. 2012, 32, 720-730.
43. Culmsee, C.; Zhu, C.; Landshamer, S.; Becattini, B.; Wagner, E.; Pellecchia, M.; Blomgren, K.; Plesnila, N. Apoptosis-inducing factor triggered by poly(ADP-ribose) polymerase and Bid mediates neuronal cell death after oxygen-glucose deprivation and focal cerebral ischemia. J. Neurosci. 2005, 25, 10262-10272.
44. Hu, G.; Wu, Z.; Yang, F.; Zhao, H.; Liu, X.; Deng, Y.; Shi, M.; Zhao, G. Ginsenoside Rd blocks AIF mitochondrio-nuclear translocation and NF-κB nuclear accumulation by inhibiting poly(ADP-ribose) polymerase-1 after focal cerebral ischemia in rats. Neurol. Sci. 2013, doi:10.1007/s10072-013-1344-6.
45. Yang, X.; Wang, S.; Lin, Y.; Han, Y.; Qiu, X.; Zhao, X.; Cao, L.; Wang, X.; Chi, Z. Poly (ADP-ribose) polymerase inhibition protects epileptic hippocampal neurons from apoptosis via suppressing Akt-mediated apoptosis-inducing factor translocation in vitro. Neuroscience 2013, 231, 353-362.
46. Zemlyak, I.; Brooke, S.M.; Singh, M.H.; Sapolsky, R.M. Effects of overexpression of antioxidants on the release of cytochrome c and apoptosis-inducing factor in the model of ischemia. Neurosci. Lett. 2009, 453, 182-185.
47. Hashimoto, R.; Yu, J.; Koizumi, H.; Ouchi, Y.; Okabe, T. Ginsenoside Rb1 prevents MPP(+)-induced apoptosis in PC12 cells by stimulating estrogen receptors with consequent activation of ERK1/2, Akt and inhibition of SAPK/JNK, p38 MAPK. Evid. Based Complement. Alternat. Med. 2012, 2012, e693717.
48. Er, E.; Oliver, L.; Cartron, P.F.; Juin, P.; Manon, S.; Vallette, F.M. Mitochondria as the target of the pro-apoptotic protein Bax. Biochim. Biophys. Acta 2006, 1757, 1301-1311.