Antioxidants and cognitive training interact to affect oxidative stress and memory in APP/PSEN1 mice

Nutritional Neuroscience

Volumn 12, Issue 5, 2009, Pages 203-218

  Harrison, F E ^a   Allard, J ^a   Bixler, R ^a   Usoh, C ^a   Li, L ^a   May, J M ^a   McDonald, M P ^a,b  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Alzheimer's disease; Cognition; Oxidative stress; Vitamin C; Vitamin E

Indexed keywords

ALPHA TOCOPHEROL; AMYLOID PRECURSOR PROTEIN; ASCORBIC ACID; ISOPROSTANE DERIVATIVE; MALONALDEHYDE; PRESENILIN 2;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; COGNITION; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG MEGADOSE; GENOTYPE; HABITUATION; LEARNING; LIPID PEROXIDATION; LOCOMOTION; MEMORY; MOUSE; NEUROCHEMISTRY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TASK PERFORMANCE; TRANSGENIC MOUSE; VITAMIN SUPPLEMENTATION;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANALYSIS OF VARIANCE; ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; BEHAVIOR, ANIMAL; BRAIN CHEMISTRY; COGNITION; DIET; DISEASE MODELS, ANIMAL; FEMALE; LIVER; MALE; MEMORY; MICE; MICE, TRANSGENIC; OXIDATIVE STRESS; PRESENILIN-1; SENILE PLAQUES; VITAMIN E;

MUS; MUS MUSCULUS;

EID: 71049178586     PISSN: 1028415X     EISSN: 14768305     Source Type: Journal    
DOI: 10.1179/147683009X423364     Document Type: Article

References (84)

