Neuroprotective effects of ginsenoside Rg1 through the Wnt/β-catenin signaling pathway in both in vivo and in vitro models of Parkinson's disease

Neuropharmacology

Volumn 101, Issue , 2016, Pages 480-489

  Zhou, Tingting ^a   Zu, Guo ^a   Zhang, Xiaogang ^a   Wang, Xi ^a   Li, Shao ^a   Gong, Xiaoyang ^a   Liang, Zhanhua ^a   Zhao, Jie ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

Author keywords

Ginsenoside Rg1; Neurodegeneration; Neuroprotection; Parkinson's disease; Wnt catenin signaling pathway

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; BETA CATENIN; DICKKOPF 1 PROTEIN; GINSENOSIDE RG 1; MESSENGER RNA; PROTEIN; WNT PROTEIN; GINSENOSIDE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; NEUROPROTECTIVE AGENT; TYROSINE 3 MONOOXYGENASE; WNT1 PROTEIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL LOSS; CELL VIABILITY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SUBSTANTIA NIGRA PARS COMPACTA; WNT SIGNALING PATHWAY; ANIMAL; BRAIN; C57BL MOUSE; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MPTP POISONING; PC12 CELL LINE; TIME FACTOR; TUNEL ASSAY;

ANIMALS; BETA CATENIN; BRAIN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; GINSENOSIDES; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; IN SITU NICK-END LABELING; MICE; MICE, INBRED C57BL; MPTP POISONING; NEUROPROTECTIVE AGENTS; PC12 CELLS; RATS; RNA, MESSENGER; TIME FACTORS; TYROSINE 3-MONOOXYGENASE; WNT SIGNALING PATHWAY; WNT1 PROTEIN;

EID: 84946208322     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.10.024     Document Type: Article

References (49)

