Neuroprotective effects of curcumin

Advances in Experimental Medicine and Biology

Volumn 595, Issue , 2007, Pages 197-212

  Cole, Greg M ^a   Teter, Bruce ^b   Frautschy, Sally A ^b  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; AMYLOID; CURCUMIN; SYNUCLEIN;

AGING; ALZHEIMER DISEASE; BOVINE SPONGIFORM ENCEPHALOPATHY; CELL DIFFERENTIATION; CEREBROVASCULAR DISEASE; DOSE RESPONSE; DRUG ACTIVITY; DRUG EFFECT; DRUG INHIBITION; DRUG MECHANISM; DRUG MEGADOSE; FRONTOTEMPORAL DEMENTIA; HEAD INJURY; HUMAN; HUNTINGTON CHOREA; IN VITRO STUDY; IN VIVO STUDY; LOW DRUG DOSE; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; STEM CELL; STROKE; TAUOPATHY;

EID: 84934440892     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-0-387-46401-5_8     Document Type: Review

References (90)

1. G. M. Cole, F. Yang, G. P. Lim, J. L. Cummings, D. L. Masterman, and S. A. Frautschy, A rationale for curcuminoids for the prevention or treatment of Alzheimer's disease. Curr Med Chem-Immun, Endoc, & Metab Agents 3, 15-25 (2003).
2. J. M. Ringman, S. A. Frautschy, G. M. Cole, D L. Masterman, and J. L. Cummings, A potential role of the curry spice curcumin in Alzheimer's disease. Curr Alzheimer Res 2, 131-136 (2005).
3. G. Garcea, D. J. Jones, R. Singh, A. R. Dennison, p. B. Farmer, R. A. Sharma, W. P. Steward, A. J. Gescher, and D. P. Berry, Detection of curcumin and its metabolites in hepatic tissue and portal blood of patients following oral administration. Br J Cancer 90, 1011-1015 (2001).
4. C. D. Lao, M. T. T. Ruffin, D. Normolle, D. D. Heath, S. I. Murray, J. M. Bailey, M. E. Boggs, J. Crowell, C. L. Rock, and D. E. Brenner, Dose escalation of a curcuminoid formulation. BMC Complement Altern Med 6, 10 (2006).
5. H. Y. Hsu and M. H. Wen, Lipopolysaccharide-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J Biol Chem 277, 22,131-22,139 (2002).
6. A. A. Nanji, K. Jokelainen, G. L. Tipoe, A. Rahemtulla, P. Thomas, and A. J. Dannenberg, Curcumin prevents alcohol-induced liver disease in rats by inhibiting the expression of NF-kappa B-dependent genes. Am J Physiol Gastrointest Liver Physiol 284, G321-327 (2003).
7. F. A. Al-Omar, M. N. Nagi, M. M. Abdulgadir, K. S. Al Joni, and A. A. Al-Majed, Immediate and delayed treatments with curcumin prevents forebrain ischemia-induced neuronal damage and oxidative insult in the rat hippocampus. Neurochem Res 31, 611-618 (2006).
8. S. Shishodia, P. Potdar, C. G. Gairola, and B. B. Aggarwal, Curcumin (diferuloylmethane) down-regulates cigarette smoke-induced NF-kappaB activation through inhibition of IkappaBalpha kinase in human lung epithelial cells: Correlation with suppression of COX-2, MMP-9 and cyclin D1. Carcinogenesis 24, 1269-1279 (2005).
9. G. Kang, P. J. Kong, Y. J. Yuh, S. Y. Lim, S. V. Yim, W. Chun, and S. S. Kim, Curcumin suppresses lipopolysaccharide-induced cyclooxygenase-2 expression by inhibiting activator protein 1 and nuclear factor kappab bindings in BV2 microglial cells. J Pharmacol Sci 94, 325-328 (2004).
10. I. Rahman, J. Marwick, and P. Kirkham, Redox modulation of chromatin remodeling: Impact on histone acetylation and deacetylation, NF-kappaB and pro-inflammatory gene expression. Biochem Pharmacol 68, 1255-1267 (2004).
11. J. Fang, J. Lu, an d A. Holmgren, Thioredoxin reductase is irreversibly modified by curcumin: A novel molecular mechanism for its anticancer activity. J Biol Chem 280, 25,284-25,290 (2005).