1. Tandon A, Rogaeva E, Mullan M, St George-Hyslop PH. Molecular genetics of Alzheimer's disease: the role of beta-amyloid and the presenilins. Curr Opin Neurol 2000; 13: 377-384.
2. Mattson MP. Existing data suggest that Alzheimer's disease is preventable. Ann NY Acad Sci 2000; 924: 153-159.
3. Weih M, Wiltfang J, Kornhuber J. Non-pharmacologic prevention of Alzheimer's disease: nutritional and life-style risk factors. J Neural Transm 2007; 114: 1187-1197.
4. Engelhart MJ, Geerlings MI, Ruitenberg A et al. Dietary intake of antioxidants and risk of Alzheimer disease. JAMA 2002; 287: 3223-3229.
5. Morris MC, Beckett LA, Scherr PA et al. Vitamin E and vitamin C supplement use and risk of incident Alzheimer disease. Alzheimer Dis Assoc Disord 1998; 12: 121-126.
6. Zandi PP, Anthony JC, Khachaturian AS et al. Reduced risk of Alzheimer disease in users of antioxidant vitamin supplements: the Cache County Study. Arch Neurol 2004; 61: 82-88.
7. Fillenbaum GG, Kuchibhatla MN, Hanlon JT et al. Dementia and Alzheimer's disease in community-dwelling elders taking vitamin C and/or vitamin E. Ann Pharmacother 2005; 39: 2009-2014.
8. Laurin D, Masaki KH, Foley DJ, White LR, Launer LJ. Midlife dietary intake of antioxidants and risk of late-life incident dementia: the Honolulu-Asia Aging Study. Am J Epidemiol 2004; 159: 959-967.
9. Luchsinger JA, Tang MX, Shea S, Mayeux R. Antioxidant vitamin intake and risk of Alzheimer disease. Arch Neurol 2003; 60: 203-208.
10. Andersen JK. Oxidative stress in neurodegeneration: cause or consequence? Nat Med 2004; 10 (Suppl): S18-S25.
11. Christen Y. Oxidative stress and Alzheimer disease. Am J Clin Nutr 2000; 71: 621S-629S.
12. Niki E. Interaction of ascorbate and alpha-tocopherol. Ann NY Acad Sci 1987; 498: 186-199.
13. Mohmmad Abdul H, Wenk GL, Gramling M, Hauss-Wegrzyniak B, Butterfield DA. APP and PS-1 mutations induce brain oxidative stress independent of dietary cholesterol: implications for Alzheimer's disease. Neurosci Lett 2004; 368: 148-150.
14. Tamagno E, Guglielmotto M, Aragno M et al. Oxidative stress activates a positive feedback between the gamma- and beta-secretase cleavages of the beta-amyloid precursor protein. J Neurochem 2008; 104: 683-695.
15. Schuessel K, Frey C, Jourdan C et al. Aging sensitizes toward ROS formation and lipid peroxidation in PS1M146L transgenic mice. Free Radic Biol Med 2006; 40: 850-862.
16. Leutner S, Czech C, Schindowski K, Touchet N, Eckert A, Muller WE. Reduced antioxidant enzyme activity in brains of mice transgenic for human presenilin-1 with single or multiple mutations. Neurosci Lett 2000; 292: 87-90.
17. Gibson GE, Zhang H, Sheu KR, Park LC. Differential alterations in antioxidant capacity in cells from Alzheimer patients. Biochim Biophys Acta 2000; 1502: 319-329.
18. Nishida Y, Yokota T, Takahashi T, Uchihara T, Jishage K,Mizusawa H. Deletion of vitamin E enhances phenotype of Alzheimer disease model mouse. Biochem Biophys Res Commun 2006; 350: 530-536.
19. Fukui K, Takatsu H, Shinkai T, Suzuki S, Abe K, Urano S. Appearance of amyloid beta-like substances and delayed-type apoptosis in rat hippocampus CA1 region through aging and oxidative stress. J Alzheimers Dis 2005; 8: 299-309.
20. Mark RJ, Blanc EM, Mattson MP. Amyloid beta-peptide and oxidative cellular injury in Alzheimer's disease. Mol Neurobiol 1996; 12: 211-224.
21. Pappolla MA, Chyan YJ, Omar RA et al. Evidence of oxidative stress and in vivo neurotoxicity of beta-amyloid in a transgenic mouse model of Alzheimer's disease: a chronic oxidative paradigm for testing antioxidant therapies in vivo. Am J Pathol 1998; 152: 871-877.
22. Butterfield DA. Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review. Free Radic Res 2002; 36: 1307-1313.
23. Goodman Y, Mattson MP. Secreted forms of beta-amyloid precursor protein protect hippocampal neurons against amyloid beta-peptide-induced oxidative injury. Exp Neurol 1994; 128: 1-12.