1. R.S. Akhtar, J.M. Ness, and K.A. Roth Bcl-2 family regulation of neuronal development and neurodegeneration Biochim. Biophys. Acta 1644 2004 189 203
2. E.R. Andersson, C. Saltó, J.C. Villaescusa, L. Cajanek, S. Yang, L. Bryjova, I.I. Nagy, S.J. Vainio, C. Ramirez, V. Bryja, and E. Arenas Wnt5a cooperates with canonical Wnts to generate midbrain dopaminergic neurons in vivo and in stem cells Proc. Natl. Acad. Sci. U. S. A. 110 2013 E602 E610
3. M.T. Ardah, K.E. Paleologou, G. Lv, S.A. Menon, S.B. Abul Khair, J.H. Lu, B. Safieh-Garabedian, A.A. Al-Hayani, D. Eliezer, M. Li, and O. El-Agnaf Ginsenoside Rb1 inhibits fibrillation and toxicity of alpha-synuclein and disaggregates preformed fibrils Neurobiol. Dis. 74 2015 89 101
4. E. Arenas Wnt signaling in midbrain dopaminergic neuron development and regenerative medicine for Parkinson's disease J. Mol. Cell Biol. 6 2014 42 53
5. J.L. Badger, O. Cordero-Llana, E.M. Hartfield, and R. Wade-Martins Parkinson's disease in a dish - using stem cells as a molecular tool Neuropharmacology 76 Pt A 2014 88 96
6. G. Castelo-Branco, and E. Arenas Function of Wnts in dopaminergic neuron development Neurodegener. Dis. 3 2006 5 11
7. G. Castelo-Branco, N. Rawal, and E. Arenas GSK-3beta inhibition/beta-catenin stabilization in ventral midbrain precursors increases differentiation into dopamine neurons J. Cell Sci. 117 2004 5731 5737
8. G. Castelo-Branco, J. Wagner, F.J. Rodriguez, J. Kele, K. Sousa, N. Rawal, H.A. Pasolli, E. Fuchs, J. Kitajewski, and E. Arenas Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a Proc. Natl. Acad. Sci. U. S. A. 100 2003 12747 12752
9. B.Y. Chen, X. Wang, Z.Y. Wang, Y.Z. Wang, L.W. Chen, and Z.J. Luo Brain-derived neurotrophic factor stimulates proliferation and differentiation of neural stem cells, possibly by triggering the Wnt/β-catenin signaling pathway J. Neurosci. Res. 91 2013 30 41
10. X.C. Chen, Y. Chen, Y.G. Zhu, F. Fang, and L.M. Chen Protective effect of ginsenoside Rg1 against MPTP-induced apoptosis in mouse substantia nigra neurons Acta Pharmacol. Sin. 23 2002 829 834
11. X.C. Chen, Y.C. Zhou, Y. Chen, Y.G. Zhu, F. Fang, and L.M. Chen Ginsenoside Rg1 reduces MPTP-induced substantia nigra neuron loss by suppressing oxidative stress Acta Pharmacol. Sin. 26 2005 56 62
12. X.C. Chen, Y.G. Zhu, L.A. Zhu, C. Huang, Y. Chen, L.M. Chen, F. Fang, Y.C. Zhou, and C.H. Zhao Ginsenoside Rg1 attenuates dopamine-induced apoptosis in PC12 cells by suppressing oxidative stress Eur. J. Pharmacol. 473 2003 1 7
13. H. Clevers Wnt/beta-catenin signaling in development and disease Cell 127 2006 469 480
14. H. Clevers, and R. Nusse Wnt/β-catenin signaling and disease Cell 149 2012 1192 1205
15. Y. Dun, Y. Yang, Z. Xiong, M. Feng, Y. Zhang, M. Wang, J. Xiang, G. Li, and R. Ma Induction of Dickkopf-1 contributes to the neurotoxicity of MPP+ in PC12 cells via inhibition of the canonical Wnt signaling pathway Neuropharmacology 67 2013 168 175
16. O. Eberhardt, and J.B. Schulz Apoptotic mechanisms and antiapoptotic therapy in the MPTP model of Parkinson's disease Toxicol. Lett. 139 2003 135 151
17. N.R. Goldberg, A.K. Haack, N.S. Lim, O.K. Janson, and C.K. Meshul Dopaminergic and behavioral correlates of progressive lesioning of the nigrostriatal pathway with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine Neuroscience 180 2011 256 271
18. E. González-Burgos, C. Fernandez-Moriano, and M.P. Gómez-Serranillos Potential neuroprotective activity of Ginseng in Parkinson's disease: a review J. Neuroimmune Pharmacol. 10 2015 14 29
19. K. Harvey, and B. Marchetti Regulating Wnt signaling: a strategy to prevent neurodegeneration and induce regeneration J. Mol. Cell Biol. 6 2014 1 2
20. N.C. Inestrosa, and E. Arenas Emerging roles of Wnts in the adult nervous system Nat. Rev. Neurosci. 11 2010 77 86
21. Y. Itano, Y. Kitamura, and Y. Nomura 1-Methyl-4-phenylpyridinium (MPP+)-induced cell death in PC12 cells: inhibitory effects of several drugs Neurochem. Int. 25 1994 419 424
22. V. Jackson-Lewis, and S. Przedborski Protocol for the MPTP mouse model of Parkinson's disease Nat. Protoc. 2 2007 141 151
23. P. Jenner, and C.W. Olanow The pathogenesis of cell death in Parkinson's disease Neurology 66 2006 S24 S36
24. H. Jiang, P. He, C.H. Adler, H. Shill, T.G. Beach, R. Li, and Y. Shen Bid signal pathway components are identified in the temporal cortex with Parkinson disease Neurology 79 2012 1767 1773
