Inhibition of glycogen synthase kinase-3β by Angelica sinensis extract decreases β-amyloid-induced neurotoxicity and tau phosphorylation in cultured cortical neurons

Journal of Neuroscience Research

Volumn 89, Issue 3, 2011, Pages 437-447

  Zhang, Zhaoxu ^a   Zhao, Ruiping ^a   Qi, Jiping ^a   Wen, Shirong ^a   Tang, Ying ^a   Wang, Desheng ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Akt; Alzheimer's disease; Amyloid; Glycogen synthase; Tau proteins

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AMYLOID BETA PROTEIN[1-42]; ANGELICA SINENSIS EXTRACT; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TAU PROTEIN;

ALZHEIMER DISEASE; ANGELICA SINENSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CELL; CELL CULTURE; CELL VIABILITY; CHINESE MEDICINE; CONTROLLED STUDY; DOSE RESPONSE; DRUG INHIBITION; ENZYME PHOSPHORYLATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; WESTERN BLOTTING;

AMYLOID BETA-PEPTIDES; ANALYSIS OF VARIANCE; ANGELICA SINENSIS; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BENZIMIDAZOLES; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; LITHIUM CHLORIDE; NEURONS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PLANT PREPARATIONS; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; TAU PROTEINS;

EID: 78751700479     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22563     Document Type: Article

References (55)