24. Prehn JH, Bindokas VP, Jordan J et al. Protective effect of transforming growth factor-beta 1 on beta-amyloid neurotoxicity in rat hippocampal neurons. Mol Pharmacol 1996; 49: 319-328.
25. Huang J, May JM. Ascorbic acid protects SH-SY5Y neuroblastoma cells from apoptosis and death induced by beta-amyloid. Brain Res 2006; 1097: 52-58.
26. Nicolle MM, Gonzalez J, Sugaya K et al. Signatures of hippocampal oxidative stress in aged spatial learning-impaired rodents. Neuroscience 2001; 107: 415-431.
27. Fukui K, Omoi NO, Hayasaka T et al. Cognitive impairment of rats caused by oxidative stress and aging, and its prevention by vitamin E. Ann NY Acad Sci 2002; 959: 275-284.
28. Joseph JA, Denisova NA, Arendash G et al. Blueberry supplementation enhances signaling and prevents behavioral deficits in an Alzheimer disease model. Nutr Neurosci 2003; 6: 153-162.
29. Lim GP, Chu T, Yang F, Beech W, Frautschy SA, Cole GM. The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J Neurosci 2001; 21: 8370-8377.
30. Conte V, Uryu K, Fujimoto S et al. Vitamin E reduces amyloidosis and improves cognitive function in Tg2576 mice following repetitive concussive brain injury. J Neurochem 2004; 90: 758-764.
31. Joseph JA, Shukitt-Hale B, Denisova NA et al. Long-term dietary strawberry, spinach, or vitamin E supplementation retards the onset of age-related neuronal signal-transduction and cognitive behavioral deficits. J Neurosci 1998; 18: 8047-8055.
32. Kolosova NG, Shcheglova TV, Sergeeva SV, Loskutova LV. Longterm antioxidant supplementation attenuates oxidative stress markers and cognitive deficits in senescent-accelerated OXYS rats. Neurobiol Aging 2006; 27: 1289-1297.
33. Navarro A, Gomez C, Sanchez-Pino MJ et al. Vitamin E at high doses improves survival, neurological performance, and brain mitochondrial function in aging male mice. Am J Physiol 2005; 289: R1392-R1399.
34. Veinbergs I, Mallory M, Sagara Y, Masliah E. Vitamin E supplementation prevents spatial learning deficits and dendritic alterations in aged apolipoprotein E-deficient mice. Eur J Neurosci 2000; 12: 4541-4546.
35. Price DL, Wong PC, Markowska AL et al. The value of transgenic models for the study of neurodegenerative diseases. Ann NY Acad Sci 2000; 920: 179-191.
36. Reiserer RS, Harrison FE, Syverud DC, McDonald MP. Impaired spatial learning in the APPSwe + PSEN1DeltaE9 bigenic mouse model of Alzheimer's disease. Genes Brain Behav 2007; 6: 54-65.
37. Bernardo A, Harrison FE, McCord M et al. Elimination of GD3 synthase improves memory and reduces amyloid-beta plaque load in transgenic mice. Neurobiol Aging 2008; Epub ahead of print.
38. Lalonde R, Kim HD, Maxwell JA, Fukuchi K. Exploratory activity and spatial learning in 12-month-old APP(695)SWE/ co+PS1/DeltaE9 mice with amyloid plaques. Neurosci Lett 2005; 390: 87-92.
39. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX et al. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 2006; 24: 516-524. (Pubitemid 44716680)
40. Miyakawa T, Yamada M, Duttaroy A, Wess J. Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. J Neurosci 2001; 21: 5239-5250.
41. McDonald MP, Wong R, Goldstein G, Weintraub B, Cheng SY, Crawley JN. Hyperactivity and learning deficits in transgenic mice bearing a human mutant thyroid hormone beta1 receptor gene. Learn Mem 1998; 5: 289-301.
42. Siesser WB, Cheng SY, McDonald MP. Hyperactivity, impaired learning on a vigilance task, and a differential response to methylphenidate in the TRbetaPV knock-in mouse. Psychopharmacology (Berl) 2005; 181: 653-663.
43. Harrison FE, Yu SS, Van Den Bossche KL, Li L, May JM, McDonald MP. Elevated oxidative stress and sensorimotor deficits but normal cognition in mice that cannot synthesize ascorbic acid. J Neurochem 2008; 106: 1198-1208.
44. Platel A, Porsolt RD. Habituation of exploratory activity in mice: a screening test for memory enhancing drugs. Psychopharmacology (Berl) 1982; 78: 346-352.
45. Bernardo A, McCord M, Troen AM, Allison JD, McDonald MP. Impaired spatial memory in APP-overexpressing mice on a homocysteinemia-inducing diet. Neurobiol Aging 2007; 28: 1195-1205.
