Dietary (-)-epicatechin as a potent inhibitor of βγ-secretase amyloid precursor protein processing

Neurobiology of Aging

Volumn 36, Issue 1, 2015, Pages 178-187

  Cox, Carla J ^a   Choudhry, Fahd ^b   Peacey, Eleanor ^b   Perkinton, Michael S ^b,g   Richardson, Jill C ^c   Howlett, David R ^b   Lichtenthaler, Stefan F ^d,e,f   Francis, Paul T ^b   Williams, Robert J ^a  

^a University of Bath   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^f Germany 3 Munich Cluster for Systems Neurology   (Germany)

^g MEDIMMUNE   (United States)

Author keywords

Alzheimer's disease; Amyloid pathology; APP processing; A ; BACE1; Catechin; Dementia; Dietary polyphenolic; Flavanol; Flavonoid; TASTPM

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; APIGENIN; APIGETRIN; BETA SECRETASE; BETA SECRETASE 1; CATECHIN; COUMARIN; CYANIDIN CHLORIDE; DELPHINIDIN; DIOSMETIN; EPICATECHIN; EPICATECHIN GALLATE; EPIGALLOCATECHIN; EPIGALLOCATECHIN GALLATE; FISETIN; FLAVONOID; GAMMA SECRETASE; HESPERETIN; HYPERIN; KAEMPFEROL; NARIRUTIN; NICOTIFLORIN; PELARGONIDIN; QUERCETIN; SINENSETIN; UNCLASSIFIED DRUG; GALLOCATECHIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; DIET; DRUG MECHANISM; DRUG SCREENING; ENZYME INHIBITION; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PROTEIN PROCESSING; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; CELL CULTURE; DISEASE COURSE; GENETICS; METABOLISM; ORAL DRUG ADMINISTRATION; TRANSGENIC MOUSE;

ADMINISTRATION, ORAL; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CATECHIN; CELLS, CULTURED; DISEASE PROGRESSION; MALE; MICE, TRANSGENIC;

EID: 84920421756     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.07.032     Document Type: Article

References (47)

