Ginsenoside Rd ameliorates experimental autoimmune encephalomyelitis in C57BL/6 mice

Journal of Neuroscience Research

Volumn 92, Issue 9, 2014, Pages 1217-1226

  Zhu, Dongliang ^a   Liu, Mei ^a   Yang, Yaowu ^a   Ma, Lili ^a   Jiang, Ying ^a   Zhou, Linli ^a   Huang, Qiling ^a   Pi, Rongbiao ^a   Chen, Xiaohong ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Experimental autoimmune encephalomyelitis; Ginsenoside Rd; Multiple sclerosis; Therapy

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GAMMA INTERFERON; GINSENOSIDE RD; INTERLEUKIN 4; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; NERVE GROWTH FACTOR; GINSENOSIDE; MYELIN OLIGODENDROCYTE GLYCOPROTEIN (35-55); PEPTIDE FRAGMENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE COURSE; DRUG EFFICACY; DRUG INHIBITION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LUMBAR SPINAL CORD; MEMBRANE PERMEABILITY; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; SUPERNATANT; TH2 CELL; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; C57BL MOUSE; CAPILLARY PERMEABILITY; CHEMICALLY INDUCED; CHEMISTRY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME LINKED IMMUNOSORBENT ASSAY; LYMPHOCYTE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; SPINAL CORD; TOXICITY;

ANALYSIS OF VARIANCE; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CAPILLARY PERMEABILITY; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GINSENOSIDES; INTERFERON-GAMMA; INTERLEUKIN-4; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE FRAGMENTS; SPINAL CORD;

EID: 84904245385     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23397     Document Type: Article

References (47)

