The Journal of Nutritional Biochemistry
Volume 22, Issue 5 , Pages 476-486 , May 2011

4-O-methylhonokiol attenuated β-amyloid-induced memory impairment through reduction of oxidative damages via inactivation of p38 MAP kinase

  • Yong Kyung Lee

      Affiliations

    • College of Pharmacy and MRC, Chungbuk National University, Heungduk-gu, Cheongju, Chungbuk 361-763, South Korea
    • ,
  • Im Seop Choi

      Affiliations

    • College of Pharmacy and MRC, Chungbuk National University, Heungduk-gu, Cheongju, Chungbuk 361-763, South Korea
    • ,
  • Jung Ok Ban

      Affiliations

    • College of Pharmacy and MRC, Chungbuk National University, Heungduk-gu, Cheongju, Chungbuk 361-763, South Korea
    • ,
  • Hwa Jeong Lee

      Affiliations

    • College of Pharmacy and MRC, Chungbuk National University, Heungduk-gu, Cheongju, Chungbuk 361-763, South Korea
    • ,
  • Ung Soo Lee

      Affiliations

    • Department of Food and Biotechnology, Chungju National University, Iryu-myeon, Chungju, Chungbuk 380-702, South Korea
    • ,
  • Sang Bae Han

      Affiliations

    • College of Pharmacy and MRC, Chungbuk National University, Heungduk-gu, Cheongju, Chungbuk 361-763, South Korea
    • ,
  • Jae Kyung Jung

      Affiliations

    • College of Pharmacy and MRC, Chungbuk National University, Heungduk-gu, Cheongju, Chungbuk 361-763, South Korea
    • ,
  • Young Hee Kim

      Affiliations

    • R&D Center, Bioland Ltd., Songjeong, Byongchon, Cheonan-Si, Chungnam 330-863, South Korea
    • ,
  • Ki Ho Kim

      Affiliations

    • R&D Center, Bioland Ltd., Songjeong, Byongchon, Cheonan-Si, Chungnam 330-863, South Korea
    • ,
  • Ki-Wan Oh

      Affiliations

    • College of Pharmacy and MRC, Chungbuk National University, Heungduk-gu, Cheongju, Chungbuk 361-763, South Korea
    • ,
  • Jin Tae Hong

      Affiliations

    • College of Pharmacy and MRC, Chungbuk National University, Heungduk-gu, Cheongju, Chungbuk 361-763, South Korea
    • Corresponding Author InformationCorresponding author. College of Pharmacy, Chungbuk National University, Heungduk-gu, Cheongju, Chungbuk 361-763, South Korea. Tel.: +82 43 261 2813; fax: +82 43 268 2732.

Received 24 October 2009 ,Revised 4 April 2010 ,Accepted 5 April 2010.