1. Alvarez G, Munoz-Montano JR, Satrustegui J, Avila J, Bogonez E, Diaz-Nido J. 2002. Regulation of tau phosphorylation and protection against beta-amyloid-induced neurodegeneration by lithium. Possible implications for Alzheimer's disease. Bipolar Disord 4: 153-165.
2. Baki L, Shioi J, Wen P, Shao Z, Schwarzman A, et al. 2004. PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: effects of FAD mutations. EMBO J 23: 2586-2596.
3. Bertrand J, Plouffe V, Senechal P, Leclerc N. 2010. The pattern of human tau phosphorylation is the result of priming and feedback events in primary hippocampal neurons. Neuroscience 168: 323-334.
4. Busciglio J, Lorenzo A, Yeh J, Yankner BA. 1995. Beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14: 879-888.
5. Cardona-Gomez GP, Mendez P, Garcia-Segura LM. 2002. Synergistic interaction of estradiol and insulin-like growth factor-I in the activation of PI3K/Akt signaling in the adult rat hypothalamus. Brain Res Mol Brain Res 107: 80-88.
6. Cardona-Gomez P, Perez M, Avila J, Garcia-Segura LM, Wandosell F. 2004. Estradiol inhibits GSK3 and regulates interaction of estrogen receptors, GSK3, and beta-catenin in the hippocampus. Mol Cell Neurosci 25: 363-373.
7. Chao WW, Hong YH, Chen ML, Lin BF. 2010. Inhibitory effects of Angelica sinensis ethyl acetate extract and major compounds on NF-kappaB trans-activation activity and LPS-induced inflammation. J Ethnopharmacol 129: 244-249.
8. Du K, Montminy M. 1998. CREB is a regulatory target for the protein kinase Akt/PKB. J Biol Chem 273: 32377-32379.
9. Elyaman W, Terro F, Wong NS, Hugon J. 2002. In vivo activation and nuclear translocation of phosphorylated glycogen synthase kinase-3beta in neuronal apoptosis: links to tau phosphorylation. Eur J Neurosci 15: 651-660.
10. Ferrer I, Gomez-Isla T, Puig B, Freixes M, Ribe E, et al. 2005. Current advances on different kinases involved in tau phosphorylation, and implications in Alzheimer's disease and tauopathies. Curr Alzheimer Res 2: 3-18.
11. Goedert M. 1998. Neurofibrillary pathology of Alzheimer's disease and other tauopathies. Prog Brain Res 117: 287-306.
12. Grimes CA, Jope RS. 2001. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol 65: 391-426.
13. Hamaguchi T, Ono K, Murase A, Yamada M. 2009. Phenolic compounds prevent Alzheimer's pathology through different effects on the amyloid-beta aggregation pathway. Am J Pathol 175: 2557-2565.
14. Hong M, Chen DC, Klein PS, Lee VM. 1997. Lithium reduces tau phosphorylation by inhibition of glycogen synthase kinase-3. J Biol Chem 272: 25326-25332.
15. Hsiao YH, Chen PS, Yeh SH, Lin CH, Gean PW. 2008. N-acetylcysteine prevents beta-amyloid toxicity by a stimulatory effect on p35/cyclin-dependent kinase 5 activity in cultured cortical neurons. J Neurosci Res 86: 2685-2695.
16. Huang SH, Lin CM, Chiang BH. 2008. Protective effects of Angelica sinensis extract on amyloid beta-peptide-induced neurotoxicity. Phytomedicine 15: 710-721.
17. Hui MK, Wu WK, Shin VY, So WH, Cho CH. 2006. Polysaccharides from the root of Angelica sinensis protect bone marrow and gastrointestinal tissues against the cytotoxicity of cyclophosphamide in mice. Int J Med Sci 3: 1-6.
18. Ji L, Mochon E, Arcinas M, Boxer LM. 1996. CREB proteins function as positive regulators of the translocated bcl-2 allele in t(14;18) lymphomas. J Biol Chem 271: 22687-22691.
19. Johansson S, Jamsa A, Vasange M, Winblad B, Luthman J, Cowburn RF. 2006. Increased tau phosphorylation at the Ser396 epitope after amyloid beta-exposure in organotypic cultures. Neuroreport 17: 907-911.
20. Jope RS, Johnson GV. 2004. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 29: 95-102.
21. Kang SY, Lee KY, Koo KA, Yoon JS, Lim SW, et al. 2005. ESP-102, a standardized combined extract of Angelica gigas, Saururus chinensis and Schizandra chinensis, significantly improved scopolamine-induced memory impairment in mice. Life Sci 76: 1691-1705.
22. Kang UG, Seo MS, Roh MS, Kim Y, Yoon SC, Kim YS. 2004. The effects of clozapine on the GSK-3-mediated signaling pathway. FEBS Lett 560: 115-119.
23. Kim DW, Lee JH, Park SK, Yang WM, Jeon GS, et al. 2007. Astrocytic expressions of phosphorylated Akt, GSK3beta and CREB following an excitotoxic lesion in the mouse hippocampus. Neurochem Res 32: 1460-1468.
24. Koh SH, Noh MY, Kim SH. 2008. Amyloid-beta-induced neurotoxicity is reduced by inhibition of glycogen synthase kinase-3. Brain Res 1188: 254-262.
25. Lee CW, Lau KF, Miller CC, Shaw PC. 2003a. Glycogen synthase kinase-3 beta-mediated tau phosphorylation in cultured cell lines. Neuroreport 14: 257-260.
26. Lee KY, Koh SH, Noh MY, Kim SH, Lee YJ. 2008. Phosphatidylinositol-3-kinase activation blocks amyloid beta-induced neurotoxicity. Toxicology 243: 43-50.
27. Lee MS, Kao SC, Lemere CA, Xia W, Tseng HC, et al. 2003b. APP processing is regulated by cytoplasmic phosphorylation. J Cell Biol 163: 83-95.
28. Lee VM, Goedert M, Trojanowski JQ. 2001. Neurodegenerative tauopathies. Annu Rev Neurosci 24: 1121-1159.
29. Lesort M, Jope RS, Johnson GV. 1999. Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3beta and Fyn tyrosine kinase. J Neurochem 72: 576-584.
