Identification of brain-targeted bioactive dietary quercetin-3-O- glucuronide as a novel intervention for Alzheimer's disease

FASEB Journal

Volumn 27, Issue 2, 2013, Pages 769-781

  Ho, Lap ^a   Ferruzzi, Mario G ^c,d   Janle, Elsa M ^d   Wang, Jun ^a   Gong, Bing ^a   Chen, Tzu Ying ^d   Lobo, Jessica ^c   Cooper, Bruce ^c   Wu, Qing Li ^e   Talcott, Stephen T ^f   Percival, Susan S ^g   Simon, James E ^e   Pasinetti, Giulio Maria ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c PURDUE UNIVERSITY   (United States)

^d PURDUE UNIVERSITY   (United States)

^e RUTGERS UNIVERSITY   (United States)

^f TEXAS A AND M UNIVERSITY   (United States)

^g UNIVERSITY OF FLORIDA   (United States)

Author keywords

Cognitive deterioration; Neuroplasticity; Polyphenol bioavailability

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; ANTHOCYANIN; CATECHIN; EPICATECHIN; FLAVONOL DERIVATIVE; GALLIC ACID; GLUCURONIDE; MALVIDIN CHLORIDE; MITOGEN ACTIVATED PROTEIN KINASE; PARA COUMARIC ACID; POLYPHENOL DERIVATIVE; PROANTHOCYANIDIN DERIVATIVE; QUERCETIN 3 O GLUCURONIDE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VANILLIC ACID;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BIOAVAILABILITY; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG BLOOD LEVEL; ENZYME ACTIVATION; HIPPOCAMPUS; IN VITRO STUDY; LONG TERM POTENTIATION; MEMORY; MOUSE; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; RAT; RED WINE; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ADMINISTRATION, ORAL; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANTHOCYANINS; BIOLOGICAL AVAILABILITY; BRAIN; CELLS, CULTURED; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; HUMANS; MALE; MICE; MICE, TRANSGENIC; NEURONAL PLASTICITY; NEURONS; NEUROPROTECTIVE AGENTS; POLYPHENOLS; PROTEIN MULTIMERIZATION; QUERCETIN; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; WINE;

EID: 84873455519     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-212118     Document Type: Article

References (80)