References 

  1. Weiner HL, Lemere CA, Maron R, Spooner ET, Grenfell TJ, Mori C, et al. Nasal administration of amyloid-beta peptide decreases cerebral amyloid burden in a mouse model of Alzheimer's disease. Ann Neurol. 2000;48(4):567–579
  2. Joachim CL, Selkoe DJ. The seminal role of beta-amyloid in the pathogenesis of Alzheimer disease. Alzheimer Dis Assoc Disord. 1992;6(1):7–34
  3. Cerpa W, Dinamarca MC, Inestrosa NC. Structure-function implications in Alzheimer's disease: effect of Abeta oligomers at central synapses. Curr Alzheimer Res. 2008;5(3):233–243
  4. Selkoe DJ. Presenilin, Notch, and the genesis and treatment of Alzheimer's disease. Proc Natl Acad Sci U S A. 2001;98(20):11039–11041
  5. Maccioni M, Riera CM, Rivero VE. Identification of rat prostatic steroid binding protein (PSBP) as an immunosuppressive factor. J Reprod Immunol. 2001;50(2):133–149
  6. Lecanu L, Yao W, Teper GL, Yao ZX, Greeson J, Papadopoulos V. Identification of naturally occurring spirostenols preventing beta-amyloid-induced neurotoxicity. Steroids. 2004;69(1):1–16
  7. Hwang DY, Chae KR, Kang TS, Hwang JH, Lim CH, Kang HK, et al. Alterations in behavior, amyloid beta-42, caspase-3, and Cox-2 in mutant PS2 transgenic mouse model of Alzheimer's disease. FASEB J. 2002;16:805–813
  8. Lee SY, Hwang DY, Kim YK, Lee JW, Shin IC, Oh KW, et al. PS2 mutation increases neuronal cell vulnerability to neurotoxicants through activation of caspase-3 by enhancing of ryanodine receptor-mediated calcium release. FASEB J. 2006;20:151–153
  9. Feld M, Galli C, Piccini A, Romano A. Effect on memory of acute administration of naturally secreted fibrils and synthetic amyloid-beta peptides in an invertebrate model. Neurobiol Learn Mem. 2008;89(4):407–418
  10. Repici M, Zanjani HS, Gautheron V, Borsello T, Dusart I, Mariani J. Specific JNK inhibition by D-JNKI1 protects Purkinje cells from cell death in Lurcher mutant mouse. Cerebellum. 2008;7(4):534–538
  11. Chen HS, He X, Qu F, Kang SM, Yu Y, Liao D, et al. Differential roles of peripheral mitogen-activated protein kinase signal transduction pathways in bee venom-induced nociception and inflammation in conscious rats. J Pain. 2009;10(2):201–207
  12. Munoz L, Ranaivo HR, Roy SM, Hu W, Craft JM, McNamara LK, et al. A novel p38 alpha MAPK inhibitor suppresses brain proinflammatory cytokine up-regulation and attenuates synaptic dysfunction and behavioral deficits in an Alzheimer's disease mouse model. J Neuroinflammation. 2007;4:21
  13. Zhu Y, Hou H, Nikolic WV, Ehrhart J, Rrapo E, Bickford P, et al. CD45RB is a novel molecular therapeutic target to inhibit Abeta peptide-induced microglial MAPK activation. PLoS One. 2008;3(5):e2135
  14. Origlia N, Righi M, Capsoni S, Cattaneo A, Fang F, Stern DM, et al. Receptor for advanced glycation end product-dependent activation of p38 mitogen-activated protein kinase contributes to amyloid-beta-mediated cortical synaptic dysfunction. J Neurosci. 2008 Mar 26;28(13):3521–3530
  15. Song YS, Park HJ, Kim SY, Lee SH, Yoo HS, Lee HS, et al. Protective role of Bcl-2 on beta-amyloid-induced cell death of differentiated PC12 cells: reduction of NF-kappaB and p38 MAP kinase activation. Neurosci Res. 2004;49(1):69–80
  16. Lee JW, Lee YK, Ban JO, Ha TY, Yun YP, Han SB, et al. Green tea (−)-epigallocatechin-3-gallate inhibits beta-amyloid-induced cognitive dysfunction through modification of secretase activity via inhibition of ERK and NF-kappaB pathways in mice. J Nutr. 2009;139(10):1987–1993
  17. Lee SY, Lee JW, Lee HS, Yoo HS, Yun YP, Oh KW, et al. Inhibitory effect of green tea extract on β-amyloid-induced PC12 cell death by inhibition of the activation of NF-κB and ERK/p38 MAP kinase pathway through antioxidant mechanisms. Mol Brain Res. 2005;140:45–54
  18. Butterfield DA. Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review. Free Radic Res. 2002;36(12):1307–1313
  19. Jang JH, Surh YJ. beta-Amyloid induces oxidative DNA damage and cell death through activation of c-Jun N terminal kinase. Ann N Y Acad Sci. 2002;973:228–236
  20. Dumont M, Wille E, Stack C, Calingasan NY, Beal MF, Lin MT. Reduction of oxidative stress, amyloid deposition, and memory deficit by manganese superoxide dismutase overexpression in a transgenic mouse model of Alzheimer's disease. FASEB J. 2009;23(8):2459–2466