1. Abd El Mohsen M.M., Kuhnle G., Rechner A.R., Schroeter H., Rose S., Jenner P., Rice-Evans C.A. Uptake and metabolism of epicatechin and its access to the brain after oral ingestion. Free Radic. Biol. Med. 2002, 33:1693-1702.
2. Burg V.K., Grimm H.S., Rothhaar T.L., Grosgen S., Hundsdorfer B., Haupenthal V.J., Zimmer V.C., Mett J., Weingartner O., Laufs U., Broersen L.M., Tanila H., Vanmierlo T., Lutjohann D., Hartmann T., Grimm M.O. Plant sterols the better cholesterol in Alzheimer's disease? A mechanistical study. J.Neurosci. 2013, 33:16072-16087.
3. Citron M., Oltersdorf T., Haass C., McConlogue L., Hung A.Y., Seubert P., Vigo-Pelfrey C., Lieberburg I., Selkoe D.J. Mutation of the beta-amyloid precursor protein in familial Alzheimer's disease increases beta-protein production. Nature 1992, 360:672-674.
4. Colombo A., Wang H., Kuhn P.H., Page R., Kremmer E., Dempsey P.J., Crawford H.C., Lichtenthaler S.F. Constitutive alpha- and beta-secretase cleavages of the amyloid precursor protein are partially coupled in neurons, but not in frequently used cell lines. Neurobiol. Dis. 2012, 49C:137-147.
5. Commenges D., Scotet V., Renaud S., Jacqmin-Gadda H., Barberger-Gateau P., Dartigues J.F. Intake of flavonoids and risk of dementia. Eur. J. Epidemiol. 2000, 16:357-363.
6. Dai Q., Borenstein A.R., Wu Y., Jackson J.C., Larson E.B. Fruit and vegetable juices and Alzheimer's disease: the Kame Project. Am. J. Med. 2006, 119:751-759.
7. Doody R.S., Raman R., Farlow M., Iwatsubo T., Vellas B., Joffe S., Kieburtz K., He F., Sun X., Thomas R.G., Aisen P.S., Siemers E., Sethuraman G., Mohs R. Aphase 3 trial of semagacestat for treatment of Alzheimer's disease. N.J. Med. 2013, 369:341-350.
8. Ehrnhoefer D.E., Bieschke J., Boeddrich A., Herbst M., Masino L., Lurz R., Engemann S., Pastore A., Wanker E.E. EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat. Struct. Mol. Biol. 2008, 15:558-566.
9. Fernandez J.W., Rezai-Zadeh K., Obregon D., Tan J. EGCG functions through estrogen receptor-mediated activation of ADAM10 in the promotion of non-amyloidogenic processing of APP. FEBS Lett. 2010, 584:4259-4267.
10. Garcia-Alloza M., Borrelli L.A., Rozkalne A., Hyman B.T., Bacskai B.J. Curcumin labels amyloid pathology invivo, disrupts existing plaques, and partially restores distorted neurites in an Alzheimer mouse model. J.Neurochem. 2007, 102:1095-1104.
11. Hamaguchi T., Ono K., Murase A., Yamada M. Phenolic compounds prevent Alzheimer's pathology through different effects on the amyloid-beta aggregation pathway. Am. J. Pathol. 2009, 175:2557-2565.
12. Haque A.M., Hashimoto M., Katakura M., Hara Y., Shido O. Green tea catechins prevent cognitive deficits caused by Abeta1-40 in rats. J.Nutr. Biochem. 2008, 19:619-626.
13. Hardy J. The amyloid hypothesis for Alzheimer's disease: a critical reappraisal. J.Neurochem. 2009, 110:1129-1134.
14. Hardy J., Allsop D. Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol. Sci. 1991, 12:383-388.
15. Hardy J.A., Higgins G.A. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992, 256:184-185.
16. Ho L., Ferruzzi M.G., Janle E.M., Wang J., Gong B., Chen T.Y., Lobo J., Cooper B., Wu Q.L., Talcott S.T., Percival S.S., Simon J.E., Pasinetti G.M. Identification of brain-targeted bioactive dietary quercetin-3-O-glucuronide as a novel intervention for Alzheimer's disease. FASEB J. 2013, 27:769-781.
17. Hoey S.E., Buonocore F., Cox C.J., Hammond V.J., Perkinton M.S., Williams R.J. AMPA receptor activation promotes non-amyloidogenic amyloid precursor protein processing and suppresses neuronal amyloid-beta production. PLoS One 2013, 8:e78155.
18. Hoey S.E., Williams R.J., Perkinton M.S. Synaptic NMDA receptor activation stimulates-secretase amyloid precursor protein processing and inhibits amyloid-production. J.Neurosci. 2009, 29:4442-4460.
19. Howlett D.R., Richardson J.C., Austin A., Parsons A.A., Bate S.T., Davies D.C., Gonzalez M.I. Cognitive correlates of Abeta deposition in male and female mice bearing amyloid precursor protein and presenilin-1 mutant transgenes. Brain Res. 2004, 1017:130-136.
20. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
21. Imbimbo B.P., Panza F., Frisardi V., Solfrizzi V., D'Onofrio G., Logroscino G., Seripa D., Pilotto A. Therapeutic intervention for Alzheimer's disease with gamma-secretase inhibitors: still a viable option?. Expert Opin. Investig. Drugs 2011, 20:325-341.
22. Joseph J.A., Shukitt-Hale B., Denisova N.A., Bielinski D., Martin A., McEwen J.J., Bickford P.C. Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation. J.Neurosci. 1999, 19:8114-8121.
23. Kawahata I., Yoshida M., Sun W., Nakajima A., Lai Y., Osaka N., Matsuzaki K., Yokosuka A., Mimaki Y., Naganuma A., Tomioka Y., Yamakuni T. Potent activity of nobiletin-rich citrus reticulata peel extract to facilitate cAMP/PKA/ERK/CREB signaling associated with learning and memory in cultured hippocampal neurons: identification of the substances responsible for the pharmacological action. J.Neural Transm. 2013, 120:1397-1409.
