Green tea catechin leads to global improvement among Alzheimer's disease-related phenotypes in NSE/hAPP-C105 Tg mice

Journal of Nutritional Biochemistry

Volumn 24, Issue 7, 2013, Pages 1302-1313

  Lim, Hwa Ja ^a,b   Shim, Sun Bo ^a   Jee, Seung Wan ^a   Lee, Su Hae ^a   Lim, Chul Ju ^a   Hong, Jin Tae ^c   Sheen, Yhun Yong ^a,b   Hwang, Dae Youn ^d  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b Ewha Womans University   (South Korea)

^c Chungbuk National University   (South Korea)

^d Pusan National University   (South Korea)

Author keywords

Secretase; A 42; Catechin; MAPK; Neprilysin; Pin1

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; CATECHIN; GAMMA SECRETASE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MEMBRANE METALLOENDOPEPTIDASE; MITOGEN ACTIVATED PROTEIN KINASE; PEPTIDYLPROLYL ISOMERASE PIN1; WNT PROTEIN; AMYLOID PRECURSOR PROTEIN; ENOLASE; SECRETASE; TEA;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; ENZYME ACTIVITY; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; TEA; TRANSGENIC MOUSE; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PATHOPHYSIOLOGY;

MUS; MUS MUSCULUS;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CATECHIN; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; PHOSPHOPYRUVATE HYDRATASE; TEA;

EID: 84879319405     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.10.005     Document Type: Article

References (77)