  21. Montiel T, Camacho A, Estrada-Sánchez AM, Massieu L. Differential effects of the substrate inhibitor l-trans-pyrrolidine-2,4-dicarboxylate (PDC) and the non-substrate inhibitor DL-threo-beta-benzyloxyaspartate (DL-TBOA) of glutamate transporters on neuronal damage and extracellular amino acid levels in rat brain in vivo. Neuroscience. 2005;133(3):667–678
  22. Arias C, Montiel T, Quiroz-Báez R, Massieu L. beta-Amyloid neurotoxicity is exacerbated during glycolysis inhibition and mitochondrial impairment in the rat hippocampus in vivo and in isolated nerve terminals: implications for Alzheimer's disease. Exp Neurol. 2002;176(1):163–174
  23. Yatin SM, Varadarajan S, Butterfield DA. Vitamin E prevents Alzheimer's amyloid beta-peptide (1-42)-induced neuronal protein oxidation and reactive oxygen species production. J Alzheimers Dis. 2000;2(2):123–131
  24. Liou KT, Shen YC, Chen CF, Tsao CM, Tsai SK. Honokiol protects rat brain from focal cerebral ischemia-reperfusion injury by inhibiting neutrophil infiltration and reactive oxygen species production. Brain Res. 2003;992(2):159–166
  25. Lin YR, Chen HH, Ko CH, Chan MH. Neuroprotective activity of honokiol and magnolol in cerebellar granule cell damage. Eur J Pharmacol. 2006;537(1-3):64–69
  26. Frank B, Gupta S. A review of antioxidants and Alzheimer's disease. Ann Clin Psychiatry. 2005;17(4):269–286
  27. Rezai-Zadeh K, Arendash GW, Hou H, Fernandez F, Jensen M, Runfeldt M, et al. Green tea epigallocatechin-3-gallate (EGCG) reduces beta-amyloid mediated cognitive impairment and modulates tau pathology in Alzheimer transgenic mice. Brain Res. 2008;1214:177–187
  28. Kim TI, Lee YK, Park SG, Choi IS, Ban JO, Park HK, et al. l-Theanine, an amino acid in green tea, attenuates beta-amyloid-induced cognitive dysfunction and neurotoxicity: reduction in oxidative damage and inactivation of ERK/p38 kinase and NF-kappaB pathways. Free Radic Biol Med. 2009;47:1601–1610
  29. Kuribara H, Stavinoha WB, Maruyama Y. Behavioural pharmacological characteristics of honokiol, an anxiolytic agent present in extracts of Magnolia bark, evaluated by an elevated plus-maze test in mice. J Pharm Pharmacol. 1998;50(7):819–826
  30. Watanabe K, Watanabe H, Goto Y, Yamaguchi M, Yamamoto N, Hagino K. Pharmacological properties of magnolol and honokiol extracted from Magnolia officinalis: central depressant effects. Planta Med. 1983;49(2):103–108
  31. Zhou HY, Shin EM, Guo LY, Youn UJ, Bae K, Kang SS, et al. Anti-inflammatory activity of 4-methoxyhonokiol is a function of the inhibition of iNOS and COX-2 expression in RAW 264.7 macrophages via NF-kappaB, JNK and p38 MAPK inactivation. Eur J Pharmacol. 2008;586(1-3):340–349
  32. Munroe ME, Arbiser JL, Bishop GA. Honokiol, a natural plant product, inhibits inflammatory signals and alleviates inflammatory arthritis. J Immunol. 2007;179(2):753–763
  33. Lin YR, Chen HH, Ko CH, Chan MH. Effects of honokiol and magnolol on acute and inflammatory pain models in mice. Life Sci. 2007;81(13):1071–1078
  34. Fujita S, Taira J. Biphenyl compounds are hydroxyl radical scavengers: their effective inhibition for UV-induced mutation in Salmonella typhimurium TA102. Free Radic Biol Med. 1994;17(3):273–277
  35. Dikalov S, Losik T, Arbiser JL. Honokiol is a potent scavenger of superoxide and peroxyl radicals. Biochem Pharmacol. 2008;76(5):589–596
  36. Chen CL, Chang PL, Lee SS, Peng FC, Kuo CH, Chang HT. Analysis of magnolol and honokiol in biological fluids by capillary zone electrophoresis. J Chromatogr A. 2007;1142(2):240–244
  37. Oh JH, Kang LL, Ban JO, Kim YH, Kim KH, Han SB, et al. Anti-inflammatory effect of 4-O-MH, a novel compound isolated from Magnolia officinalis through inhibition of NF-kappaB. Chem Biol Interact. 2009;180(3):506–514
  38. Lee YK, Choi IS, Kim YH, Kim KH, Nam SY, Yun YW, et al. Neurite outgrowth effect of 4-O-MH by induction of neurotrophic factors through ERK activation. Neurochem Res. 2009;34:2251–2260
  39. Lee YK, Yuk DY, Kim TI, Kim YH, Kim KT, Kim KH, et al. Protective effect of the ethanol extract of Magnolia officinalis and 4-O-MH on scopolamine-induced memory impairment and the inhibition of acetylcholinesterase activity. Nat Med (Tokyo). 2009;63(3):274–282
  40. Nabeshima T, Nitta A. Memory impairment and neuronal dysfunction induced by beta-amyloid protein in rats. Tohoku J Exp Med. 1994;174(3):241–249
  41. Frautschy SA, Hu W, Kim P, Miller SA, Chu T, Harris-White ME, et al. Phenolic anti-inflammatory antioxidant reversal of Abeta-induced cognitive deficits and neuropathology. Neurobiol Aging. 2001;22(6):993–1005
