Targeting multiple pathogenic mechanisms with polyphenols for the treatment of Alzheimer's disease-experimental approach and therapeutic implications

Frontiers in Aging Neuroscience

Volumn 6, Issue MAR, 2014, Pages

  Wang, Jun ^a,b   Bi, Weina ^a   Cheng, Alice ^a   Freire, Daniel ^a   Vempati, Prashant ^a   Zhao, Wei ^a   Gong, Bing ^a   Janle, Elsa M ^c   Chen, Tzu Ying ^c   Ferruzzi, Mario G ^c   Schmeidler, James ^a   Ho, Lap ^a   Pasinetti, Giulio M ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Alzheimer's disease (ad); Grape juice; Grape seed extract; J20 mice; Polyphenols; Resveratrol

Indexed keywords

3' O METHYL CATECHIN O BETA GLUCURINIDE; 3' O METHYL EPICATECHIN O BETA GLUCURONIDE; AMYLOID BETA PROTEIN; ANTHOCYANIN; CATECHIN; CATECHIN O BETA GLUCURINIDE; CONCORD GRAPE JUICE EXTRACT; CYANIDIN 3 O GLUCOSIDE; CYANIDIN GLUCOSIDE; DELPHINIDIN 3 O GLUCOSIDE; DELPHINIDIN GLUCOSIDE; EPICATECHIN; EPICATECHIN O BETA GLUCURONIDE; GALLIC ACID; GRAPE SEED EXTRACT; ISOQUERCITRIN; MALVIDIN 3 O GLUCOSIDE; MALVIDIN GLUCOSIDE; O METHYL QUERCETIN GLUCURONIDE; OLIGOMER; PEONIDIN 3 O GLUCOSIDE; PEONIDIN GLUCOSIDE; PETUNIDIN GLUCOSIDE; PETUNIDINBRAIN 3 O GLUCOSIDE; PLANT EXTRACT; POLYPHENOL DERIVATIVE; PROANTHOCYANIDIN; QUERCETIN; QUERCETIN GLUCURONIDE; RESVERATROL; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG EFFICACY; FEMALE; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MALE; MEMORY; MOUSE; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; PROTEIN CONTENT; RAT;

EID: 84898025679     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00042     Document Type: Article

References (51)

