The anti-inflammatory effect of donepezil on experimental autoimmune encephalomyelitis in C57 BL/6 mice

Neuropharmacology

Volumn 73, Issue , 2013, Pages 415-424

  Jiang, Ying ^a   Yan, Zou ^a   Chen, Shaoqiong ^a   Zhu, Cansheng ^a   Wu, Aimin ^a   Liu, Yingying ^a   Ma, Lili ^a   Zhu, Dongliang ^a   Ma, Xiaomeng ^a   Liu, Mei ^a   Kang, Zhuang ^a   Pi, Rongbiao ^a   Peng, Fuhua ^a   Wang, Qing ^a   Chen, Xiaohong ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Anti inflammatory effect; Bloodebrain barrier; Donepezil; Encephalomyelitis; Experimental autoimmune; Interferon ; Interleukin 4; Matrix metalloproteinase 2; Matrix metalloproteinase 9; Nerve growth factor

Indexed keywords

DONEPEZIL; EVANS BLUE; GAMMA INTERFERON; GELATINASE A; GELATINASE B; INTERLEUKIN 4; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; NERVE GROWTH FACTOR; PHOSPHATE BUFFERED SALINE; PROTEIN KINASE B; PROTEIN PRECURSOR;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; BRAIN; CELL CULTURE; CONTROLLED STUDY; DISEASE SEVERITY; DOSE RESPONSE; DOWN REGULATION; DRUG EFFICACY; EARLY INTERVENTION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; FEMALE; HISTOPATHOLOGY; MOUSE; NONHUMAN; POST EXPOSURE PROPHYLAXIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCORING SYSTEM; SPLEEN CELL; SUPERNATANT; TREATMENT DURATION; WESTERN BLOTTING;

ANTI-INFLAMMATORY EFFECT; BLOOD-BRAIN BARRIER; DONEPEZIL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; INTERFERON-Γ; INTERLEUKIN-4; MATRIX METALLOPROTEINASE-2; MATRIX METALLOPROTEINASE-9; NERVE GROWTH FACTOR;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BLOOD-BRAIN BARRIER; BRAIN; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; EVANS BLUE; FEMALE; INDANS; INTERFERON-GAMMA; INTERLEUKIN-4; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTOR; PHOSPHORYLATION; PIPERIDINES; PROTEIN PRECURSORS; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84885159099     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.06.023     Document Type: Article

References (69)

1. Anthony, D.C., Ferguson, B., Matyzak, M.K., Miller, K.M., Esiri, M.M., Perry, V.H., 1997. Differential matrix metalloproteinase expression in cases of multiple sclerosis and stroke. Neuropathol. Appl. Neurobiol. 23, 406-415.
2. Arikawa, M., Kakinuma, Y., Handa, T., Yamasaki, F., Sato, T., 2011. Donepezil, antiAlzheimer's disease drug, prevents cardiac rupture during acute phase of myocardial infarction in mice. PLoS One 6, e20629.
3. Arredondo, L.R., Deng, C., Ratts, R.B., Lovett-Racke, A.E., Holtzman, D.M., Racke, M.K., 2001. Role of nerve growth factor in experimental autoimmune encephalomyelitis. Eur. J. Immunol. 31, 625-633.
4. Avolio, C., Ruggieri, M., Giuliani, F., Liuzzi, G.M., Leante, R., Riccio, P., Livrea, P., Trojano, M., 2003. Serum MMP-2 and MMP-9 are elevated in different multiple sclerosis subtypes. J. Neuroimmunol. 136, 46-53.
5. Awatsuji, H., Furukawa, Y., Hirota, M., Furukawa, S., Hayashi, K., 1995. Interferons suppress nerve growth factor synthesis as a result of interference with cell growth in astrocytes cultured from neonatal mouse brain. J. Neurochem. 64, 1476-1482.
6. Awatsuji, H., Furukawa, Y., Hirota, M., Murakami, Y., Nii, S., Furukawa, S., Hayashi, K., 1993. Interleukin-4 and -5 as modulators of nerve growth factor synthesis/secretion in astrocytes. J. Neurosci. Res. 34, 539-545.