1. Vassar R., Bennetm B.D., Babu-Khan S., Khan S., Mendiaz E.A., Denis P., et al. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 1999, 286:735-741.
2. Xia W., Ray W.J., Ostaszewski B.L., Rahmati T., Kimberly W.T., Wolfe M.S., et al. Presenilin complexes with the C-terminal fragments of amyloid precursor protein at the sites of amyloid beta-protein generation. Proc Natl Acad Sci USA 2000, 1:9299-9304.
3. Andrau D., Dumanchin-Njock C., Ayral E., Vizzavona J., Farzan H., Boisbrun M., et al. BACE1- and BACE2-expressing human cells characterization of β-amyloid precursor protein-derived catabolites, design of a novel fluorimetric assay, and identification of new in vitro inhibitor. J Biol Chem 2003, 278:25859-25866.
4. Lee E.B., Skovronsky D.M., Abtahian F., Doms R.W., Lee V.M. Secretion and intracellular generation of truncated Aβ in BACE expressing human neurons. J Biol Chem 2002, 278:4458-4466.
5. Kimberly W.T., LaVoie M.J., Ostaszewiski B.L., Ye W., Wolfe M.S., Selkoe D.J. γ-Secretase is a membrane protein complex composed of presenilin, nicastrin, Aph-1, and Pen-2. Proc Natl Acad Sci USA 2003, 100:6382-6387.
6. Lim H.J., Cho J.S., Oh J.H., Shim S.B., Hwang D.Y., Jee S.W., et al. NSE-controlled carboxyl-terminus of APP gene over-expressing in Tg mice induces altered expressions in behavior, Aβ-42, and GSK3β binding proteins. Cell Mol Neurobiol 2005, 25:833-850.
7. Weinreb O.D., Mandal S., Amit T., Youdim M.B. Neurological mechanisms of green tea polyphenols in Alzheimer's and Parkins disease. J Nutr Biochem 2004, 15:506-516.
8. Van de Craen M., de Jonghe C., van den Brande I., Declercq W., van Gassen G., van Criekinge W., et al. Identification of caspases that cleave presenilin-1 and presenilin-2. Five presenilin-1 (PS1) mutations do not alter the sensitivity of PS1 to caspases. FEBS Lett 1999, 445:149-154.
9. Choi Y.T., Jung C.H., Lee S.R., Bae J.H., Back W.K., Suh M.H., et al. The green tea polyphenol (-)-epigallocatechin gallate attenuates β-amyloid-induced neurotoxicity in cultured hippocampal neurons. Life Sci 2001, 70:603-614.
10. Bastianetto S., Yao Z.X., Papadopoulos Y., Quirion R. Neuroprotective effects of green and black teas and their catechin gallate ester against beta-amyloid-induced toxicity. Eur J Neurosci 2006, 23:55-64.
11. Rezai-Zadeh K., Shytle D., Sun N., Mori T., Hou H., Jeanniton D., et al. Green tea epigallocatechin-3-gallate (EGCG) modulates amyloid precursor protein cleavage and reduces cerebral amyloidosis in Alzheimer transgenic mice. J Neurobiol 2005, 25:8807-8817.
12. Ikeda I., Kobayashi M., Hamada T., Tsuda K., Goto H., Imaizumi K., et al. Heat-epimerized tea catechins rich in gallocatechin gallate and catechin gallate are more effective to inhibit cholesterol absorption than tea catechins rich in epigallocatechin gallate and epicatechin gallate. J Agric Food Chem 2003, 51:7303-7307.
13. Unno K., Takabayashi F., Oku N. Improvement in brain function and oxidative damage of aged senescence-accelerated mice by green tea catechins. Int Congress Series 2004, 1260:409-412.
14. Sarma D.N., Barrett M.L., Chavez M.L., Gardiner P., Ko R., Mahady G.B., et al. Safety of green tea extracts: a systematic review by the US Pharmacopeia. Drug Saf 2008, 31:469-484.
15. Hwang D.Y., Chae K.R., Kang T.S., Hwang J.H., Lim C.H., Kang H.K., et al. Alterations in behavior, amyloid β-42, caspase-3, and Cox-2 in mutant PS2 Tg mouse model of Alzheimer's disease. FASEB J 2002, 16:805-813.
16. Hwang D.Y., Cho J.S., Lee S.H., Chae K.R., Lim H.J., Min S.H., et al. Aberrant expressions of pathogenic phenotypes in Alzheimer's diseased transgenic mice carrying NSE-controlled APPsw. Exp Neurol 2004, 186:20-32.
17. Iwata N., Tsubuki S., Takaki Y., Watanabe K., Sekikuchi M., Hosoli E., et al. Identification of the major Aβ-42-degrading catabolic pathway in brain parenchyma: suppression leads to biochemical and pathological deposition. Nat Med 2000, 6:143-150.