1. Abbott NJ. 2002. Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 200:629-638.
2. Arredondo LR, Deng C, Ratts RB, Lovett-Racke AE, Holtzman DM, Racke MK. 2001. Role of nerve growth factor in experimental autoimmune encephalomyelitis. Eur J Immunol 31:625-633.
3. Attele AS, Wu JA, Yuan CS. 1999. Ginseng pharmacology: multiple constituents and multiple actions. Biochem Pharmacol 58:1685-1693.
4. Brodie C. 1996. Differential effects of Th1 and Th2 derived cytokines on NGF synthesis by mouse astrocytes. FEBS Lett 394:117-120.
5. Brodie C, Goldreich N. 1994. Interleukin-4 modulates the proliferation and differentiation of glial cells. J Neuroimmunol 55:91-97.
6. Brodie C, Goldreich N, Haiman T, Kazimirsky G. 1998. Functional IL-4 receptors on mouse astrocytes: IL-4 inhibits astrocyte activation and induces NGF secretion. J Neuroimmunol 81:20-30.
7. Caggiula M, Batocchi AP, Frisullo G, Angelucci F, Patanella AK, Sancricca C, Nociti V, Tonali PA, Mirabella M. 2005. Neurotrophic factors and clinical recovery in relapsing-remitting multiple sclerosis. Scand J Immunol 62:176-182.
8. Chen X, Hu X, Zou Y, Pi R, Liu M, Wang T, Zheng X, Lin M, Liu P, Tao L. 2009. Combined treatment with minocycline and prednisone attenuates experimental autoimmune encephalomyelitis in C57 BL/6 mice. J Neuroimmunol 210:22-29.
9. de Araujo-Martins L, de Oliveira RM, dos Santos GV, dos Santos RC, dos Santos AA, Giestal de Araujo E. 2013. Treatment in vitro of retinal cells with IL-4 increases the survival of retinal ganglion cells: the involvement of BDNF. Neurochem Res 38:162-173.
10. Derecki NC, Cardani AN, Yang CH, Quinnies KM, Crihfield A, Lynch KR, Kipnis J. 2010. Regulation of learning and memory by meningeal immunity: a key role for IL-4. J Exp Med 207:1067-1080.
11. de Vries HE, Kuiper J, de Boer AG, Van Berkel TJ, Breimer DD. 1997. The blood-brain barrier in neuroinflammatory diseases. Pharmacol Rev 49:143-155.
12. D'Intino G, Paradisi M, Fernandez M, Giuliani A, Aloe L, Giardino L, Calza L. 2005. Cognitive deficit associated with cholinergic and nerve growth factor downregulation in experimental allergic encephalomyelitis in rats. Proc Natl Acad Sci U S A 102:3070-3075.
13. Frischer JM, Bramow S, Dal-Bianco A, Lucchinetti CF, Rauschka H, Schmidbauer M, Laursen H, Sorensen PS, Lassmann H. 2009. The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 132:1175-1189.
14. Heese K, Inoue N, Sawada T. 2006. NF-κB regulates B-cell-derived nerve growth factor expression. Cell Mol Immunol 3:63-66.
15. Hohlfeld R. 2008. Neurotrophic cross-talk between the nervous and immune systems: relevance for repair strategies in multiple sclerosis? J Neurol Sci 265:93-96.
16. Hu G, Wu Z, Yang F, Zhao H, Liu X, Deng Y, Shi M, Zhao G. 2013. 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 34:2101-2106.
17. Jiang Y, Zou Y, Chen S, Zhu C, Wu A, Liu Y, Ma L, Zhu D, Ma X, Liu M, Kang Z, Pi R, Peng F, Wang Q, Chen X. 2013. The anti-inflammatory effect of donepezil on experimental autoimmune encephalomyelitis in C57 BL/6 mice. Neuropharmacology 73:415-424.
18. Kerschensteiner M, Meinl E, Hohlfeld R. 2009. Neuro-immune crosstalk in CNS diseases. Neuroscience 158:1122-1132.
19. Kuerten S, Kostova-Bales DA, Frenzel LP, Tigno JT, Tary-Lehmann M, Angelov DN, Lehmann PV. 2007. MP4- and MOG:35-55-induced EAE in C57BL/6 mice differentially targets brain, spinal cord and cerebellum. J Neuroimmunol 189:31-40.
20. Li L, Liu Z, Liu J, Tai X, Hu X, Liu X, Wu Z, Zhang G, Shi M, Zhao G. 2013. Ginsenoside Rd attenuates beta-amyloid-induced tau phosphorylation by altering the functional balance of glycogen synthase kinase 3beta and protein phosphatase 2A. Neurolbiol Dis 54:320-328.
21. Liu J, Yan X, Li L, Zhu Y, Qin K, Zhou L, Sun D, Zhang X, Ye R, Zhao G. 2012a. Ginsennoside rd attenuates cognitive dysfunction in a rat model of Alzheimer's disease. Neurochem Res 37:2738-2747.
22. Liu X, Wang L, Wen A, Yang J, Yan Y, Song Y, Liu X, Ren H, Wu Y, Li Z, Chen W, Xu Y, Li L, Xia J, Zhao G. 2012b. Ginsenoside-Rd improves outcome of acute ischaemic stroke-a randomized, double-blind, placebo-controlled, multicenter trial. Eur J Neurol 19:855-863.
23. Makar TK, Bever CT, Singh IS, Royal W, Sahu SN, Sura TP, Sultana S, Sura KT, Patel N, Dhib-Jalbut S, Trisler D. 2009. Brain-derived neurotrophic factor gene delivery in an animal model of multiple sclerosis using bone marrow stem cells as a vehicle. J Neuroimmunol 210:40-51.
24. McGeachy MJ, Anderton SM. 2005. Cytokines in the induction and resolution of experimental autoimmune encephalomyelitis. Cytokine 32:81-84.