1. Aisen, P. S., and Davis, K. L. (1994). Inflammatory mechanisms in alzheimer's disease: implications for therapy. Am. J. Psychiatry 151, 1105-1113.
2. Aisen, P. S., Gauthier, S., Ferris, S. H., Saumier, D., Haine, D., Garceau, D., et al. (2011). Tramiprosate in mild-to-moderate Alzheimer's disease-a randomized, double-blind, placebo-controlled, multi-centre study (the alphase study). Arch. Med. Sci. 7, 102-111. doi: 10.5114/aoms.2011.20612
3. Akiyama, H., Barger, S., Barnum, S., Bradt, B., Bauer, J., Cole, G. M., et al. (2000). Inflammation and Alzheimer's disease. Neurobiol. Aging 21, 383-421. doi: 10.1016/S0197-4580(00)00124-X
4. Barnes, C. A., Rao, G., and Shen, J. (1997). Age-related decrease in the N-methyl-D-aspartateR-mediated excitatory postsynaptic potential in hippocampal region CA1. Neurobiol. Aging 18, 445-452. doi: 10.1016/S0197-4580(97)00044-4
5. Blennow, K., De Leon, M. J., and Zetterberg, H. (2006). Alzheimer's disease. Lancet 368, 387-403. doi: 10.1016/S0140-6736(06)69113-7
6. Bliss, T. V., and Collingridge, G. L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39. doi: 10.1038/361031a0
7. Capiralla, H., Vingtdeux, V., Zhao, H., Sankowski, R., Al-Abed, Y., Davies, P., et al. (2012). Resveratrol mitigates lipopolysaccharide- and Abeta-mediated microglial inflammation by inhibiting the TLR4/NF-kappaB/STAT signaling cascade. J. Neurochem. 120, 461-472. doi: 10.1111/j.1471-4159.2011.07594.x
8. Cooke, S. F., and Bliss, T. V. P. (2006). Plasticity in the human central nervous system. Brain 129, 1659-1673. doi: 10.1093/brain/awl082
9. Doody, R. S., Raman, R., Farlow, M., Iwatsubo, T., Vellas, B., Joffe, S., et al. (2013). A phase 3 trial of semagacestat for treatment of Alzheimer's disease. N. Engl. J. Med. 369, 341-350. doi: 10.1056/NEJMoa1210951
10. Doody, R. S., Thomas, R. G., Farlow, M., Iwatsubo, T., Vellas, B., Joffe, S., et al. (2014). Phase 3 trials of solanezumab for mild-to-moderate Alzheimer's disease. N. Engl. J. Med. 370, 311-321. doi: 10.1056/NEJMoa1312889
11. Ehrnhoefer, D. E., Bieschke, J., Boeddrich, A., Herbst, M., Masino, L., Lurz, R., et al. (2008). EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat. Struct. Mol. Biol. 15, 558-566. doi: 10.1038/nsmb.1437
12. Gerrish, A., Russo, G., Richards, A., Moskvina, V., Ivanov, D., Harold, D., et al. (2012). The role of variation at AbetaPP, PSEN1, PSEN2, and MAPT in late onset Alzheimer's disease. J. Alzheimers. Dis. 28, 377-387. doi: 10.3233/JAD-2011-110824
13. 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. doi: 10.1172/JCI22831
14. Green, R. C., Schneider, L. S., Amato, D. A., Beelen, A. P., Wilcock, G., Swabb, E. A., et al. (2009). Effect of tarenflurbil on cognitive decline and activities of daily living in patients with mild Alzheimer disease: a randomized controlled trial. JAMA 302, 2557-2564. doi: 10.1001/jama.2009.1866
15. Hardy, J. A., and Higgins, G. A. (1992). Alzheimer's disease: the amyloid cascade hypothesis. Science 256, 184-185. doi: 10.1126/science.1566067
16. Hartman, R. E., Shah, A., Fagan, A. M., Schwetye, K. E., Parsadanian, M., Schulman, R. N., et al. (2006). Pomegranate juice decreases amyloid load and improves behavior in a mouse model of Alzheimer's disease. Neurobiol. Dis. 24, 506-515. doi: 10.1016/j.nbd.2006.08.006
17. Ho, L., Chen, L. H., Wang, J., Zhao, W., Talcott, S. T., Ono, K., et al. (2009). Heterogeneity in red wine polyphenolic contents differentially influences alzheimer's disease-type neuropathology and cognitive deterioration. J. Alzheimers Dis. 16, 59-72. doi: 10.3233/JAD-2009-0916
18. Ho, L., Ferruzzi, M. G., Janle, E. M., Chen, Y., Cooper, B., Talcott, S., et al. (2011). "Development of brain-targeted grape derived polyphenolics for Alzheimer's disease prevention and therapy," in 5th International Conference on Polyphenols and Healthy (Barcelona).