7. Benesová, Y., Vasku, A., Novotná, H., Litzman, J., Stourac, P., Beránek, M., Kadanka, Z., Bednarík, J., 2009. Matrix metalloproteinase-9 and matrix metalloproteinase-2 as biomarkers of various courses in multiple sclerosis. Mult. Scler. 15, 316-322.
8. Brodie, C., 1996. Differential effects of Th1 and Th2 derived cytokines on NGF synthesis by mouse astrocytes. FEBS Lett. 394, 117-120.
9. Brodie, C., Goldreich, N., 1994. Interleukin-4 modulates the proliferation and differentiation of glial cells. J. Neuroimmunol. 55, 91-97.
10. 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.
11. Bruno, M.A., Cuello, A.C., 2006. Activity-dependent release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by a protease cascade. Proc. Natl. Acad. Sci. U. S. A. 103, 6735-6740.
12. Chen, X., Hu, X., Zou, Y., Pi, R., Liu, M., Wang, T., Zheng, X., Liu, M., 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.
13. Chen, X., Ma, L., Jiang, Y., Chen, S., Zhu, C., Liu, M., Ma, X., Zhu, D., Liu, Y., Peng, F., Wang, Q., Pi, R., 2012. Minocycline up-regulates the expression of brain-derived neurotrophic factor and nerve growth factor in experimental autoimmune encephalomyelitis. Eur. J. Pharmacol. 686, 124-129.
14. Chen, X., Pi, R., Liu, M., Ma, X., Jiang, Y., Liu, Y., Mao, X., Hu, X., 2010. Combination of methylprednisolone and minocycline synergistically improves experimental autoimmune encephalomyelitis in C57 BL/6 mice. J. Neuroimmunol. 226, 104-109.
15. Comerford, I., Litchfield, W., Kara, E., McColl, S.R., 2012. PI3Kc drives priming and survival of autoreactive CD4+ T cells during experimental autoimmune encephalomyelitis. PLoS ONE 7, e45095.
16. Conant, K., McArthur, J.C., Griffin, D.E., Sjulson, L., Wahl, L.M., Irani, D.N., 1999. Cerebrospinal fluid levels of MMP-2, 7, and 9 are elevated in association with human immunodeficiency virus dementia. Ann. Neurol. 46, 391-398.
17. Cuzner, M.L., Gveric, D., Strand, C., Loughlin, A.J., Paemen, L., Opdenakker, G., Newcombe, J., 1996. The expression of tissue-type plasminogen activator, matrix metalloproteases and endogenous inhibitors in the central nervous system in multiple sclerosis: comparison of stages in lesion evolution. J. Neuropathol. Exp. Neurol. 55, 1194-1204.
18. Deak, T., Bellamy, C., D'Agostino, L.G., 2003. Exposure to forced swim stress does not alter central production of IL-1. Brain Res. 972, 53-63.
19. De Vries, H.E., Kuiper, J., De Boer, A.G., Van Berkel, T.J.C., Breimer, D.D., 1997. The blood-brain barrier in neuroinflammatory diseases. Pharmacol. Rev. 49, 143-155.
20. D'Intino, G., Paradisi, M., Fernandez, M., Giuliani, A., Aloe, L., Giardino, L., Calzà, L., 2005. Cognitive deficit associated with cholinergic and nerve growth factor down-regulation in experimental allergic encephalomyelitis in rats. Proc. Natl. Acad. Sci. U. S. A. 102, 3070-3075.
21. Dong, M., Liu, R., Guo, L., Li, C., Tan, G., 2008. Pathological findings in rats with experimental allergic encephalomyelitis. APMIS 116, 972-984.
22. El Behi, M., Dubucquoi, S., Lefranc, D., Zéphir, H., De Seze, J., Vermersch, P., Prin, L., 2005. New insights into cell responses involved in experimental autoimmune encephalomyelitis and multiple sclerosis. Immunol. Lett. 96, 11-26.
23. Feinstein, D.L., Galea, E., Gavrilyuk, V., Brosnan, C.F., Whitacre, C.C., Dumitrescu-Ozimek, L., Landreth, G.E., Pershadsingh, H.A., Weinberg, G., Heneka, M.T., 2002. Peroxisome proliferator-activated receptor-gamma agonists prevent experimental autoimmune encephalomyelitis. Ann. Neurol. 51, 694-702.