25. McTigue DM, Horner PJ, Stokes BT, Gage FH. 1998. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci 18:5354-5365.
26. Minagar A, Alexander JS. 2003. Blood-brain barrier disruption in multiple sclerosis. Mult Scler 9:540-549.
27. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. 2000. Multiple sclerosis. N Engl J Med 343:938-952.
28. O'Neill EJ, Day MJ, Wraith DC. 2006. IL-10 is essential for disease protection following intranasal peptide administration in the C57BL/6 model of EAE. J Neuroimmunol 178:1-8.
29. Oreja-Guevara C, Ramos-Cejudo J, Aroeira LS, Chamorro B, Diez-Tejedor E. 2012. TH1/TH2 Cytokine profile in relapsing-remitting multiple sclerosis patients treated with Glatiramer acetate or Natalizumab. BMC Neurol 12:95.
30. Poliana PL, Brok H, Furlan R, Ruffini F, Bergami A, Desina G, Marconi PC, Rovaris M, Uccelli A, Glorioso JC, Penna G, Adorini L, Comi G, 't Hart B, Martino G. 2001. Delivery to the central nervous system of a nonreplicative herpes simplex type 1 vector engineered with the interleukin 4 gene protects rhesus monkeys from hyperacute autoimmune encephalomyelitis. Hum Gene Ther 12:905-920.
31. Shang W, Yang Y, Jiang B, Jin H, Zhou L, Liu S, Chen M. 2007. Ginsenoside Rb1 promotes adipogenesis in 3T3-L1 cells by enhancing PPARgamma2 and C/EBPalpha gene expression. Life Sci 80:618-625.
32. Stadelmann C, Wegner C, Bruck W. 2011. Inflammation, demyelination, and degeneration-recent insights from MS pathology. Biochim Biophys Acta 1812:275-282.
33. Steinman L. 2007. A brief history of T(h)17, the first major revision in the T(h)1/T(h)2 hypothesis of T cell-mediated tissue damage. Nat Med 13:139-145.
34. Tysiak E, Asbach P, Aktas O, Waiczies H, Smyth M, Schnorr J, Taupitz M, Wuerfel J. 2009. Beyond blood-brain barrier breakdown-in vivo detection of occult neuroinflammatory foci by magnetic nanoparticles in high field MRI. J Neuroinflammation 6:20.
35. Valenzuela RM, Costello K, Chen M, Said A, Johnson KP, Dhib-Jalbut S. 2007. Clinical response to glatiramer acetate correlates with modulation of IFN-gamma and IL-4 expression in multiple sclerosis. Mult Scler 13:754-762.
36. Villoslada P, Hauser SL, Bartke I, Unger J, Heald N, Rosenberg D, Cheung SW, Mobley WC, Fisher S, Genain CP. 2000. Human nerve growth factor protects common marmosets against autoimmune encephalomyelitis by switching the balance of T helper cell type 1 and 2 cytokines within the central nervous system. J Exp Med 191:1799-1806.
37. Virley DJ. 2005. Developing therapeutics for the treatment of multiple sclerosis. NeuroRx 2:638-649.
38. Wang L, Zhang Y, Wang Z, Li S, Min G, Wang L, Chen J, Cheng J, Wu Y. 2012a. Inhibitory effect of ginsenoside-Rd on carrageenan-induced inflammation in rats. Can J Physiol Pharmacol 90:229-236.
39. Wang L, Zhang Y, Chen J, Li S, Wang Y, Hu L, Wang L, Wu Y. 2012b. Immunosuppressive effects of ginsenoside-Rd on skin allograft rejection in rats. J Surg Res 176:267-274.
40. Wang Y, Li X, Wang X, Lau W, Wang Y, Xing Y, Zhang X, Ma X, Gao F. 2013. Ginsenoside Rd attenuates myocardial ischemia/reperfusion injury via Akt/GSK-3β signaling and inhibition of the mitochondria-dependent apoptptic pathway. PLoS One 8:e70956.
41. Wu CF, Bi XL, Yang JY, Zhan JY, Dong YX, Wang JH, Wang JM, Zhang R, Li X. 2007. Differential effects of ginsenosides on NO and TNF-alpha production by LPS-activated N9 microglia. Immunopharmacology 7:313-320.
42. Ye R, Han J, Kong X, Zhao L, Cao R, Rao Z, Zhao G. 2008. Protective effects of ginsenoside Rd on PC12 cells against hydrogen peroxide. Biol Pharm Bull 31:1923-1927.
43. Ye R, Kong X, Yang Q, Zhang Y, Han J, Zhao G. 2011. Ginsenoside Rd attenuates redox imbalance and improves stroke outcome after focal cerebral ischemia in aged mice. Neuropharmacology 61:815-824.
44. Ye R, Li N, Han J, Kong X, Cao R, Rao Z, Zhao G. 2009. Neuroprotective effects of ginsenoside Rd against oxygen-glucose deprivation in cultured hippocampal neurons. Neurosci Res 64:306-310.
45. Yoshimura A, Mori H, Ohishi M, Aki D, Hanada T. 2003. Negative regulation of cytokine signaling influences inflammation. Curr Opin Immunol 15:704-708.
46. 2+ influx. Cell Mol Neurobiol 32:121-128.
47. Zhang YX, Wang L, Xiao EL, Li SJ, Chen JJ, Gao B, Min GN, Wang ZP, Wu YJ. 2013. Ginsenoside Rd exhibits anti-inflammatory activities thriugh elevation of antioxidant enzyme activities and inhibition of JNK and ERK activation in vivo. Int Immunopharmacol 17:1094-1100.