18. Arnold S.E., Hyman B.T., Flory J., Damasio A.R., Van Hoesen G.W. The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cereb Cortex 1991, 1:103-116.
19. West M.J., Coleman P.D., Flood D.G., Troncoso J.C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 1994, 17:769-772.
20. Yu G., Chen F., Levesque G., Nishimura M., Zhang D.M., Levesque L., et al. The presenilin 1 protein is a component of a high molecular weight intracellular complex that contains beta-catenin. J Biol Chem 1998, 273:16470-16475.
21. Goutte C., Tsunozaki M., Hale V.A., Priess J.R. APH-1 is a multipass membrane protein essential for the Notch signaling pathway in Caenorhabditis elegans embryos. Proc Natl Acad Sci USA 2002, 99:8666-8671.
22. Francis R., McGrath G., Zhang J., Ruddy D.A., Sym M., Apfeld J., et al. APH-1 and PEN-2 are required for Notch pathway signaling, γ-secretase cleavage of βAPP, and presenilin protein accumulation. Dev Cell 2002, 3:85-92.
23. Takashima A., Murayama M., Murayama O., Kohno T., Honda T., Yasutake K., et al. Presenilin 1 associates with glycogen synthase kinase-3β and its substrate tau. Proc Natl Acad Sci USA 1998, 95:9637-9641.
24. Murayama M., Tanake S., Palacino J., Murayama O., Honda T., Yasutake K., et al. Direct association of presenilin-1 with beta-catenin. FEBS Lett 1998, 433:73-77.
25. De Ferrari G.V., Chacon M.A., Barria M.I., Garrido J.L., Godoy J.A., Olivares G., et al. Activation of Wnt signaling rescues neurodegeneration and behavioral impairments induced by beta-amyloid fibrils. Mol Psychiatry 2003, 8:195-208.
26. Zhang Z., Hartmann H., Do V.M., Abramowski D., Sturchler-Pierrat C., Staufenbiel M., et al. Destabilization of β-catenin by mutation in presenilin-1 potentiates neuronal apoptosis. Nature 1998, 395:698-702.
27. Lovestone S., Hartley C.A., Pearce J., Anderton B.H. Phosphorylation of tau by glycogen synthase kinase 3β in intact mammalian cells: the effect on the organization and stability of microtubules. Neuroscience 1996, 73:1145-1157.
28. Hong M., Chen D.C., Klein P.C., Lee V.M. Lithium reduces tau phosphorylation by inhibition of glycogen synthase kinase 3. J Biol Chem 1997, 272:25326-25332.
29. Munoz-Montano J.R., Moreno F.J., Avilaa J., Diaz-Nido J. Lithium Inhibits Alzheimer's disease-like tau protein phosphorylation in neuron. FEBS Lett 1997, 411:183-188.
30. Tesco G., Tanzi R.E. GSK3β forms a tetrameric complex with endogenous PS1-CTF/NTF and β-catenin. Effects of the D257/D385A and FAD-linked mutations. Ann NY Acad Sci 2000, 920:227-232.
31. Lu K.P., Hanes S.D., Hunter T. A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 1996, 11:544-547.
32. Liou Y.C., Sun A., Ryo A., Zhou X.Z., Yu Z.X., Hwang H.K., et al. Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature 2003, 31:556-561.
33. Min S.H., Cho J.S., Oh J.H., Shim S.B., Hwang D.Y., Lee S.H., et al. Tau and GSK3β dephosphorylations are required for regulating Pin1 phosphorylation. Neurochem Res 2005, 30:955-961.
34. Atkins C.M., Selcher J.C., Petraitis J.J., Trzaskos J.M., Sweatt J.D. The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1998, 1:602-609.
35. Savage M.J., Lin Y.G., Ciallella J.R., Flood D.G., Scott R.W. Activation of c-Jun N-terminal kinase and p38 in an Alzheimer's disease model is associated with amyloid deposition. J Neurosci 2002, 22:3376-3385.
36. Kuo Y.M., Emmerling M.R., Bisgaier C.L., Essenburg A.D., Lampert H.C., Drumm D., et al. Elevated low-density lipoprotein in Alzheimer's disease correlates with brain Aβ1-42 levels. Biochem Biophys Res Commun 1998, 252:711-715.
37. Lehtonen A., Luutonen S. High-density lipoprotein cholesterol levels of old people in the diagnosis of dementia. Age Aging 1986, 15:267-270.
38. Cho J.Y., Hwang D.Y., Kang T.S., Shin D.H., Hwang J.H., Lim C.H., et al. Use of NSE/PS2-Tg mice in the study of the protective effect of exercise on Alzheimer's disease. J Sports Sci 2003, 21:943-951.