12. A. T. Dinkova-Kostova and P. Talalay, Relation of structure of curcumin analogs to their potencies as inducers of Phase 2 detoxification enzymes. Carcinogenesis 20, 911-914 (1999).
13. E. Balogun, M. Hoque, P. Gong, E. Killeen, C. J. Green, R. Foresti, J. Alam, and R. Motterlini, Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem J 371, 887-895 (2003).
14. P. Dikshit, A. Goswami, A. Mishra, N. Nukina, and N. R. Jana, Curcumin enhances the polyglutamine-expanded truncated N-terminal huntingtin-induced cell death by promoting proteasomal malfunction. Biochem Biophys Res Commun 342, 1323-1328 (2006).
15. R. E. Ali and S. I. Rattan, Curcumin's biphasic hormetic response on proteasome activity and heat-shock protein synthesis in human keratinocytes. Ann NY Acad Sci 1067, 394-399 (2006).
16. S. K. Kang, S. H. Cha, and H. G. Jeon, Curcumin-induced histone hypoacetylation enhances caspase-3-dependent glioma cell death and neurogenesis of neural progenitor cells. Stem Cells Dev 15, 165-174 (2006).
17. M. M. Chan, H. I. Huang, M. R. Fenton, and D. Fong, In vivo inhibition of nitric oxide synthase gene expression by curcumin, a cancer preventive natural product with anti-inflammatory properties. Biochem Pharmacol 55, 1955-1962 (1998).
18. F. E. Parodi, D. Mao, T. L. Ennis, M. B. Pagano, and R. W. Thompson, Oral administration of diferuloylmethane (curcumin) suppresses proinflammatory cytokines and destructive connective tissue remodeling in experimental abdominal aortic aneurysms, Ann Vasc Surg 20, 360-368 (2006).
19. Y. Luo, A. Hattori, J. Munoz, Z. Qin, and G. Roth, Intrastriatal dopamine injection induces apoptosis through oxidation-involved activation of transcription factors ap-1 and nf-kappab in rats. Mol Pharmacol 56, 254-264 (1999).
20. R. Brookmeyer, S. Gray, and C. Kawas, Projections of Alzheimer's disease in the United States and the public health impact of delaying disease onset. Am J Public Health 88, 1337-1342 (1998).
21. J. Hardy, Amyloid, the presenilins and Alzheimer's disease . Trends Neurosci 20, 154-159 (1997).
22. D. J. Selkoe, Alzheimer's disease: Genotypes, phenotypes, and treatments. Science 275, 630-631 (1997).
23. D. Games, D. Adams, R. Alessandrini, R. Barbour, P. Berthelette, C. Blackwell, T. Carr, J. Clemens, T. Donaldson, F. Gillespie, T. Guido, S. Hagoplan, K. Johnson-Wood, K. Khan, M. Lee, P. Leibowitz, I. Lieberburg, S. Little, E. Masliah, L. McConlogue, M. Montoya-Zavala, L. Mucke, L. Paganini, E. Penniman, M. Power, D. Schenk, P. Seubert, B. Snyder, F. Soriano, H. Tan, J. Vitale, S. Wadsworth, B. Wolozin, and J. Zhao, Alzheimer-type neuropathology in transgenic mice overexpressing V717F b-amyloid precursor protein. Nature 373, 523-527 (1995).
24. K. Hsiao, P. Chapman, S. Nilsen, C. Eckman, Y. Harigaya, S. Younkin, F. Yang, and G. Cole, G., Correlative memory deficits, Ab elevation and amyloid plaques in transgenic mice. Science 274, 99-102 (1996).
25. G. P. Lim, T. Chu, F. Yang, W. Beech, S. A. Frautschy, and G. M. Cole, The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J Neurosci 21, 8370-8377 (2001).
26. S. A. Frautschy, W. Hu, S. A. Miller, P. Kim, M. E. Harris-White, and G. M. Cole, Phenolic anti-inflammatory antioxidant reversal of Aβ-induced cognitive deficits and neuropathology. Neurobiol Aging 22, 991-1003 (2001).