  42. Morris R. Developments of water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 1984;11:47–60
  43. Gibson GE, Zhang H. Abnormalities in oxidative processes in non-neuronal tissues from patients with Alzheimer's disease. J Alzheimers Dis. 2001;3(3):329–338
  44. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature. 2000;408(6809):239–247
  45. Chiu JH, Ho CT, Wei YH, Lui WY, Hong CY. In vitro and in vivo protective effect of honokiol on rat liver from peroxidative injury. Life Sci. 1997;61(19):1961–1971
  46. Ou HC, Chou FP, Lin TM, Yang CH, Sheu WH. Protective effects of honokiol against oxidized LDL-induced cytotoxicity and adhesion molecule expression in endothelial cells. Chem Biol Interact. 2006;161(1):1–13
  47. Ou HC, Chou FP, Sheu WH, Hsu SL, Lee WJ. Protective effects of magnolol against oxidized LDL-induced apoptosis in endothelial cells. Arch Toxicol. 2007;81(6):421–432
  48. Drouet B, Pinçon-Raymond M, Chambaz J, Pillot T. Molecular basis of Alzheimer's disease. Cell Mol Life Sci. 2000;57(5):705–715
  49. Yankner BA. Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron. 1996;16(5):921–932
  50. Harkany T, Abrahám I, Kónya C, Nyakas C, Zarándi M, Penke B, et al. Mechanisms of beta-amyloid neurotoxicity: perspectives of pharmacotherapy. Rev Neurosci. 2000;11(4):329–382[Review]
  51. Behl C, Davis JB, Lesley R, Schubert D. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell. 1994;77(6):817–827
  52. Yatin SM, Aksenova M, Aksenov M, Markesbery WR, Aulick T, Butterfield DA. Temporal relations among amyloid beta-peptide-induced free-radical oxidative stress, neuronal toxicity, and neuronal defensive responses. J Mol Neurosci. 1998;11(3):183–197
  53. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, Jenkins NA, et al. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron. 1997;19:939–945
  54. Wasilewska-Sampaio AP, Silveira MS, Holub O, Goecking R, Gomes FC, Neto VM, et al. Neuritogenesis and neuronal differentiation promoted by 2,4-dinitrophenol, a novel anti-amyloidogenic compound. FASEB J. 2005;19(12):1627–1636
  55. Marques CA, Keil U, Bonert A, Steiner B, Haass C, Muller WE, et al. Neurotoxic mechanisms caused by the Alzheimer's disease-linked Swedish amyloid precursor protein mutation: oxidative stress, caspases, and the JNK pathway. J Biol Chem. 2003;278(30):28294–28302
  56. Ekinci FJ, Malik KU, Shea TB. Activation of the L voltage-sensitive calcium channel by mitogen-activated protein (MAP) kinase following exposure of neuronal cells to beta-amyloid. MAP kinase mediates beta-amyloid-induced neurodegeneration. J Biol Chem. 1999;274(42):30322–30327
  57. Choi MS, Lee SH, Cho HS, Kim Y, Yun YP, Jung HY, et al. Inhibitory effect of obovatol on nitric oxide production and activation of NF-kappaB/MAP kinases in lipopolysaccharide-treated RAW 264.7cells. Eur J Pharmacol. 2007;556(1-3):181–189
  58. Zhai H, Nakade K, Oda M, Mitsumoto Y, Akagi M, Sakurai J, et al. Honokiol-induced neurite outgrowth promotion depends on activation of extracellular signal-regulated kinases (ERK1/2). Eur J Pharmacol. 2005;516(2):112–117
  59. Tsai TH, Chou CJ, Chen CF. Pharmacokinetics and brain distribution of magnolol in the rat after intravenous bolus injection. J Pharm Pharmacol. 1996;48(1):57–59
  60. Lin YL, Chen HH, Ko CH, Chan MH. Differential inhibitory effect of honokiol and magnolol on excitatory amino acid-evoked cation signals and NMDA-induced seizures. J Neuropharm. 2005;542:550–558
  61. Cui HS, Huang LS, Sok DE, Shin J, Kwon BM, Youn UJ, et al. Protective action of honokiol, administered orally, against oxidative stress in brain of mice challenged with NMDA. (1–100 mg/kg 3days). Phytomedicine. 2007;14(10):696–700
  62. Maruyama Y, Kuribara H, Kishi E, Weintraub ST, Ito Y. Confirmation of the anxiolytic-like effect of dihydrohonokiol following behavioural and biochemical assessments. J Pharm Pharmacol. 2001;53(5):721–725
  63. Liu Z, Zhang X, Cui W, Zhang X, Li N, Chen J, et al. Evaluation of short-term and subchronic toxicity of magnolia bark extract in rats. Regul Toxicol Pharmacol. 2007;49(3):160–171

☆ Grants: This work was supported by the Korea Research Foundation Grant (MRC, 2009-0091433) and by the Research Grant from Bioland (Chungnam, Korea).

PII: S0955-2863(10)00100-2

doi: 10.1016/j.jnutbio.2010.04.002

The Journal of Nutritional Biochemistry
Volume 22, Issue 5 , Pages 476-486 , May 2011

Article Tools

* Image Usage & Resolution