30. Li X, Lu F, Tian Q, Yang Y, Wang Q, Wang JZ. 2006. Activation of glycogen synthase kinase-3 induces Alzheimer-like tau hyperphosphorylation in rat hippocampus slices in culture. J Neural Transm 113: 93-102.
31. Lu GH, Chan K, Leung K, Chan CL, Zhao ZZ, Jiang ZH. 2005. Assay of free ferulic acid and total ferulic acid for quality assessment of Angelica sinensis. J Chromatogr A 1068: 209-219.
32. Lucas JJ, Hernandez F, Gomez-Ramos P, Moran MA, Hen R, Avila J. 2001. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J 20: 27-39.
33. Mai L, Jope RS, Li X. 2002. BDNF-mediated signal transduction is modulated by GSK3beta and mood stabilizing agents. J Neurochem 82: 75-83.
34. Mohmmad Abdul H, Butterfield DA. 2005. Protection against amyloid beta-peptide (1-42)-induced loss of phospholipid asymmetry in synaptosomal membranes by tricyclodecan-9-xanthogenate (D609) and ferulic acid ethyl ester: implications for Alzheimer's disease. Biochim Biophys Acta 1741: 140-148.
35. Moule SK, Welsh GI, Edgell NJ, Foulstone EJ, Proud CG, Denton RM. 1997. Regulation of protein kinase B and glycogen synthase kinase-3 by insulin and beta-adrenergic agonists in rat epididymal fat cells. Activation of protein kinase B by wortmannin-sensitive and -insensitive mechanisms. J Biol Chem 272: 7713-7719.
36. Noble W, Planel E, Zehr C, Olm V, Meyerson J, et al. 2005. Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc Natl Acad Sci U S A 102: 6990-6995.
37. Noh MY, Koh SH, Kim Y, Kim HY, Cho GW, Kim SH. 2009. Neuroprotective effects of donepezil through inhibition of GSK-3 activity in amyloid-beta-induced neuronal cell death. J Neurochem 108: 1116-1125.
38. Pap M, Cooper GM. 1998. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 273: 19929-19932.
39. Plattner F, Angelo M, Giese KP. 2006. The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J Biol Chem 281: 25457-25465.
40. Reynolds CH, Betts JC, Blackstock WP, Nebreda AR, Anderton BH. 2000. Phosphorylation sites on tau identified by nanoelectrospray mass spectrometry: differences in vitro between the mitogen-activated protein kinases ERK2, c-Jun N-terminal kinase and P38, and glycogen synthase kinase-3beta. J Neurochem 74: 1587-1595.
41. Salas TR, Reddy SA, Clifford JL, Davis RJ, Kikuchi A, et al. 2003. Alleviating the suppression of glycogen synthase kinase-3beta by Akt leads to the phosphorylation of cAMP-response element-binding protein and its transactivation in intact cell nuclei. J Biol Chem 278: 41338-41346.
42. Salkovic-Petrisic M, Tribl F, Schmidt M, Hoyer S, Riederer P. 2006. Alzheimer-like changes in protein kinase B and glycogen synthase kinase-3 in rat frontal cortex and hippocampus after damage to the insulin signalling pathway. J Neurochem 96: 1005-1015.
43. Shi HR, Zhu LQ, Wang SH, Liu XA, Tian Q, et al. 2008. 17Beta-estradiol attenuates glycogen synthase kinase-3beta activation and tau hyperphosphorylation in Akt-independent manner. J Neural Transm 115: 879-888.
44. Song MS, Rauw G, Baker GB, Kar S. 2008. Memantine protects rat cortical cultured neurons against beta-amyloid-induced toxicity by attenuating tau phosphorylation. Eur J Neurosci 28: 1989-2002.
45. Sperber BR, Leight S, Goedert M, Lee VM. 1995. Glycogen synthase kinase-3 beta phosphorylates tau protein at multiple sites in intact cells. Neurosci Lett 197: 149-153.
46. Sul D, Kim HS, Lee D, Joo SS, Hwang KW, Park SY. 2009. Protective effect of caffeic acid against beta-amyloid-induced neurotoxicity by the inhibition of calcium influx and tau phosphorylation. Life Sci 84: 257-262.
47. Takashima A, Noguchi K, Michel G, Mercken M, Hoshi M, et al. 1996. Exposure of rat hippocampal neurons to amyloid beta peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3 beta. Neurosci Lett 203: 33-36.
48. Tran NL, Adams DG, Vaillancourt RR, Heimark RL. 2002. Signal transduction from N-cadherin increases Bcl-2. Regulation of the phosphatidylinositol 3-kinase/Akt pathway by homophilic adhesion and actin cytoskeletal organization. J Biol Chem 277: 32905-32914.
49. Tsai NM, Lin SZ, Lee CC, Chen SP, Su HC, et al. 2005. The antitumor effects of Angelica sinensis on malignant brain tumors in vitro and in vivo. Clin Cancer Res 11: 3475-3484.
50. Wang H, Li W, Li J, Rendon-Mitchell B, Ochani M, et al. 2006. The aqueous extract of a popular herbal nutrient supplement, Angelica sinensis, protects mice against lethal endotoxemia and sepsis. J Nutr 136: 360-365.
51. Yan JJ, Kim DH, Moon YS, Jung JS, Ahn EM, et al. 2004. Protection against beta-amyloid peptide-induced memory impairment with long-term administration of extract of Angelica gigas or decursinol in mice. Prog Neuropsychopharmacol Biol Psychiatry 28: 25-30.
52. Yap AS, Kovacs EM. 2003. Direct cadherin-activated cell signaling: a view from the plasma membrane. J Cell Biol 160: 11-16.
53. Ye YN, Liu ES, Li Y, So HL, Cho CC, et al. 2001. Protective effect of polysaccharides-enriched fraction from Angelica sinensis on hepatic injury. Life Sci 69: 637-646.
54. Zhao J, Wang D, Duan S, Wang J, Bai J, Li W. 2009. Analysis of fuzhisan and quantitation of baicalin and ginsenoside Rb(1) by HPLC-DAD-ELSD. Arch Pharm Res 32: 989-996.
55. Zheng WH, Bastianetto S, Mennicken F, Ma W, Kar S. 2002. Amyloid beta peptide induces tau phosphorylation and loss of cholinergic neurons in rat primary septal cultures. Neuroscience 115: 201-211.