25. F. L'Episcopo, C. Tirolo, N. Testa, S. Caniglia, M.C. Morale, C. Cossetti, P. D'Adamo, E. Zardini, L. Andreoni, A.E. Ihekwaba, P.A. Serra, D. Franciotta, G. Martino, S. Pluchino, and B. Marchetti Reactive astrocytes and Wnt/β-catenin signaling link nigrostriatal injury to repair in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease Neurobiol. Dis. 41 2011 508 527
26. F. L'Episcopo, C. Tirolo, N. Testa, S. Caniglia, M.C. Morale, M. Deleidi, M.F. Serapide, S. Pluchino, and B. Marchetti Plasticity of subventricular zone neuroprogenitors in MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) mouse model of Parkinson's disease involves cross talk between inflammatory and Wnt/β-catenin signaling pathways: functional consequences for neuroprotection and repair J. Neurosci. 32 2012 2062 2085
27. F. L'Episcopo, C. Tirolo, N. Testa, S. Caniglia, M.C. Morale, M.F. Serapide, S. Pluchino, and B. Marchetti Wnt/β-catenin signaling is required to rescue midbrain dopaminergic progenitors and promote neurorepair in ageing mouse model of Parkinson's disease Stem Cells 32 2014 2147 2163
28. A.J. Lees, J. Hardy, and T. Revesz Parkinson's disease Lancet 373 2009 2055 2066
29. B.T. MacDonald, K. Tamai, and X. He Wnt/beta-catenin signaling: components, mechanisms, and diseases Dev. Cell 17 2009 9 26
30. B. Marchetti, F. L'Episcopo, M.C. Morale, C. Tirolo, N. Testa, S. Caniglia, M.F. Serapide, and S. Pluchino Uncovering novel actors in astrocyte-neuron crosstalk in Parkinson's disease: the Wnt/β-catenin signaling cascade as the common final pathway for neuroprotection and self-repair Eur. J. Neurosci. 37 2013 1550 1563
31. K. Matsuura, H. Kabuto, H. Makino, and N. Ogawa Pole test is a useful method for evaluating the mouse movement disorder caused by striatal dopamine depletion J. Neurosci. Methods 73 1997 45 48
32. R.T. Moon, A.D. Kohn, G.V. De Ferrari, and A. Kaykas WNT and beta-catenin signalling: diseases and therapies Nat. Rev. Genet. 5 2004 691 701
33. S.Y. Nah, D.H. Kim, and H. Rhim Ginsenosides: are any of them candidates for drugs acting on the central nervous system? CNS Drug Rev. 13 2007 381 404
34. A. Nicotra, and S. Parvez Apoptotic molecules and MPTP-induced cell death Neurotoxicol. Teratol. 24 2002 599 605
35. C.W. Olanow, and A.H. Schapira Therapeutic prospects for Parkinson disease Ann. Neurol. 74 2013 337 347
36. C.L. Parish, and L.H. Thompson Modulating Wnt signaling to improve cell replacement therapy for Parkinson's disease J. Mol. Cell Biol. 6 2014 54 63
37. S. Przedborski, V. Jackson-Lewis, R. Djaldetti, G. Liberatore, M. Vila, S. Vukosavic, and G. Almer The parkinsonian toxin MPTP: action and mechanism Restor. Neurol. Neurosci. 16 2000 135 142
38. K. Radad, G. Gille, L. Liu, and W.D. Rausch Use of ginseng in medicine with emphasis on neurodegenerative disorders J. Pharmacol. Sci. 100 2006 175 186
39. K. Radad, G. Gille, R. Moldzio, H. Saito, and W.D. Rausch Ginsenosides Rb1 and Rg1 effects on mesencephalic dopaminergic cells stressed with glutamate Brain Res. 1021 2004 41 53
40. K. Radad, R. Moldzio, and W.D. Rausch Ginsenosides and their CNS targets CNS Neurosci. Ther. 17 2011 761 768
41. A.H. Schapira Molecular and clinical pathways to neuroprotection of dopaminergic drugs in Parkinson disease Neurology 72 2009 S44 S50
42. M.D. Sconce, M.J. Churchill, R.E. Greene, and C.K. Meshul Intervention with exercise restores motor deficits but not nigrostriatal loss in a progressive MPTP mouse model of Parkinson's disease Neuroscience 23 2015 156 174
43. E.L. Scott, and D.W. Brann Estrogen regulation of Dkk1 and Wnt/β-Catenin signaling in neurodegenerative disease Brain Res. 1514 2013 63 74
44. M. Sedelis, R.K. Schwarting, and J.P. Huston Behavioral phenotyping of the MPTP mouse model of Parkinson's disease Behav. Brain Res. 125 2001 109 125
45. L. Shen, and J. Zhang NMDA receptor and iNOS are involved in the effects of ginsenoside Rg1 on hippocampal neurogenesis in ischemic gerbils Neurol. Res. 29 2007 270 273
46. M.T. Veeman, J.D. Axelrod, and R.T. Moon A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling Dev. Cell 5 2003 367 377
47. W. Wang, C. Ma, Z. Mao, and M. Li JNK inhibition as a potential strategy in treating Parkinson's disease Drug News Perspect. 17 2004 646 654
48. L. Xu, W.F. Chen, and M.S. Wong Ginsenoside Rg1 protects dopaminergic neurons in a rat model of Parkinson's disease through the IGF-I receptor signalling pathway Br. J. Pharmacol. 158 2009 738 748
49. Y.X. Yang, N.W. Wood, and D.S. Latchman Molecular basis of Parkinson's disease Neuroreport 20 2009 150 156