Immunomodulatory and neuroprotective effects of ginsenoside Rg1 in the MPTP(1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) -induced mouse model of Parkinson's disease

International Immunopharmacology

Volumn 29, Issue 2, 2015, Pages 334-343

  Zhou, Ting Ting ^a   Zu, Guo ^a   Wang, Xi ^a   Zhang, Xiao Gang ^a   Li, Shao ^a   Liang, Zhan Hua ^a   Zhao, Jie ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

Author keywords

Ginsenoside Rg1; Neurodegenerative disease; Neuroimmunology; Neuroprotection; Parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; GAMMA INTERFERON; GINSENOSIDE RG 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; GINSENOSIDE; IMMUNOLOGIC FACTOR; NEUROPROTECTIVE AGENT; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD25+ T LYMPHOCYTE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; IMMUNOMODULATION; LYMPHOCYTIC INFILTRATION; MALE; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; ANIMAL; BIOSYNTHESIS; BRAIN; C57BL MOUSE; DRUG EFFECTS; LYMPHOCYTE COUNT; METABOLISM; MPTP POISONING; PATHOLOGY; SUBSTANTIA NIGRA; T LYMPHOCYTE;

ANIMALS; BRAIN; CYTOKINES; GINSENOSIDES; IMMUNOLOGIC FACTORS; LYMPHOCYTE COUNT; MALE; MICE; MICE, INBRED C57BL; MPTP POISONING; NEUROPROTECTIVE AGENTS; SUBSTANTIA NIGRA; T-LYMPHOCYTES; TYROSINE 3-MONOOXYGENASE;

EID: 84948445951     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2015.10.032     Document Type: Article

References (50)