1. Alzheimer's Association (2012) 2012 Alzheimer's disease facts and figures. Alzheimers Dement. 8, 131-168
2. Thies, W., and Bleiler, L. (2011) 2011 Alzheimer's disease facts and figures. Alzheimers Dement. 7, 208-244
3. Germain, S., Adam, S., Olivier, C., Cash, H., Ousset, P. J., Andrieu, S., Vellas, B., Meulemans, T., Reynish, E., and Salmon, E. (2009) Does cognitive impairment influence burden in caregivers of patients with Alzheimer's diseaseJ. Alzheimers Dis. 17, 105-114
4. Gonzalez, E. W., Polansky, M., Lippa, C. F., Walker, D., and Feng, D. (2011) Family caregivers at risk: who are theyIssues Ment. Health Nurs. 32, 528-536
5. Mausbach, B. T., Chattillion, E. A., Roepke, S. K., Patterson, T., Grant, I. (2012) A comparison of psychosocial outcomes in elderly Alzheimer caregivers and noncaregivers. [E-pub ahead of print] Am. J. Geriatr. Psychiatry doi: 10.1097/JGP.0b013e31824472d5
6. Mohamed, S., Rosenheck, R., Lyketsos, C. G., Schneider, L. S. (2010) Caregiver burden in Alzheimer disease: cross-sectional and longitudinal patient correlates. Am. J. Geriatr. Psychiatry 18, 917-927
7. Cummings, J. L. (2004) Alzheimer's disease. N. Engl. J. Med. 351, 56-67
8. Dorozynski, A. (1997) Wine may prevent dementia. BMJ 314, 997
9. Larrieu, S., Letenneur, L., Helmer, C., Dartigues, J. F., and Barberger-Gateau, P. (2004) Nutritional factors and risk of incident dementia in the PAQUID longitudinal cohort. J. Nutr. Health Aging 8, 150-154
10. Lindsay, J., Laurin, D., Verreault, R., Hebert, R., Helliwell, B., Hill, G. B., and McDowell, I. (2002) Risk factors for Alzheimer's disease: a prospective analysis from the Canadian Study of Health and Aging. Am. J. Epidemiol. 156, 445-453
11. Luchsinger, J. A., Tang, M. X., Siddiqui, M., Shea, S., and Mayeux, R. (2004) Alcohol intake and risk of dementia. J. Am. Geriatr. Soc. 52, 540-546
12. Orgogozo, J. M., Dartigues, J. F., Lafont, S., Letenneur, L., Commenges, D., Salamon, R., Renaud, S., and Breteler, M. B. (1997) Wine consumption and dementia in the elderly: a prospective community study in the Bordeaux area. Rev. Neurol. (Paris) 153, 185-192
13. Truelsen, T., Thudium, D., and Gronbaek, M. (2002) Amount and type of alcohol and risk of dementia: the Copenhagen City Heart Study. Neurology 59, 1313-1319
14. Wang, J., Ho, L., Zhao, Z., Seror, I., Humala, N., Dickstein, D. L., Thiyagarajan, M., Percival, S. S., Talcott, S. T., and Pasinetti, G. M. (2006) Moderate consumption of Cabernet Sauvignon attenuates Abeta neuropathology in a mouse model of Alzheimer's disease. FASEB J. 20, 2313-2320
15. German, J. B., and Walzem, R. L. (2000) The health benefits of wine. Annu. Rev. Nutr. 20, 561-593
16. Quideau, S., Deffieux, D., Douat-Casassus, C., and Pouysegu, L. (2011) Plant polyphenols: chemical properties, biological activities, and synthesis. Angew. Chem. Int. Ed. Engl. 50, 586-621
17. Zenebe, W., and Pechanova, O. (2002) Effects of red wine polyphenolic compounds on the cardiovascular system. Bratisl. Lek. Listy. 103, 159-165
18. Ho, L., Chen, L. H., Wang, J., Zhao, W., Talcott, S. T., Ono, K., Teplow, D., Humala, N., Cheng, A., Percival, S. S., Ferruzzi, M., Janle, E., Dickstein, D. L., and Pasinetti, G. M. (2009) Heterogeneity in red wine polyphenolic contents differentially influences Alzheimer's disease-type neuropathology and cognitive deterioration. J. Alzheimers Dis. 16, 59-72
19. Thimothe, J., Bonsi, I. A., Padilla-Zakour, O. I., and Koo, H. (2007) Chemical characterization of red wine grape (Vitis vinifera and Vitis interspecific hybrids) and pomace phenolic extracts and their biological activity against Streptococcus mutans. J. Agric. Food Chem. 55, 10200-10207
20. Cantos, E., Espin, J. C., and Tomas-Barberan, F. A. (2002) Varietal differences among the polyphenol profiles of seven table grape cultivars studied by LC-DAD-MS-MS. J. Agric. Food Chem. 50, 5691-5696
21. Masa, A., Vilanova, M., and Pomar, F. (2007) Varietal differences among the flavonoid profiles of white grape cultivars studied by high-performance liquid chromatography. J. Chromatogr. A 1164, 291-297