24. Gambi, F., Reale, M., Iarlori, C., Salone, A., Toma, L., Paladini, C., De Luca, G., Feliciani, C., Salvatore, M., Salerno, R.M., Theoharides, T.C., Conti, P., Exton, M., Gambi, D., 2004. Alzheimer patients treated with an AchE inhibitor show higher IL-4 and lower IL-1 beta levels and expression in peripheral blood mononuclear cells. J. Clin. Psychopharmacol. 24, 314-321.
25. Geurts, J.J.G., Barkhof, F., 2008. Grey matter pathology in multiple sclerosis. Lancet Neurol. 7, 841-851.
26. Hartung, H.P., Kieseier, B.C., 2000. The role of matrix metalloproteinases in autoimmune damage to the central and peripheral nervous system. J. Neuroimmunol. 107, 140-147.
27. Hartung, H.P., Rieckmann, P., 1997. Pathogenesis of immune-mediated demyelination in the CNS. J. Neural Transm. Suppl. 50, 173-181.
28. Haylock-Jacobs, S., Comerford, I., Bunting, M., Kara, E., Townley, S., Klingler-Hoffmann, M., Vanhaesebroeck, B., Puri, K.D., McColl, S.R., 2011. PI3Kd drives the pathogenesis of experimental autoimmune encephalomyelitis by inhibiting effector T cell apoptosis and promoting Th17 differentiation. J. Autoimmun. 36, 278-287.
29. Hobom, M., Storch, M.K., Weissert, R., Maier, K., Radhakrishnan, A., Kramer, B., Bähr, M., Diem, R., 2004. Mechanisms and time course of neuronal degeneration in experimental autoimmune encephalomyelitis. Brain Pathol. 14, 148-157.
30. Hofstetter, H.H., Sewell, D.L., Liu, F., Sandor, M., Forsthuber, T., Lehmann, P.V., Fabry, Z., 2003. Autoreactive T cells promote post-traumatic healing in the central nervous system. J. Neuroimmunol. 134, 25-34.
31. Hwang, J., Hwang, H., Lee, H.W., Suk, K., 2010. Microglia signaling as a target of donepezil. Neuropharmacology 58, 1122-1129.
32. Issazadeh, S., Mustafa, M., Ljungdahl, A., Hojeberg, B., Dagerlind, A., Elde, R., Olsson, T., 1995. Interferon gamma, interleukin 4 and transforming growth factor beta in experimental autoimmune encephalomyelitis in Lewis rats: dynamics of cellular mRNA expression in the central nervous system and lymphoid cells. J. Neurosci. Res. 40, 579-590.
33. Issazadeh, S., Lorentzen, J.C., Mustafa, M.I., Hojeberg, B., Mussener, A., Olsson, T., 1996. Cytokines in relapsing experimental autoimmune encephalomyelitis in DA rats: persistent mRNA expression of proinflammatory cytokines and absent expression of interleukin-10 and transforming growth factor-beta. J. Neuroimmunol. 69, 103-115.
34. Janowsky, D.S., Davis, J.M., Overstreet, D.H., 2005. Anticholinesterase (DFP) toxicity antagonism by chronic donepezil: a potential nerve agent treatment. Pharmacol. Biochem. Behav. 81, 917-922.
35. Kassiotis, G., Kranidioti, K., Kollias, G., 2001. Defective CD4 T cell priming and resistance to experimental autoimmune encephalomyelitis in TNF-deficient mice due to innate immune hypo-responsiveness. J. Neuroimmunol. 119, 239-247.
36. Kaya, D., Gursoy-Ozdemir, Y., Yemisci, M., Tuncer, N., Aktan, S., Dalkara, T., 2005. VEGF protects brain against focal ischemia without increasing blood-brain permeability when administered intracerebroventricularly. J. Cereb. Blood Flow Metab. 25, 1111-1118.