1. A.J. Lees, J. Hardy, and T. Revesz Parkinson's disease Lancet 373 2009 2055 2066
2. P. Jenner, and C.W. Olanow The pathogenesis of cell death in Parkinson's disease Neurology 66 2006 S24 S36
3. M.G. Tansey, and M.S. Goldberg Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention Neurobiol. Dis. 37 2010 510 518
4. H. Chen, E.J. O'Reilly, M.A. Schwarzschild, and A. Ascherio Peripheral inflammatory biomarkers and risk of Parkinson's disease Am. J. Epidemiol. 167 2008 90 95
5. Y.S. Kim, and T.H. Joh Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease Exp. Mol. Med. 38 2006 333 347
6. M.C. Hernández-Romero, M.J. Delgado-Cortés, M. Sarmiento, R.M. de Pablos, A.M. Espinosa-Oliva, S. Argüelles, and et al. Peripheral inflammation increases the deleterious effect of CNS inflammation on the nigrostriatal dopaminergic system Neurotoxicology 33 2012 347 360
7. S. Amor, and M.N. Woodroofe Innate and adaptive immune responses in neurodegeneration and repair Immunology 141 2014 287 291
8. L.W. Chen, Y.Q. Wang, L.C. Wei, M. Shi, and Y.S. Chan Chinese herbs and herbal extracts for neuroprotection of dopaminergic neurons and potential therapeutic treatment of Parkinson's disease CNS Neurol. Disord. Drug Targets 6 2007 273 281
9. 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
10. Q. Liu, J.P. Kou, and B.Y. Yu Ginsenoside Rg1 protects against hydrogen peroxide-induced cell death in PC12 cells via inhibiting NF-κB activation Neurochem. Int. 58 2011 119 125
11. 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
12. K.W. Leung, K.K. Yung, N.K. Mak, Y.S. Chan, T.P. Fan, and R.N. Wong Neuroprotective effects of ginsenoside-Rg1 in primary nigral neurons against rotenone toxicity Neuropharmacology 52 2007 827 835
13. G.E. Meredith, and D.J. Rademacher MPTP mouse models of Parkinson's disease: an update J. Park. Dis. 1 2011 19 33
14. S. Przedborski, V. Jackson-Lewis, R. Djaldetti, G. Liberatore, M. Vila, S. Vukosavic, and et al. The parkinsonian toxin MPTP: action and mechanism Restor. Neurol. Neurosci. 16 2000 135 142
15. C.W. Olanow, and A.H. Schapira Therapeutic prospects for Parkinson disease Ann. Neurol. 74 2013 337 347
16. V. Jackson-Lewis, and S. Przedborski Protocol for the MPTP mouse model of Parkinson's disease Nat. Protoc. 2 2007 141 151
17. E.C. Hirsch, and S. Hunot Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol. 8 2009 382 397
18. V. Brochard, B. Combadière, A. Prigent, Y. Laouar, A. Perrin, V. Beray-Berthat, and et al. Infiltration of CD4 + lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease J. Clin. Invest. 119 2009 182 192
19. K. Radad, R. Moldzio, and W.D. Rausch Ginsenosides and their CNS targets CNS Neurosci. Ther. 17 2011 761 768
20. 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
21. 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
22. 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
23. D.K. Stone, A.D. Reynolds, R.L. Mosley, and H.E. Gendelman Innate and adaptive immunity for the pathobiology of Parkinson's disease Antioxid. Redox Signal. 11 2009 2151 2166
24. Y. Yang, X. Li, L. Zhang, L. Liu, G. Jing, and H. Cai Ginsenoside Rg1 suppressed inflammation and neuron apoptosis by activating PPARγ/HO-1 in hippocampus in rat model of cerebral ischemia-reperfusion injury Int. J. Clin. Exp. Pathol. 8 2015 2484 2494
25. Y. Zong, Q.L. Ai, L.M. Zhong, J.N. Dai, P. Yang, Y. He, and et al. Ginsenoside Rg1 attenuates lipopolysaccharide-induced inflammatory responses via the phospholipase C-γ1 signaling pathway in murine BV-2 microglial cells Curr. Med. Chem. 19 2012 770 779
26. S. Amor, L.A. Peferoen, D.Y. Vogel, M. Breur, P. van der Valk, D. Baker, and et al. Inflammation in neurodegenerative diseases - an update Immunology 142 2014 151 166
27. C.F. Orr, D.B. Rowe, Y. Mizuno, H. Mori, and G.M. Halliday A possible role for humoral immunity in the pathogenesis of Parkinson's disease Brain 128 2005 2665 2674
28. K. Hisanaga, M. Asagi, Y. Itoyama, and Y. Iwasaki Increase in peripheral CD4 bright + CD8 dull + T cells in Parkinson disease Arch. Neurol. 58 2001 1580 1583
29. J. Bas, M. Calopa, M. Mestre, D.G. Molleví, B. Cutillas, S. Ambrosio, and et al. Lymphocyte populations in Parkinson's disease and in rat models of parkinsonism J. Neuroimmunol. 113 2001 146 152