27. F. Yang, G. P. Lim, A. N. Begum, O. J. Ubeda, M. R. Simmons, S. S. Ambegaokar, P. P. Chen, R. Kayed, C. G. Glabe, S. A. Frautschy, and G. M. Cole, Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J Biol Chem 280, 5892-5901 (2005).
28. P. Das, M. P. Murphy, L. H. Younkin, S. G. Younkin, and T. E. Golde, Reduced effectiveness of Abeta1-42 immunization in APP transgenic mice with significant amyloid deposition. Neurobiol Aging 22, 721-727 (2001).
29. S. Sung, Y. Yao, K. Uryu, H. Yang, V. M. Lee, J. Q. Trojanowski, and D. Pratico,. Early vitamin E supplementation in young but not aged mice reduces Abeta levels and amyloid deposition in a transgenic model of Alzheimer's disease. FASEB J 18, 323-325 (2004).
30. X. Huang, C. S. Atwood, R. D. Moir, M. A. Hartshorn, R. E. Tanzi, and A. I. Bush, Trace metal contamination initiates the apparent auto-aggregation, amyloidosis, and oligomerization of Alzheimer's Abeta peptides. J Biol Inorg Chem 9, 954-960 (2004).
31. K. Fassbender, M. Simons, C. Bergmann, M. Stroick, D. Lutjohann, P. Keller, H. Runz, S. Kuhl, T. Bertsch, K. von Bergmann, M. Hennerici, K. Beyreuther, and T. Hartmann, Simvastatin strongly reduces levels of Alzheimer's disease beta -amyloid peptides Abeta 42 and Abeta 40 in vitro and in vivo. Proc Natl Acad Sci USA 98, 5856-5861 (2001).
32. L. M. Refolo, M. A. Pappola, J. LaFrancois, B. Malester, S. D. Schmidt, T. Thomas-Bryant, G. S. Tint, R. Wang, M. Mercken, S. S. Petanceska, and K. E. Duff, A cholesterol-lowering drug reduces β-amyloid pathology in a transgenic mouse model of Alzheimer's disease. Neurobiol Dis 8, 890-899 (2001).
33. M. Sastre, I. Dewachter, G. E. Landreth, T. M. Willson, T. Klockgether, F. van Leuven, and M. T. Heneka, Nonsteroidal anti-inflammatory drugs and peroxisome proliferator-activated receptor-gamma agonists modulate immunostimulated processing of amyloid precursor protein through regulation of beta-secretase. J Neurosci 23, 9796-9804 (2003).
34. M. Tabaton, Oxidative stress and beta-APP proteolytic processing. Neurobiol Aging 25 (S2), S69 (S64-02-03) (2004).
35. E. Tamagno, M. Parola, P. Bardini, A. Piccini, R. Borhi, M. Gugliemotto, G. Santoro, A. Davit, O. Danni, M. A. Smith, G. Perry, M. Tabaton, Beta-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinasses pathways. J Neurochem 92, 628-636 (2005).
36. L. Baum and A. Ng, Curcumin interaction with copper and iron suggests one possible mechanism of action in Alzheimer"s disease animal models. J Alzheimers Dis 6, 367-377; discussion 443-469 (2004).
37. K. B.Suni and R. Kuttan, Effect of oral curcumin administration on serum peroxides and cholesterol levels in human volunteers. Indian J Physiol Pharmacol 36, 273-275 (1992).
38. M. N. Sreejayan Rao, Curcuminoids as potent inhibitors of lipid peroxidation. J Pharm Pharmacol 46(12), 1013-1016 (1994).
39. P. Venkatesanand and M. N. Structure-activity relationships for the inhibition of lipid peroxidation and the scavenging of free radicals by synthetic symmetrical curcumin analogues. J Pharm Pharmacol 52, 1123-1128 (2000).
40. D. Peschel, R. Koerting, and N. Nass, Curcumin induces changes in expression of genes involved in cholesterol homeostasis. J Nutr Biochem (2006).
41. Y. Abe, S. Hashimoto, and T. Horie, Curcumin inhibition of inflammatory cytokine production by human peripheral blood monocytes and alveolar macrophages. Pharmacol Res 39, 41-47 (1999).
42. Y. Jiao, J. T. Wilkinson, E. Christine Pietsch, J. L. Buss, W. Wang, R. Planalp, F. M. Torti, and S. V. Torti, Iron chelation in the biological activity of curcumin. Free Radical Biol Med 40, 1152-1160 (2006).