22. Onso Borbalan, A. M., Zorro, L., Guillen, D. A., and Barroso, C. G. (2003) Study of the polyphenol content of red and white grape varieties by liquid chromatography-mass spectrometry and its relationship to antioxidant power. J. Chromatogr. A 1012, 31-38
23. Perez-Magarino, S., and Gonzalez-San Jose, M. L. (2004) Evolution of flavanols, anthocyanins, and their derivatives during the aging of red wines elaborated from grapes harvested at different stages of ripening. J. Agric. Food Chem. 52, 1181-1189
24. De La Hera Orts, M. L., Martinez-Cutillas, A., Lopez Roca, J. M., Perez-Prieto, E., and Gomez-Plaze, E. (2005) Effect of deficit irrigation on anthocyanin content of Monastrell grapes and wines. J. Intl. Sci. Vigne Vin 39, 47-55
25. Esteban, M. A., Villanueva, M. J., and Lissarrague, J. R. (2001) Effect of irrigation on changes in the anthocyanin composition of the skin of cv Tempranillo (Vitis vinifera L.) grape berries during ripening. J. Sci. Food Agric. 81, 409-420
26. Radovanovic, B. C., Radovanovic, A. N., and Souquet, J. M. (2010) Phenolic profile and free radical-scavenging activity of Cabernet Sauvignon wines of different geographical origins from the Balkan region. J. Sci. Food Agric. 90, 2455-2461
27. Yokotsuka, K., Nagao, A., Nakazawa, K., and Sato, M. (1999) Changes in anthocyanins in berry skins of Merlot and Cabernet Sauvignon grapes grown in two soils modified with limestone or oyster shell versus a native soil over two years. Am. J. Enol. Viticult. 50, 1-12
28. Brouillard, R., George, F., and Fougerousse, A. (1997) Polyphenols produced during red wine ageing. Biofactors 6, 403-410
29. Ginjom, I. R., D'Arcy, B. R., Caffin, N. A., and Gidley, M. J. (2010) Phenolic contents and antioxidant activities of major Australian red wines throughout the winemaking process. J. Agric. Food Chem. 58, 10133-10142
30. Lee, J. E., Hwang, G. S., Van Den, B. F., Lee, C. H., and Hong, Y. S. (2009) Evidence of vintage effects on grape wines using 1H NMR-based metabolomic study. Anal. Chim. Acta 648, 71-76
31. Manach, C., Scalbert, A., Morand, C., Remesy, C., and Jimenez, L. (2004) Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79, 727-747
32. Han, X., Shan, T., and Lou, H. (2007) Dietary polyphenols and their biological significance. Int. J. Mol. Sci. 8, 47-53
33. Xu, Y., Simon, J. E., Welch, C., Wightman, J. D., Ferruzzi, M. G., Ho, L., Passinetti, G. M., and Wu, Q. (2011) Survey of polyphenol constituents in grapes and grape-derived products. J. Agric. Food Chem. 59, 10586-10593
34. Craggs, L., and Kalaria, R. N. (2011) Revisiting dietary antioxidants, neurodegeneration and dementia. Neuroreport 22, 1-3
35. Ho, L., and Pasinetti, G. M. (2010) Polyphenolic compounds for treating neurodegenerative disorders involving protein misfolding. Expert Rev. Proteom. 7, 579-589
36. Joseph, J., Cole, G., Head, E., and Ingram, D. (2009) Nutrition, brain aging, and neurodegeneration. J. Neurosci. 29, 12795-12801
37. Magrone, T., and Jirillo, E. (2011) Potential application of dietary polyphenols from red wine to attaining healthy ageing. Curr. Top. Med. Chem. 11, 1780-1796
38. Mandel, S. A., Weinreb, O., Amit, T., and Youdim, M. B. (2012) Molecular mechanisms of the neuroprotective/neurorescue action of multi-target green tea polyphenols. Front. Biosci. 4, 581-598
39. Ramesh, B. N., Rao, T. S., Prakasam, A., Sambamurti, K., and Rao, K. S. (2010) Neuronutrition and Alzheimer's disease. J. Alzheimers Dis. 19, 1123-1139
40. Vafeiadou, K., Vauzour, D., and Spencer, J. P. (2007) Neuroinflammation and its modulation by flavonoids. Endocr. Metab. Immune. Disord. Drug Targets 7, 211-224
41. Percival, S. S., and Sims, C. A. (2000) Wine modifies the effects of alcohol on immune cells of mice. J. Nutr. 130, 1091-1094
42. Zoecklein, B. W., Fugelsang, K. C., Gump, B. H., Nury, F. S., and Abraham, S. K. (1990) Production Wine Analysis, Van Nostrand Reinhold, New York
43. Talcott, S. T., and Lee, J. H. (2002) Ellagic acid and flavonoid antioxidant content of muscadine wine and juice. J. Agric. Food Chem. 50, 3186-3192