19. Ho, L., Ferruzzi, M. G., Janle, E. M., Wang, J., Gong, B., Chen, T. Y., et al. (2013). Identification of brain-targeted bioactive dietary quercetin-3-O-glucuronide as a novel intervention for Alzheimer's disease. FASEB J. 27, 769-781. doi: 10.1096/fj.12-212118
20. Karuppagounder, S. S., Pinto, J. T., Xu, H., Chen, H. L., Beal, M. F., and Gibson, G. E. (2009). Dietary supplementation with resveratrol reduces plaque pathology in a transgenic model of Alzheimer's disease. Neurochem. Int. 54, 111-118. doi: 10.1016/j.neuint.2008.10.008
21. Krikorian, R., Nash, T. A., Shidler, M. D., Shukitt-Hale, B., and Joseph, J. A. (2010). Concord grape juice supplementation improves memory function in older adults with mild cognitive impairment. Br. J. Nutr. 103, 730-734. doi: 10.1017/S0007114509992364
22. Krstic, D., and Knuesel, I. (2013). Deciphering the mechanism underlying late-onset Alzheimer disease. Nat. Rev. Neurol. 9, 25-34. doi: 10.1038/nrneurol.2012.236
23. Krstic, D., Madhusudan, A., Doehner, J., Vogel, P., Notter, T., Imhof, C., et al. (2012). Systemic immune challenges trigger and drive Alzheimer-like neuropathology in mice. J. Neuroinflammation 9, 151. doi: 10.1186/1742-2094-9-151
24. Kumar, A., and Foster, T. C. (2013). Linking redox regulation of NMDAR synaptic function to cognitive decline during aging. J. Neurosci. 33, 15710-15715. doi: 10.1523/JNEUROSCI.2176-13.2013
25. Lagouge, M., Argmann, C., Gerhart-Hines, Z., Meziane, H., Lerin, C., Daussin, F., et al. (2006). Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127, 1109-1122. doi: 10.1016/j.cell.2006.11.013
26. Lee, W. H., Kumar, A., Rani, A., and Foster, T. C. (2013). Role of antioxidant enzymes in redox regulation of N-methyl-D-aspartate receptor function and memory in middle-aged rats. Neurobiol. Aging. doi: 10.1016/j.neurobiolaging.2013.12.002. [Epub ahead of print].
27. Liu, P., Kemper, L., Wang, J., Zahs, K., Ashe, K., and Pasinetti, G. (2011). Grape seed polyphenolic extract specifically decreases Aâ*56 in the brains of Tg2576 mice. J. Alzheimers Dis. 26, 657-666. doi: 10.3233/JAD-2011-110383
28. Marambaud, P., Zhao, H., and Davies, P. (2005). Resveratrol promotes clearance of Alzheimer's disease amyloid-β peptides. J. Biol. Chem. 280, 37377-37382. doi: 10.1074/jbc. M508246200
29. Morris, R. (1984). Developments of a water-maze procedure for studying spatial-learning in the rat. J. Neurosci. Methods 11, 47-60. doi: 10.1016/0165-0270(84)90007-4
30. Mucke, L., Masliah, E., Yu, G. Q., Mallory, M., Rockenstein, E. M., Tatsuno, G., et al. (2000). High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J. Neurosci. 20, 4050-4058.
31. Olsen, K. M., and Sheng, M. (2012). NMDA receptors and BAX are essential for Abeta impairment of LTP. Sci. Rep. 2, 225. doi: 10.1038/srep00225
32. Ono, K., Condron, M. M., Ho, L., Wang, J., Zhao, W., Pasinetti, G. M., et al. (2008). Effects of grape seed-derived polyphenols on amyloid {beta}-protein self-assembly and cytotoxicity. J. Biol. Chem. 283, 32176-32187. doi: 10.1074/jbc. M806154200
33. Rezai-Zadeh, K., Shytle, D., Sun, N., Mori, T., Hou, H., Jeanniton, D., et al. (2005). Green tea epigallocatechin-3-gallate (EGCG) modulates amyloid precursor protein cleavage and reduces cerebral amyloidosis in alzheimer transgenic mice. J. Neurosci. 25, 8807-8814. doi: 10.1523/JNEUROSCI.1521-05.2005
34. Ringman, J. M., Frautschy, S. A., Cole, G. M., Masterman, D. L., and Cummings, J. L. (2005). A potential role of the curry spice curcumin in Alzheimer's disease. Curr. Alzheimer Res. 2, 131-136. doi: 10.2174/1567205053585882
35. Rocha-Gonzalez, H. I., Ambriz-Tututi, M., and Granados-Soto, V. (2008). Resveratrol: a natural compound with pharmacological potential in neurodegenerative diseases. CNS Neurosci. Ther. 14, 234-247. doi: 10.1111/j.1755-5949.2008.00045.x