43. G. Scapagnini, C. Colombrita, M. Amadio, V. D'Agata, E. Arcelli, M. Sapienza, A. Quattrone, and V. Calabrese, Curcumin activates defensive genes and protects neurons against oxidative stress. Antioxid Redox Signal 8, 395-403 (2006).
44. K. Ohtsukaand T. Suzuki, Roles of molecular chaperones in the nervous system. Brain Res Bull 53, 141-146 (2000).
45. C. J. Cummings, Y. Sun, P. Opal, B. Antalffy, R. Mestril, H. T. Orr, W. H. Dillmann, and Y. Zoghbi, Over-expression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum Mol Genet 10, 1511-1518 (2001).
46. K. Kato, H. Ito, K. Kamei, and I. Iwamoto, Stimulation of the stress-induced expression of stress proteins by curcumin in cultured cells and in rat tissues in vivo. Cell Stress Chaperones 3, 152-160 (1998).
47. M. S. Garcia-Alloz, L. Dodwell, A. Borelli, S. Raju, and B J. Backskai, In vivo reduction of plaque size in APPswe/PS1D9 mice treated with curcumin (P4-342). Alzheimer's and Dementia 2(Suppl), S617 (2006).
48. C. Behl, J. Davis, G. M. Cole, and D. Schubert, Vitamin E protects nerve cells from amyloid β-protein toxicity. Biochem Biophys Res Commun 186, 944-950 (1992).
49. C. Behl, J. B. Davis, R. Lesley, and D. Schubert, Hydrogen peroxide mediates amyloid β-protein toxicity. Cell 77, 817-827 (1994).
50. R. E. Mrakand W. S. Griffin, Interleukin-1, neuroinflammation, and Alzheimer's disease. Neurobiol Aging 22, 903-908 (2001).
51. Z. Xie, M. Wei, T. E. Morgan, P. Fabrizio, D. Han, C. E. Finch, and V. D. Longo, Peroxynitrite mediates neurotoxicity of amyloid beta-peptide1-42- and lipopolysaccharide-activated microglia. J Neurosci 22, 3484-3492 (2002).
52. W. Wei, X. Wang, and J. W. Kusiak, Signaling events in amyloid beta-peptide-induced neuronal death and insulin-like growth factor I protection. J Biol Chem 277, 17,649-17,656 (2002).
53. A. M. Minogue, A. W. Schmid, M. P. Fogarty, A. C. Moore, V. A. Campbell, C. E. Herron, and M. A. Lynch, Activation of the c-Jun N-terminal kinase signaling cascade mediates the effect of amyloid-beta on long term potentiation and cell death in hippocampus: A role for interleukin-1beta? J Biol Chem 278, 27,971-27,980 (2003).
54. P. Kuner, R. Schubenel, and C. Hertel, Beta-amyloid binds to p57NTR and activates NFkappaB in human neuroblastoma cells. J Neurosci Res 54, 798-804 (1998).
55. T. C. Gamblin, M. E. King, J. Kuret, R. W. Berry, and L. I. Binder, Oxidative regulation of fatty acid-induced tau polymerization. Biochemistry 39, 14,203-14,210 (2000).
56. X. Zhu, H. G. Lee, A. K. Raina, G. Perry, and M. A. Smith, The role of mitogen-activated protein kinase pathways in Alzheimer's disease, Neurosignals 11, 270-281 (2002).
57. D. C. David, S. Hauptmann, I. Scherping, K. Schuessel, U. Keil, P. Rizzu, R. Ravid, S. Drose, U. Brandt, W. E. Muller, A. Eckert, and J. Gotz, Proteomic and functional analyses reveal a mitochondrial dysfunction in P301L tau transgenic mice. J Biol Chem 280, 23,802-23,814 (2005).
58. V. Chandra, R. Pandav, H. H. Dodge, J. M. Johnston, S. H. Belle, S. T. DeKosky, and M. Ganguli, Incidence of Alzheimer's disease in a rural community in India, the Indo-US study, Neurology 57, 985-989 (2001).
59. R. J. Mehlhornand G. M. Cole, The free radical theory of aging: A critical review. Adv Free Radical Biol Med 1, 165-223 (1985).