44. Kelley, K. A., Ho, L., Winger, D., Freire-Moar, J., Borelli, C. B., Aisen, P. S., and Pasinetti, G. M. (1999) Potentiation of excitotoxicity in transgenic mice overexpressing neuronal cyclooxygenase-2. Am. J. Pathol. 155, 995-1004
45. Bitan, G., Lomakin, A., and Teplow, D. B. (2001) Amyloid beta-protein oligomerization: prenucleation interactions revealed by photo-induced cross-linking of unmodified proteins. J. Biol. Chem. 276, 35176-35184
46. Gong, B., Vitolo, O. V., Trinchese, F., Liu, S., Shelanski, M., and Arancio, O. (2004) Persistent improvement in synaptic and cognitive functions in an Alzheimer mouse model after rolipram treatment. J. Clin. Invest. 114, 1624-1634
47. Shih, P. H., Wu, C. H., Yeh, C. T., and Yen, G. C. (2011) Protective effects of anthocyanins against amyloid beta-peptideinduced damage in neuro-2A cells. J. Agric. Food Chem. 59, 1683-1689
48. Hou, Y., Aboukhatwa, M. A., Lei, D. L., Manaye, K., Khan, I., and Luo, Y. (2010) Anti-depressant natural flavonols modulate BDNF and beta amyloid in neurons and hippocampus of double TgAD mice. Neuropharmacology 58, 911-920
49. Bitan, G., Kirkitadze, M. D., Lomakin, A., Vollers, S. S., Benedek, G. B., and Teplow, D. B. (2003) Amyloid beta-protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc. Natl. Acad. Sci. U. S. A. 100, 330-335
50. Bitan, G., Fradinger, E. A., Spring, S. M., and Teplow, D. B. (2005) Neurotoxic protein oligomers-what you see is not always what you get. Amyloid 12, 88-95
51. Bliss, T. V., and Collingridge, G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39
52. Bartsch, D., Casadio, A., Karl, K. A., Serodio, P., and Kandel, E. R. (1998) CREB1 encodes a nuclear activator, a repressor, and a cytoplasmic modulator that form a regulatory unit critical for long-term facilitation. Cell 95, 211-223
53. Bito, H., and Takemoto-Kimura, S. (2003) Ca2/CREB/CBPdependent gene regulation: a shared mechanism critical in long-term synaptic plasticity and neuronal survival. Cell Calcium 34, 425-430
54. Guedj, F., Sebrie, C., Rivals, I., Ledru, A., Paly, E., Bizot, J. C., Smith, D., Rubin, E., Gillet, B., Arbones, M., and Delabar, J. M. (2009) Green tea polyphenols rescue of brain defects induced by overexpression of DYRK1A. PLoS One 4, e4606
55. Xu, Y., Cui, C., Pang, C., Christen, Y., and Luo, Y. (2007) Restoration of impaired phosphorylation of cyclic AMP response element-binding protein (CREB) by EGb 761 and its constituents in Aexpressing neuroblastoma cells. Eur. J. Neurosci. 26, 2931-2939
56. Ohta, K., Mizuno, A., Li, S., Itoh, M., Ueda, M., Ohta, E., Hida, Y., Wang, M. X., Furoi, M., Tsuzuki, Y., Sobajima, M., Bohmoto, Y., Fukushima, T., Kobori, M., Inuzuka, T., and Nakagawa, T. (2011) Endoplasmic reticulum stress enhances gamma-secretase activity. Biochem. Biophys. Res. Commun. 416, 362-366
57. Yao, Y., Han, D. D., Zhang, T., and Yang, Z. (2010) Quercetin improves cognitive deficits in rats with chronic cerebral ischemia and inhibits voltage-dependent sodium channels in hippocampal CA1 pyramidal neurons. Phytother. Res. 24, 136-140
58. Hu, P., Wang, M., Chen, W. H., Liu, J., Chen, L., Yin, S. T., Yong, W., Chen, J. T., Wang, H. L., and Ruan, D. Y. (2008) Quercetin relieves chronic lead exposure-induced impairment of synaptic plasticity in rat dentate gyrus in vivo. Naunyn Schmiedebergs Arch. Pharmacol. 378, 43-51
59. Alberini, C. M. (2005) Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processesTrends Neurosci. 28, 51-56
60. Hsiao, K., Chapman, P., Nilsen, S., Eckman, C., Harigaya, Y., Younkin, S., Yang, F., and Cole, G. (1996) Correlative memory deficits, A-elevation, and amyloid plaques in transgenic mice. Science 274, 99-102
61. Fitzjohn, S. M., Morton, R. A., Kuenzi, F., Rosahl, T. W., Shearman, M., Lewis, H., Smith, D., Reynolds, D. S., Davies, C. H., Collingridge, G. L., and Seabrook, G. R. (2001) Agerelated impairment of synaptic transmission but normal longterm potentiation in transgenic mice that overexpress the human APP695SWE mutant form of amyloid precursor protein. J. Neurosci. 21, 4691-4698
62. Scalbert, A., Johnson, I. T., and Saltmarsh, M. (2005) Polyphenols: antioxidants and beyond. Am. J. Clin. Nutr. 81, 215S-217S