36. Salloway, S., Sperling, R., Fox, N. C., Blennow, K., Klunk, W., Raskind, M., et al. (2014). Two phase 3 trials of bapineuzumab in mild-to-moderate Alzheimer's disease. N. Engl. J. Med. 370, 322-333. doi: 10.1056/NEJMoa1304839
37. Selkoe, D. J. (2011). Resolving controversies on the path to Alzheimer's therapeutics. Nat. Med. 17, 1060-1065. doi: 10.1038/nm.2460
38. Smith, M. A., Rottkamp, C. A., Nunomura, A., Raina, A. K., and Perry, G. (2000). Oxidative stress in Alzheimer's disease. Biochim. Biophys. Acta 1502, 139-144. doi: 10.1016/S0925-4439(00)00040-5
39. Sperling, R. A., Aisen, P. S., Beckett, L. A., Bennett, D. A., Craft, S., Fagan, A. M., et al. (2011). Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 7, 280-292. doi: 10.1016/j.jalz.2011.03.003
40. Thomas, P., Wang, Y. J., Zhong, J. H., Kosaraju, S., O'Callaghan, N. J., Zhou, X. F., et al. (2009). Grape seed polyphenols and curcumin reduce genomic instability events in a transgenic mouse model for Alzheimer's disease. Mutat. Res. 661, 25-34. doi: 10.1016/j.mrfmmm.2008.10.016
41. Vingtdeux, V., Dreses-Werringloer, U., Zhao, H., Davies, P., and Marambaud, P. (2008). Therapeutic potential of resveratrol in Alzheimer's disease. BMC Neurosci. 9(Suppl. 2):S6. doi: 10.1186/1471-2202-9-S2-S6
42. Vingtdeux, V., Giliberto, L., Zhao, H., Chandakkar, P., Wu, Q., Simon, J. E., et al. (2010). AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J. Biol. Chem. 285, 9100-9113. doi: 10.1074/jbc. M109.060061
43. Wang, H. W., Pasternak, J. F., Kuo, H., Ristic, H., Lambert, M. P., Chromy, B., et al. (2002). Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res. 924, 133-140. doi: 10.1016/S0006-8993(01)03058-X
44. Wang, J., Ferruzzi, M. G., Ho, L., Blount, J., Janle, E. M., Gong, B., et al. (2012). Brain-targeted proanthocyanidin metabolites for Alzheimer's Disease treatment. J. Neurol. Sci. 32, 5144-5150. doi: 10.1523/JNEUROSCI.6437-11.2012
45. Wang, J., Ho, L., Chen, L., Zhao, Z., Zhao, W., Qian, X., et al. (2007). Valsartan lowers brain beta-amyloid protein levels and improves spatial learning in a mouse model of Alzheimer disease. J. Clin. Invest. 117, 3393-3402. doi: 10.1172/JCI31547
46. Wang, J., Ho, L., Qin, W., Rocher, A. B., Seror, I., Humala, N., et al. (2005). Caloric restriction attenuates beta-amyloid neuropathology in a mouse model of Alzheimer's disease. FASEB J. 19, 659-661. doi: 10.1096/fj.04-3182fje
47. Wang, J., Ho, L., Zhao, W., Ono, K., Rosensweig, C., Chen, L., et al. (2008). Grape-derived polyphenolics prevent Abeta oligomerization and attenuate cognitive deterioration in a mouse model of Alzheimer's disease. J. Neurosci. 28, 6388-6392. doi: 10.1523/JNEUROSCI.0364-08.2008
48. Wang, J., Ho, L., Zhao, Z., Seror, I., Humala, N., Dickstein, D. L., et al. (2006). Moderate consumption of cabernet sauvignon attenuates abeta neuropathology in a mouse model of Alzheimer's disease. FASEB J. 20, 2313-2320. doi: 10.1096/fj.06-6281com
49. Wang, J., Santa-Maria, I., Ho, L., Ksiezak-Reding, H., Ono, K., Teplow, D. B., et al. (2010). Grape derived polyphenols attenuate tau neuropathology in a mouse model of Alzheimer's disease. J. Alzheimers Dis. 22, 653-661. doi: 10.3233/JAD-2010-101074
50. Wang, Y. J., Thomas, P., Zhong, J. H., Bi, F. F., Kosaraju, S., Pollard, A., et al. (2009). Consumption of grape seed extract prevents amyloid-beta deposition and attenuates inflammation in brain of an Alzheimer's disease mouse. Neurotox. Res. 15, 3-14. doi: 10.1007/s12640-009-9000-x
51. Xu, Y., Simon, J. E., Welch, C., Wightman, J. D., Ferruzzi, M. G., Ho, L., et al. (2011). Survey of polyphenol constituents in grapes and grape-derived products. J. Agric. Food Chem. 59, 10586-10593. doi: 10.1021/jf202438d