39. Mandel S.A., Averamovich-Tirosh Y., Reqnichenko L., Zheng H., Weireb O., Admit T., et al. Multifunctional activities of green tea catechins in neuroprotection. Modulation of cell survival genes, iron-dependent oxidative stress and PKC signaling pathway. Neurosignals 2005, 14:46-60.
40. Butterfield D.A. Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta peptide. Trends Mol Med 2001, 7:548-554.
41. Cotman C.W., Berchtold N.C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 2002, 25:295-301.
42. Bush A.I., Masters C.L., Tanzi R.E. Copper, beta amyloid, and Alzheimer's disease: tapping a sensitive connection. Proc Natl Acad Sci USA 2003, 100:11193-11194.
43. Morgan D., Diamond D.M., Gottschall P.E., Ugen K.E., Dickey C., Hardy J., et al. Aβ peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 2000, 408:982-985.
44. Watson G.S., Craft S. The role of insulin resistance in the pathogenesis of Alzheimer's disease: implication for treatment. CNS Drugs 2003, 17:27-45.
45. Rogere J.T., Randall J.D., Cahill C.M., Eder P.S., Huang X., Gunshin H., et al. An iron-responsive element type II in the 5'-untranslated region of the Alzheimer's amyloid precursor protein transcript. J Biol Chem 2002, 277:45518-45528.
46. Hwang D.Y., Cho J.S., Kim C.K., Shim S.B., Jee S.W., Lee S.H., et al. Changes in presenilin 2-binding Wnt proteins, behavior, amyloid-β 42, γ-secretase activity, and testosterone sensitivity in Tg mice coexpressing tetracycline-controlled transactivator and human mutant presenilin 2. Neuromolecular Med 2006, 8:415-432.
47. Leu L.F., Kuo Y.M., Roher A.E., Brachova L., Sue L., Beach T., et al. Soluble amyloid β[U+F020]peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 1999, 155:853-862.
48. McLean C.A., Cherny R.A., Fraser F.W., Fuller S.J., Smith M.J., Beyreuter K., et al. Soluble pool of Aβ[U+F020]amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 1999, 46:860-866.
49. Naslund J., Haroutunian V., Moshs R., Davis K.L., Davies P., Greengard P., et al. Correlation between elevated levels of amyloid β-peptide in the brain and cognitive decline. J Am Med Assoc 2000, 283:1571-1577.
50. Wang J., Dickson D.W., Trojanowski J.Q., Lee V.M. The levels of soluble versus insoluble brain Abeta distinguish Alzheimer's disease from normal and pathologic aging. Exp Neurol 1999, 158:328-337.
51. Kuo Y.M., Emmerling M.R., Vigo-Pelfrey C., Kasunic T.C., Kirkpatrickm J.B., Murdock G.H., et al. Water-soluble Aβ (N-40, N-42) oligomers in normal and Alzheimer's disease brains. J Biol Chem 1996, 27:4077-4081.
52. Levities Y., Amit T., Youdim M.B., Mandel S. Involvement of protein kinase C activation and cell survival/cell cycle genes in green tea polyphenol, (-)-epigallocatechine-3-gallate neuroprotective action. J Biol Chem 2002, 277:30574-30580.
53. Pastorino L., Ikins A.F., Lamprianou S., Vacaresse N., Revelli J.P., Platt K., et al. BACE (β-secretase) modulates the processing of APLP2 in vivo. Mol Cell Neurosci 2004, 25:642-649.
54. Lazarov O., Robinson J., Tang Y.P., Hairston I.S., Korade-Mirnics Z., Lee V.M.Y., et al. Environmental enrichment reduces Aβ levels and amyloid deposition in Tg mice. Cell 2005, 120:701-703.
55. Barbiero L., Benussi L., Ghidoni R., Alberici A., Russo C., Schettini G., et al. BACE-2 is overexpressed in Down's syndrome. Exp Neurol 2003, 182:335-345.
56. Melzig M.F., Janka M. Enhancement of neutral endopeptidase activity in SK-N-SH cells by green tea extract. Phytomedicine 2003, 10:494-498.
57. Choi I.S., Lee Y.J., Choi D.Y., Lee Y.K., Lee Y.H., Kim K.H., et al. 4-O-methylhonokiol attenuated memory impairment through modulation of oxidative damage of enzymes involving amyloid-β generation and accumulation in a mouse model of Alzheimer's disease. J Alzheimers Dis 2011, 27:127-141.
58. Jeon S.Y., Bae K.W., Seong Y.H., Song K.S. Green tea cathechins as a BACE 1 (β-secretase) inhibitor. Bioorg Med Chem Lett 2003, 13:3905-3908.