37. Keegan, B.M., Noseworthy, J.H., 2002. Multiple sclerosis. Annu. Rev. Med. 53, 285-302.
38. Kerschensteiner, M., Stadelmann, C., Dechant, G., Wekerle, H., Hohlfeld, R., 2003. Neurotrophic cross-talk between the nervous and immune systems: implications for neurological diseases. Ann. Neurol. 53, 292-304.
39. Kerschensteiner, M., Meinl, E., Hohlfeld, R., 2009. Neuro-immune crosstalk in CNS diseases. Neuroscience 158, 1122-1132.
40. Krupp, L.B., Christodoulou, C., Melville, P., Scherl, W.F., Pai, L.Y., Muenz, L.R., He, D., Benedict, R.H., Goodman, A., Rizvi, S., Schwid, S.R., Weinstock-Guttman, B., Westervelt, H.J., Wishart, H., 2011. Multicenter randomized clinical trial of donepezil for memory impairment in multiple sclerosis. Neurology 76, 1500-1507.
41. Kuerten, S., Kostova-Bales, D.A., Frenzel, L.P., Tigno, J.T., Tary-Lehmann, M., Angelov, D.N., Lehmann, P.V., 2007. MP4-and MOG: 35-55-induced EAE in C57BL/6 mice differentially targets brain, spinal cord and cerebellum. J. Neuroimmunol. 189, 31-40.
42. Ma, X., Jiang, Y., Wu, A., Chen, X., Pi, R., Liu, M., Liu, Y., 2010. Berberine attenuates experimental autoimmune encephalomyelitis in C57 BL/6 mice. PloS One 5, e13489.
43. Matrisian, L.M., 1990. Metalloproteinases and their inhibitors in matrix remodeling. Trends Genet. 6, 121-125.
44. McGeachy, M.J., Anderton, S.M., 2005. Cytokines in the induction and resolution of experimental autoimmune encephalomyelitis. Cytokine 32, 81-84.
45. Mun-Bryce, S., Rosenberg, G.A., 1998. Gelatinase B modulates selective opening of the blood-brain barrier during inflammation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 274, 1203-1211.
46. Nizri, E., Irony-Tur-Sinai, M., Faranesh, N., Lavon, I., Lavi, E., Weinstock, M., Brenner, T., 2008. Suppression of neuroinflammation and immunomodulation by the acetylcholinesterase inhibitor rivastigmine. J. Neuroimmunol. 203, 12-22.
47. Noseworthy, J.H., Lucchinetti, C., Rodriguez, M., Weinshenker, B.G., 2000. Multiple sclerosis. N. Engl. J. Med. 343, 938-952.
48. Nykjaer, A., Lee, R., Teng, K.K., Jansen, P., Madsen, P., Nielsen, M.S., Jacobsen, C., Kliemannel, M., Schwarz, E., Willnow, T.E., Hempstead, B.L., Petersen, C.M., 2004. Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843-848.
49. O'Neill, E.J., Day, M.J., Wraith, D.C., 2006. IL-10 is essential for disease protection following intranasal peptide administration in the C57BL/6 model of EAE. J. Neuroimmunol. 178, 1-8.
50. Oreja-Guevara, C., Ramos-Cejudo, J., Stark Aroeira, L., 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.
51. Pachner, A.R., 2011. Experimental models of multiple sclerosis. Curr. Opin. Neurol. 24, 291-299.
52. Racke, M.K., Quigley, L., Cannella, B., Raine, C.S., McFarlin, D.E., Scott, D.E., 1994. Superantigen modulation of experimental allergic encephalomyelitis: activation of energy determines outcome. J. Immunol. 152, 2051-2059.
53. Reale, M., Iarlori, C., Gambi, F., Feliciani, C., Isabella, L., Gambi, D., 2006. The acetylcholinesterase inhibitor, Donepezil, regulates a Th2 bias in Alzheimer's disease patients. Neuropharmacology 50, 606-613.
54. Renno, T., Taupin, V., Bourbonniere, L., Verge, G., Tran, E., De Simone, R., 1998. Interferon-gamma in progression to chronic demyelination and neurological deficit following acute EAE. Mol. Cell. Neurosci. 12, 376-389.