30. A.D. Reynolds, R. Banerjee, J. Liu, H.E. Gendelman, and R.L. Mosley Neuroprotective activities of CD4 + CD25 + regulatory T cells in an animal model of Parkinson's disease J. Leukoc. Biol. 82 2007 1083 1094
31. A.D. Reynolds, D.K. Stone, R.L. Mosley, and H.E. Gendelman Nitrated {alpha}-synuclein-induced alterations in microglial immunity are regulated by CD4 + T cell subsets J. Immunol. 182 2009 4137 4149
32. Y. Baba, A. Kuroiwa, R.J. Uitti, Z.K. Wszolek, and T. Yamada Alterations of T-lymphocyte populations in Parkinson disease Parkinsonism Relat. Disord. 11 2005 493 498
33. G. Laćan, H. Dang, B. Middleton, M.A. Horwitz, J. Tian, W.P. Melega, and et al. Bacillus Calmette-Guerin vaccine-mediated neuroprotection is associated with regulatory T-cell induction in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease J. Neurosci. Res. 91 2013 1292 1302
34. C.A. Dinarello Historical insights into cytokines Eur. J. Immunol. 37 2007 S34 S45
35. D. Koziorowski, R. Tomasiuk, S. Szlufik, and A. Friedman Inflammatory cytokines and NT-proCNP in Parkinson's disease patients Cytokine 60 2012 762 766
36. R.J. Dobbs, A. Charlett, A.G. Purkiss, S.M. Dobbs, C. Weller, and D.W. Peterson Association of circulating TNF-alpha and IL-6 with ageing and parkinsonism Acta Neurol. Scand. 100 1999 34 41
37. M.P. Mount, A. Lira, D. Grimes, P.D. Smith, S. Faucher, R. Slack, and et al. Involvement of interferon-gamma in microglial-mediated loss of dopaminergic neurons J. Neurosci. 27 2007 3328 3337
38. V.H. Perry, and J. Teeling Microglia and macrophages of the central nervous system: the contribution of microglia priming and systemic inflammation to chronic neurodegeneration Semin. Immunopathol. 35 2013 601 612
39. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo Science 308 2005 1314 1318
40. P.L. McGeer, C. Schwab, A. Parent, and D. Doudet Presence of reactive microglia in monkey substantia nigra years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine administration Ann. Neurol. 54 2003 599 604
41. B. Liu, and J.S. Hong Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention J. Pharmacol. Exp. Ther. 304 2003 1 7
42. Z. Chen, and T.D. Palmer Cellular repair of CNS disorders: an immunological perspective Hum. Mol. Genet. 17 2008 R84 R92
43. R. Kortekaas, K.L. Leenders, J.C. van Oostrom, W. Vaalburg, J. Bart, A.T. Willemsen, and et al. Blood-brain barrier dysfunction in parkinsonian midbrain in vivo Ann. Neurol. 57 2005 176 179
44. I. Kurkowska-Jastrzebska, A. Wrońska, M. Kohutnicka, A. Członkowski, and A. Członkowska MHC class II positive microglia and lymphocytic infiltration are present in the substantia nigra and striatum in mouse model of Parkinson's disease Acta Neurobiol. Exp. (Wars) 59 1999 1 8
45. C. Depboylu, S. Stricker, J.P. Ghobril, W.H. Oertel, J. Priller, and G.U. Höglinger Brain-resident microglia predominate over infiltrating myeloid cells in activation, phagocytosis and interaction with T-lymphocytes in the MPTP mouse model of Parkinson disease Exp. Neurol. 238 2012 183 191
46. E.C. Hirsch, T. Breidert, E. Rousselet, S. Hunot, A. Hartmann, and P.P. Michel The role of glial reaction and inflammation in Parkinson's disease Ann. N. Y. Acad. Sci. 991 2003 214 228
47. K.W. Leung, Y.L. Pon, R.N. Wong, and A.S. Wong Ginsenoside-Rg1 induces vascular endothelial growth factor expression through the glucocorticoid receptor-related phosphatidylinositol 3-kinase/Akt and beta-catenin/T-cell factor-dependent pathway in human endothelial cells J. Biol. Chem. 281 2006 36280 36288
48. W.F. Chen, W.S. Lau, P.Y. Cheung, D.A. Guo, and M.S. Wong Activation of insulin-like growth factor I receptor-mediated pathway by ginsenoside Rg1 Br. J. Pharmacol. 147 2006 542 551
49. B. Johannesson, S. Sattler, E. Semenova, and S. Pastore Insulin-like growth factor-1 induces regulatory T cell-mediated suppression of allergic contact dermatitis in mice Dis. Model. Mech. 7 2014 977 985
50. X. Liu, C. Linnington, H.D. Webster, S. Lassmann, D.L. Yao, L.D. Hudson, H. Wekerle, and G.W. Kreutzberg Insulin-like growth factor-I treatment reduces immune cell responses in acute non-demyelinative experimental autoimmune encephalomyelitis J. Neurosci. Res. 47 1997 531 538