59. Levites Y., Amit T., Mandel S., Youdim M.B. Neuroprotection and neurorescue against Aβ toxicity and PKC-dependent release of nonamyloidogenic soluble precursor protein by green tea polyphenol (-)-epigallocatechin-3-gallate. FASEB J 2003, 17:952-954.
60. Dashwood W.M., Orner G.A., Dashwood R.H. Inhibition of β-catenin/Tcf activity by white tea, green tea, and epigallocatechin-3-gallate (EGCG): minor contribution of H2O2 at physiologically relevant EGCG concentrations. Biochem Biophys Res Commun 2002, 296:584-588.
61. Long L.H., Clement M.V., Halliwell B. Artifact in cell culture rapidgeneration of hydrogen peroxide on addition of (-)-epigallocatechin, (-)-epigallocatechin gallate, (+) catechine, and quercetin to commonly used cell culture media. Biochem Biophys Res Commun 2000, 273:50-53.
62. Nusse R. WNT targets. Repression and activation. Trends Genet 1999, 15:1-3.
63. Koh S.H., Kim S.H., Kwon H., Kim J.G., Kim J.H., Yang K.H., et al. Phosphatidylinositol-3 kinase/Akt and GSK3 mediated cytoprotective effect of epigallocatechin gallate on oxidative stress-injured neuronal-differentiated N18D3 cells. Neurotoxicology 2004, 25:793-802.
64. Doble B.W., Woodgett J.R. GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 2003, 1:1175-1186.
65. Lee J.W., Lee Y.K., Ban J.O., Ha T.Y., Yun Y.P., Han S.B., 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, 139:1987-1993.
66. Kim S.K., Park H.J., Hong H.S., Baik E.J., Jung M.W., Mook-Jung I. ERK1/2 is an endogenous negative regulator of the gamma-secretase activity. FASEB J 2006, 20:157-159.
67. Cho H.J., Kim S.K., Jin S.M., Hwang E.M., Kim Y.S., Huh K., et al. IFN-gamma-induced BACE1 expression is mediated by activation of JAK2 and ERK1/2 signaling pathways and direct binding of STAT1 to BACE1 promoter in astrocytes. Glia 2007, 55:253-262.
68. Goto J.J., Tanzi R.E. The role of the low-density lipoprotein receptor-related protein (LRP1) in Alzheimer's Aβ-generation: development of a cell-based model system. J Mol Neurosci 2002, 191:37-41.
69. Bursill C., Roach P.D., Bottema C.D., Pal S. Green tea upregulates the low-density lipoprotein receptors through the sterol-regulated element binding protein in HepG2 liver cell. J Agric Food Chem 2001, 49:5639-5645.
70. Raederstorff D.G., Schlacchter M.F., Elste V., Weber P. Effect of EGCG on lipid absorption and plasma lipid levels on rats. J Nutr Biochem 2003, 14:328-332.
71. Weinreb O., Mandel S., Youdim M.B. cDNA gene expression profile homology of antioxidants and their antiapoptotic and proapoptotic activities in human neuroblastoma cells. FASEB J 2003, 17:935-937.
72. Murakami K., Irie K., Ohigashi H., Hara H., Nagao M., Shimizu T., et al. Formation and stabilization model of the 42-mer Abeta radical: implications for the long-lasting oxidative stress in Alzheimer's disease. J Am Chem Soc 2005, 127:15168-15174.
73. Tabner B.J., El-Agnaf O.M., Turnbull S., German M.J., Paleologou K.E., Hayashi Y., et al. Hydrogen peroxide is generated during the very early stages of aggregation of the amyloid peptides implicated in Alzheimer disease and familial British dementia. J Biol Chem 2005, 280:35789-35792.
74. Tamagno E., Bardini P., Obbili A., Vitali A., Borghi R., Zaccheo D., et al. Oxidative stress increases expression and activity of BACE in NT2 neurons. Neurobiol Dis 2002, 10:279-288.
75. Tong Y., Zhou W., Fung V., Christensen M.A., Qing H., Sun X., et al. Oxidative stress potentiates BACE1 gene expression and Abeta generation. J Neural Transm 2005, 112:455-469.
76. Kern A., Behl C. The unsolved relationship of brain aging and lateonset Alzheimer disease. Biochim Biophys Acta 2009, 1790:1124-1132.
77. Guglielmotto M., Giliberto L., Tamagno E., Tabaton M. Oxidative stress mediates the pathogenic effect of different Alzheimer's disease risk factors. Front Aging Neurosci 2010, 2:3.