63. Urquiaga, I., and Leighton, F. (2000) Plant polyphenol antioxidants and oxidative stress. Biol. Res. 33, 55-64
64. Bastianetto, S., Krantic, S., Chabot, J. G., and Quirion, R. (2011) Possible involvement of programmed cell death pathways in the neuroprotective action of polyphenols. Curr. Alzheimer Res. 8, 445-451
65. Darvesh, A. S., Carroll, R. T., Bishayee, A., Geldenhuys, W. J., and Van der Schyf, C. J. (2010) Oxidative stress and Alzheimer's disease: dietary polyphenols as potential therapeutic agents. Expert Rev. Neurother. 10, 729-745
66. Singh, M., Arseneault, M., Sanderson, T., Murthy, V., and Ramassamy, C. (2008) Challenges for research on polyphenols from foods in Alzheimer's disease: bioavailability, metabolism, and cellular and molecular mechanisms. J. Agric. Food Chem. 56, 4855-4873
67. Wang, J., Santa-Maria, I., Ho, L., Ksiezak-Reding, H., Ono, K., Teplow, D. B., and Pasinetti, G. M. (2010) Grape derived polyphenols attenuate tau neuropathology in a mouse model of Alzheimer's disease. J. Alzheimers Dis. 22, 653-661
68. Wang, J., Ferruzzi, M. G., Ho, L., Blount, J., Janle, E. M., Gong, B., Pan, Y., Gowda, G. A., Raftery, D., rrieta-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., and Pasinetti, G. M. (2012) Brain-targeted proanthocyanidin metabolites for Alzheimer's disease treatment. J. Neurosci. 32, 5144-5150
69. Andres-Lacueva, C., Shukitt-Hale, B., Galli, R. L., Jauregui, O., Lamuela-Raventos, R. M., and Joseph, J. A. (2005) Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory. Nutr. Neurosci. 8, 111-120
70. Rangel-Ordonez, L., Noldner, M., Schubert-Zsilavecz, M., and Wurglics, M. (2010) Plasma levels and distribution of flavonoids in rat brain after single and repeated doses of standardized Ginkgo biloba extract EGb 761(R). Planta Med. 76, 1683-1690
71. De Boer, V. C., Dihal, A. A., van der Woude, H., Arts, I. C., Wolffram, S., Alink, G. M., Rietjens, I. M., Keijer, J., and Hollman, P. C. (2005) Tissue distribution of quercetin in rats and pigs. J. Nutr. 135, 1718-1725
72. Rivera, F., Urbanavicius, J., Gervaz, E., Morquio, A., and Dajas, F. (2004) Some aspects of the in vivo neuroprotective capacity of flavonoids: bioavailability and structure-activity relationship. Neurotox. Res. 6, 543-553
73. Meiers, S., Kemeny, M., Weyand, U., Gastpar, R., von, A. E., and Marko, D. (2001) The anthocyanidins cyanidin and delphinidin are potent inhibitors of the epidermal growth-factor receptor. J. Agric. Food Chem. 49, 958-962
74. Moon, J. H., Tsushida, T., Nakahara, K., and Terao, J. (2001) Identification of quercetin 3-O-beta-d-glucuronide as an antioxidative metabolite in rat plasma after oral administration of quercetin. Free Radic. Biol. Med. 30, 1274-1285
75. Day, A. J., Gee, J. M., DuPont, M. S., Johnson, I. T., and Williamson, G. (2003) Absorption of quercetin-3-glucoside and quercetin-4=-glucoside in the rat small intestine: the role of lactase phlorizin hydrolase and the sodium-dependent glucose transporter. Biochem. Pharmacol. 65, 1199-1206
76. Spencer, J. P., Rice-Evans, C., and Williams, R. J. (2003) Modulation of pro-survival Akt/protein kinase B and ERK1/2 signaling cascades by quercetin and its in vivo metabolites underlie their action on neuronal viability. J. Biol. Chem. 278, 34783-34793
77. Vafeiadou, K., Vauzour, D., Rodriguez-Mateos, A., Whiteman, M., Williams, R. J., and Spencer, J. P. (2008) Glial metabolism of quercetin reduces its neurotoxic potential. Arch. Biochem. Biophys. 478, 195-200
78. Shimmyo, Y., Kihara, T., Akaike, A., Niidome, T., and Sugimoto, H. (2008) 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 1780, 819-825
79. Tchantchou, F., Lacor, P. N., Cao, Z., Lao, L., Hou, Y., Cui, C., Klein, W. L., and Luo, Y. (2009) Stimulation of neurogenesis and synaptogenesis by bilobalide and quercetin via common final pathway in hippocampal neurons. J. Alzheimers Dis. 18, 787-798
80. Porat, Y., Abramowitz, A., and Gazit, E. (2006) Inhibition of amyloid fibril formation by polyphenols: structural similarity and aromatic interactions as a common inhibition mechanisms. Chem. Biol. Drug Des. 67, 27037