24. Kuriyama S., Hozawa A., Ohmori K., Shimazu T., Matsui T., Ebihara S., Awata S., Nagatomi R., Arai H., Tsuji I. Green tea consumption and cognitive function: a cross-sectional study from the Tsurugaya Project 1. Am. J. Clin. Nutr. 2006, 83:355-361.
25. Lam I.K., Alex D., Wang Y.H., Liu P., Liu A.L., Du G.H., Lee S.M. Invitro and invivo structure and activity relationship analysis of polymethoxylated flavonoids: identifying sinensetin as a novel antiangiogenesis agent. Mol. Nutr. Food Res. 2012, 56:945-956.
26. Letenneur L., Proust-Lima C., Le Gouge A., Dartigues J., Barberger-Gateau P. Flavonoid intake and cognitive decline over a 10-year period. Am. J. Epidemiol. 2007, 165:1364-1371.
27. Maher P., Akaishi T., Abe K. Flavonoid fisetin promotes ERK-dependent long-term potentiation and enhances memory. Proc. Natl. Acad. Sci. U.S.A 2006, 103:16568-16573.
28. Manach C., Scalbert A., Morand C., Rémésy C., Jiménez L. Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 2004, 79:727-747.
29. Mandel S.A., Amit T., Kalfon L., Reznichenko L., Youdim M.B. Targeting multiple neurodegenerative diseases etiologies with multimodal-acting green tea catechins. J.Nutr. 2008, 138:1578S-1583S.
30. Mandel S.A., Amit T., Weinreb O., Youdim M.B. Understanding the broad-spectrum neuroprotective action profile of green tea polyphenols in aging and neurodegenerative diseases. J.Alzheimers Dis. 2011, 25:187-208.
31. Obregon D.F., Rezai-Zadeh K., Bai Y., Sun N., Hou H., Ehrhart J., Zeng J., Mori T., Arendash G.W., Shytle D., Town T., Tan J. ADAM10 activation is required for green tea (-)-epigallocatechin-3-gallate-induced alpha-secretase cleavage of amyloid precursor protein. J.Biol. Chem. 2006, 281:16419-16427.
32. Pasinetti G.M. Novel role of red wine-derived polyphenols in the prevention of Alzheimer's disease dementia and brain pathology: experimental approaches and clinical implications. Planta Med. 2012, 78:1614-1619.
33. Perkinton M.S., Standen C.L., Lau K.F., Kesavapany S., Byers H.L., Ward M., McLoughlin D.M., Miller C.C. The c-Abl tyrosine kinase phosphorylates the Fe65 adaptor protein to stimulate Fe65/amyloid precursor protein nuclear signaling. J.Biol. Chem. 2004, 279:22084-22091.
34. Ramassamy C. Emerging role of polyphenolic compounds in the treatment of neurodegenerative diseases: a review of their intracellular targets. Eur. J. Pharmacol. 2006, 545:51-64.
35. Renouf M., Marmet C., Guy P.A., Beaumont M., Lepage M., Williamson G., Dionisi F. Dose-response plasma appearance of green tea catechins in adults. Mol. Nutr. Food Res. 2013, 57:833-839.
36. Rezai-Zadeh K. Green tea epigallocatechin-3-gallate (EGCG) modulates amyloid precursor protein cleavage and reduces cerebral amyloidosis in Alzheimer transgenic mice. J.Neurosci. 2005, 25:8807-8814.
37. Rezai-Zadeh K., Arendash G.W., Hou H., Fernandez F., Jensen M., Runfeldt M., Shytle R.D., Tan J. 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.
38. Rice-Evans C.A., Miller N.J., Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 1996, 20:933-956.
39. Schroeter H., Heiss C., Balzer J., Kleinbongard P., Keen C.L., Hollenberg N.K., Sies H., Kwik-Uribe C., Schmitz H.H., Kelm M. (-)-Epicatechin mediates beneficial effects of flavanol-rich cocoa on vascular function in humans. Proc. Natl. Acad. Sci. U.S.A 2006, 103:1024-1029.
40. Shimmyo Y., Kihara T., Akaike A., Niidome T., Sugimoto H. Flavonols and flavones as BACE-1 inhibitors: structure-activity relationship in cell-free, cell-based and in silico studies reveal novel pharmacophore features. Biochim. Biophys. Acta 2008, 1780:819-825.
41. Suh J., Choi S.H., Romano D.M., Gannon M.A., Lesinski A.N., Kim D.Y., Tanzi R.E. ADAM10 missense mutations potentiate beta-amyloid accumulation by impairing prodomain chaperone function. Neuron 2013, 80:385-401.
42. van Praag H., Lucero M.J., Yeo G.W., Stecker K., Heivand N., Zhao C., Yip E., Afanador M., Schroeter H., Hammerstone J., Gage F.H. Plant-derived flavanol (-)epicatechin enhances angiogenesis and retention of spatial memory in mice. J.Neurosci. 2007, 27:5869-5878.
43. Vauzour D., Vafeiadou K., Rice-Evans C., Williams R.J., Spencer J.P. Activation of pro-survival Akt and ERK1/2 signalling pathways underlie the anti-apoptotic effects of flavanones in cortical neurons. J.Neurochem. 2007, 103:1355-1367.
44. Wang J., Ferruzzi M.G., Ho L., Blount J., Janle E.M., Gong B., Pan Y., Gowda G.A., Raftery D., Arrieta-Cruz I., Sharma V., Cooper B., Lobo J., Simon J.E., Zhang C., Cheng A., Qian X., Ono K., Teplow D.B., Pavlides C., Dixon R.A., Pasinetti G.M. Brain-targeted proanthocyanidin metabolites for Alzheimer's disease treatment. J.Neurosci. 2012, 32:5144-5150.
45. Wang J., Ho L., Zhao W., Ono K., Rosensweig C., Chen L., Humala N., Teplow D.B., Pasinetti G.M. Grape-derived polyphenolics prevent a oligomerization and attenuate cognitive deterioration in a mouse model of Alzheimer's disease. J.Neurosci. 2008, 28:6388-6392.
46. Williams R.J., Spencer J.P. Flavonoids, cognition, and dementia: actions, mechanisms, and potential therapeutic utility for Alzheimer disease. Free Radic. Biol. Med. 2012, 52:35-45.
47. Williams R.J., Spencer J.P.E., Rice-Evans C. Flavonoids: antioxidants or signalling molecules?. Free Radic. Biol. Med. 2004, 36:838-849.