60. W. Duan and M P. Mattson, Dietary restriction and 2-deoxyglucose administration improve behavioral outcome and reduce degeneration of dopaminergic neurons in models of Parkinson's disease. J Neurosci Res 57, 195-206 (1999).
61. Y. Zhou, G. Gu, D. R. Goodlett, T. Zhang, C. Pan, T. J. Montine, K. S. Montine, R. H. Aebersold, and J. Zhang,. Analysis of alpha -synuclein-associated proteins by quantitative proteomics, J Biol Chem 279, 39155-39164 (2004).
62. J. S. Hong, Role of inflammation in the pathogenesis of Parkinson's disease: Models, mechanisms, and therapeutic interventions. Ann NY Acad Sci 1053, 151-152 (2005).
63. K. Uéda, H. Fukushima, E. Masliah, Y. Xia, A. Iwai, D. Otero, J. Kondo, Y. Ihara, and T. Saitoh, Molecular cloning of a novel amyloid component in Alzheimer's disease. Proc Natl Acad Sci USA 90, 11,282-11,286 (1993).
64. B. I. Giasson, J. E. Duda, I. V. MurrayQ. Chen, J. M. Souza, H. I. Hurtig, H. Ischiropoulos, J. Q. Trojanowski, and V. M. Lee, Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290, 985-989 (2000).
65. T. Takahashi, H. Yamashita, T. Nakamura, Y. Nagano, and S. Nakamura, Tyrosine 125 of alpha-synuclein plays a critical role for dimerization following nitrative stress. Brain Res 938, 73-80 (2002).
66. K. Onoand M. Yamada, Antioxidant compounds have potent anti-fibrillogenic and fibril-destabilizing effects for alpha-synuclein fibrils in vitro. J Neurochem 97, 105-115 (2006).
67. N. Pandey and J. E. Galvin, Curcumin prevents aggregation of alpha-synuclein. Soc Neurosci 31, abs 1007.9 (2005).
68. B. Caughey, L. D. Raymond, G. J. Raymond, L. Maxson, J. Silveira, and G. S. Baron, Inhibition of protease-resistant prion protein accumulation in vitro by curcumin. J Virol 77, 5499-5502 (2003).
69. N. F. Bence, R. R. Sampat, and R. R. Kopito, Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292, 1552-1555 (2001).
70. C. Zhu, M. A. Hickey, K. Gallant, M. S. Levine, M. F. Chesselet. Differential effects of curcumin and coenzyme Q10 treatment on huntingtin aggregate in CAG 140 knock-in mouse model of Huntington's disease Soc. Neurosci 32, Abs 472.8 (2006).
71. M. Khajavi, K. Inoue, W. Wiszniewski, T. Ohyama, G. J. Snipes, and J. R. Lupski, Curcumin treatment abrogates endoplasmic reticulum retention and aggregation-induced apoptosis associated with neuropathy-causing myelin protein zero-truncating mutants. Am J Hum Genet 77, 841-850 (2005).
72. M Hutton, J. Lewis, D. Dickson, S. H. Yen, and E. McGowan, Analysis of tauopathies with transgenic mice. Trends Mol Med 7, 467-470 (2001).
73. K. Santacruz, J. Lewis, T. Spires, J. Paulson, L. Kotilinek, M. Ingelsson, A. Guimaraes, M. DeTure, M. Ramsden, E. McGowan, C. Forster, M. Yue, J. Orne, C. Janus, A. Mariash, M. Kuskowski, B. Hyman, M/Hutton, and K. H. Ashe, Tau suppression in a neurodegenerative mouse model improves memory function. Science 309, 476-481 (2005).
74. K. Bhattacharya, K. B. Rank, B. D. Evans, and S. K. Sharma, S.K., Role of cysteine-291 and cysteine-322 in the polymerization of human tau into Alzheimer-like filaments. Biochem Biophys Res Commun 285, 20-26 (2001).
75. B. E. Dwyer, A. K. Raina, G. Perry, and M. A. Smith, Homocysteine and Alzheimer's disease: A modifiable risk? Free Radical Biol Med 36, 1471-1475 (2004).