55. Scali, C., Casamenti, F., Bellucci, A., Costagli, C., Schmidt, B., Pepeu, G., 2002. Effect of subchronic administration of metrifonate, rivastigmine and donepezil on brain acetylcholine in aged F344 rats. J. Neural Transm. 109, 1067-1080.
56. Schmidt, S., Moric, E., Schmidt, M., Sastre, M., Feinstein, D.L., Heneka, M.T., 2004. Anti-inflammatory and antiproliferative actions of PPAR-gamma agonists on T lymphocytes derived from MS patients. J. Leukoc. Biol. 75, 478-485.
57. Stromnes, I.M., Goverman, J.M., 2006. Active induction of experimentalallergic encephalomyelitis. Nat. Protoc. 1, 1810-1819.
58. Takatori, Y.T., Kume, T., Sugimoto, M., Katsuki, H., Sugimoto, H., Akaike, A., 2006. Acetylcholinesterase inhibitors used in treatment of Alzheimer's disease prevent glutamate neurotoxicity via nicotinic acetylcholine receptors and phosphatidylinositol 3-kinase cascade. Neuropharmacology 51, 474-486.
59. Tsiperson, V., Gruber, R.C., Goldberg, M.F., Jordan, A., Weinger, J.G., Macian, F., Shafit-Zagardo, B., 2013. Suppression of inflammatory responses during myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis is regulated by AKT3 signaling. J. Immunol. 190, 1528-1539.
60. Tyagi, E., Agrawal, R., Nath, C., Shukla, R., 2010. Cholinergic protection via alpha7 nicotinic acetylcholine receptors and PI3K-Akt pathway in LPS-induced neuroinflammation. Neurochem. Int. 56, 135-142.
61. Villoslada, P., Hauser, S.L., Bartke, I., Unger, J., Heald, N., Rosenberg, D., Cheung, S.W., Mobley, W.C., Fisher, S., Genain, C.P., 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.
62. Wiebenga, O.T., Hulst, H.E., Kooi, E.J., Killestein, J., Geurts, J.J., Heilman, K.M., Williamson, J.B., Krupp, L.B., Christodoulou, C., Benedict, R.H., 2011. Multicenter randomized clinical trial of donepezil for memory impairment in multiple sclerosis. Neurology 77, 1998-2000.
63. Xiao, B.G., Wu, X.C., Yang, J.S., Xu, L.Y., Liu, X., Huang, Y.M., Bjelke, B., Link, H., 2004. Therapeutic potential of IFN-gamma-modified dendritic cells in acute and chronic experimental allergic encephalomyelitis. Int. Immunol. 16, 13-22.
64. Yin, L.L., Lin, L.L., Zhang, L., Li, L., 2012. Epimedium flavonoids ameliorate experimental autoimmune encephalomyelitis in rats by modulating neuroinflammatory and neurotrophic responses. Neuropharmacology 63, 851-862.
65. Yong, V.W., Power, C., Forsyth, P., Edwards, D.R., 2001. Metalloproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci. 2, 502-511.
66. Yoshiyama, Y., Kojima, A., Ishikawa, C., Arai, K., 2010. Anti-inflammatory action of donepezil ameliorates tau pathology, synaptic loss, and neurodegeneration in a tauopathy mouse model. J. Alzheimers Dis. 22, 295-306.
67. Zappia, E., Casazza, S., Pedemonte, E., Benvenuto, F., Bonanni, I., Gerdoni, E., Giunti, D., Ceravolo, A., Cazzanti, F., Frassoni, F., Mancardi, G., Uccelli, A., 2005. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106, 1755-1761.
68. Zhang, J., Brodie, C., Li, Y., Zheng, X., Roberts, C., Lu, M., Gao, Q., Borneman, J., Savant-Bhonsale, S., Elias, S.B., Chopp, M., 2009. Bone marrow stromal cell therapy reduces proNGF and p75 expression in mice with experimental autoimmune encephalomyelitis. J. Neurol. Sci. 279, 30-38.
69. Zhou, X., Patel, A.R., Perez, F., Jurivich, D.A., 2009. Acteylcholinesterase inhibitor rivastigmine enhances cellular defenses in neuronal and macrophage-like cell lines. Transl. Res. 153, 132-141.