76. G. Ramaswami, H. Chai, Q. Yao, P. H. Lin, A. B. Lumsden, and C. Chen, Curcumin blocks homocysteine-induced endothelial dysfunction in porcine coronary arteries. J Vasc Surg 40, 1216-1222 (2004).
77. J. Chen, X. O. Tang, J. L. Zhi, Y. Cui, H. M. Yu, E. H. Tang, S. N. Sun, J. Q. Feng, nd P. X. Chen, Curcumin protects PC12 cells against 1-methyl-4-phenylpyridinium ion-induced apoptosis by bcl-2-mitochondria-ROS-iNOS pathway. Apoptosis 11, 943-953 (2006).
78. Q. Wang, A. Y. Sun, A. Simonyi, M. D. JensenP.B. Shelat, G. E., Rottinghaus, R. S. MacDonald, D. K. Miller, D. E., Lubahn, G. A. Weisman, and G. Y. Sun, Neuroprotective mechanisms of curcumin against cerebral ischemia-induced neuronal apoptosis and behavioral deficits. J Neurosci Res 82, 138-148 (2005).
79. J. A. Mortimer, C. M. Duijn, V. Chandra, L. Fratiglioni, A. B. Graves, A. Heyman, A. F. Jorm, E. Kokmen, K. Kondo, W. A. Rocca, S. L. Shalat, H. Soininen, and A. Hofman, Head trauma as a risk factor for Alzheimer's disease, A collaborative re-analysis of case-control studies. Int J Epidemiol 20, S28-S35 (1991).
80. J. L. Cummings, JH. V. Vinters, G. M. Cole, and Z. S. Khachaturian, Alzheimer's disease: Etiologies, pathophysiology, cognitive reserve, and treatment opportunities. Neurology 51, S2-17; discussion S65-S17 (1998).
81. H. Wisniewski, H. K. Narang, J. Corsellis, and R. D. Terry, Ultrastructural studies of the neuropil and neurofibrillary tangles in Alzheimer's disease and post-traumatic dementia. J Neuropathol Exp Neurol 35, 367 (1976).
82. S. M. Gentleman, B. D. Greenberg, M. J. Savage, M. Noori, S. J. Newman, G. W. Roberts, S. T. Griffin, and D. Graham, Ab42 is the prominant form of amyloid b-protein in the brains of short-term surviviors of head injury. Neuroreport 8, 1519-1522.
83. J. A. Nicoll, G. W. Roberts, and D. I. Graham, Amyloid beta-protein, APOE genotype and head injury. Ann NY Acad Sci 777, 271-275 (1996).
84. D. H. Smith, M. Nakamura, T. K. McIntosh, J. Wang, A. Rodriguez, X. H. Chen, R. Raghupathi, K. E. Saatman, J. Clemens, M. L. Schmidt, V. M. Lee, and J. Q. Trojanowski, Brain trauma induces massive hippocampal neuron death linked to a surge in beta-amyloid levels in mice overexpressing mutant amyloid precursor protein. Am J Pathol 153, 1005-1010 (1998).
85. A. Wu, Z. Ying, and F. Gomez-Pinilla, Dietary curcumin counteracts the outcome of traumatic brain injury on oxidative stress, synaptic plasticity, and cognition. Exp Neurol 197, 309-317 (2006).
86. V. Rajakrishnan, P. Viswanathan, K. Rajasekharan, and V. Menon, Neuroprotective role of curcumin from Curcuma longa on ethanol-induced brain damage. Phytother Res 13, 571-574 (1999).
87. K. Kitani, T. Yokozawa, and T. Osawa, Interventions in aging and age-associated pathologies by means of nutritional approaches. Ann NY Acad Sci 1019, 424-426 (2004).
88. K. Bala, B. C. Tripathy, and D. Sharma, Neuroprotective and anti-ageing effects of curcumin in aged rat brain regions. Biogerontology 7, 81-89 (2006).
89. G. Kempermann, H. G. Kuhn, and F. H. Gage, More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493-495 (1997).
90. E. K. Ryu, Y. S. Choe, K.-H. Lee, Y. Choi, and B.-T. Kim. Curcumin and dehydrozingerone derivatives: synthesis, radiolabeling, and evaluation for β-amyloid plaque imaging. J Med Chem 49, 6111-6119 (2006).