46. McDonald MP, Willard LB, Wenk GL, Crawley JN. Coadministration of galanin antagonist M40 with a muscarinic M1 agonist improves delayed nonmatching to position choice accuracy in rats with cholinergic lesions. J Neurosci 1998; 18: 5078-5085.
47. McDonald MP, Wenk GL, Crawley JN. Analysis of galanin and the galanin antagonist M40 on delayed non-matching-to-position performance in rats lesioned with the cholinergic immunotoxin 192 IgG-saporin. Behav Neurosci 1997; 111: 552-563.
48. McDonald MP, Crawley JN. Galanin receptor antagonist M40 blocks galanin-induced choice accuracy deficits on a delayednonmatching- to-position task. Behav Neurosci 1996; 110: 1025-1032.
49. Lalonde R. The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev 2002; 26: 91-104.
50. McDonald MP, Overmier JB. Present imperfect: a critical review of animal models of the mnemonic impairments in Alzheimer's disease. Neurosci Biobehav Rev 1998; 22: 99-120.
51. Miyakawa T, Yared E, Pak JH, Huang FL, Huang KP, Crawley JN. Neurogranin null mutant mice display performance deficits onspatial learning tasks with anxiety related components. Hippocampus 2001; 11: 763-775.
52. Pachla LA, Kissinger PT. Analysis of ascorbic acid by liquid chromatography with amperometric detection. Methods Enzymol 1979; 62: 15-24.
53. May JM, Qu ZC, Mendiratta S. Protection and recycling of alphatocopherol in human erythrocytes by intracellular ascorbic acid. Arch Biochem Biophys 1998; 349: 281-289.
54. Lang JK, Gohil K, Packer L. Simultaneous determination of tocopherols, ubiquinols, and ubiquinones in blood, plasma, tissue homogenates, and subcellular fractions. Anal Biochem 1986; 157: 106-116.
55. Roberts 2nd LJ, Montine TJ, Markesbery WR et al. Formation of isoprostane-like compounds (neuroprostanes) in vivo from docosahexaenoic acid. J Biol Chem 1998; 273: 13605-13612.
56. Sabharwal AK, May JM. alpha-Lipoic acid and ascorbate prevent LDL oxidation and oxidant stress in endothelial cells. Mol Cell Biochem 2008; 309: 125-132.
57. Casado A, Encarnacion Lopez-Fernandez M, Concepcion Casado M, de La Torre R. Lipid peroxidation and antioxidant enzyme activities in vascular and Alzheimer dementias. Neurochem Res 2008; 33: 450-458.
58. Savonenko A, Xu GM, Melnikova T et al. Episodic-like memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: relationships to beta-amyloid deposition and neurotransmitter abnormalities. Neurobiol Dis 2005; 18: 602-617.
59. Ding Y, Qiao A, Wang Z et al. Retinoic acid attenuates beta-amyloid deposition and rescues memory deficits in an Alzheimer's disease transgenic mouse model. J Neurosci 2008; 28: 11622-11634.
60. Agus DB, Gambhir SS, Pardridge WM et al. Vitamin C crosses the blood-brain barrier in the oxidized form through the glucose transporters. J Clin Invest 1997; 100: 2842-2848.
61. Socci DJ, Crandall BM, Arendash GW. Chronic antioxidant treatment improves the cognitive performance of aged rats. Brain Res 1995; 693: 88-94.
62. Sumien N, Forster MJ, Sohal RS. Supplementation with vitamin E fails to attenuate oxidative damage in aged mice. Exp Gerontol 2003; 38: 699-704.
63. Padayatty SJ, Katz A, Wang Y et al. Vitamin C as an antioxidant: evaluation of its role in disease prevention. J Am Coll Nutr 2003; 22: 18-35.
64. Harats D, Chevion S, Nahir M, Norman Y, Sagee O, Berry EM. Citrus fruit supplementation reduces lipoprotein oxidation in young men ingesting a diet high in saturated fat: presumptive evidence for an interaction between vitamins C and E in vivo. Am J Clin Nutr 1998; 67: 240-245.
65. Upston JM, Terentis AC, Stocker R. Tocopherol-mediated peroxidation of lipoproteins: implications for vitamin E as a potential antiatherogenic supplement. FASEB J 1999; 13: 977-994.
66. Sumien N, Heinrich KR, Sohal RS, Forster MJ. Short-term vitamin E intake fails to improve cognitive or psychomotor performance of aged mice. Free Radic Biol Med 2004; 36: 1424-1433.
67. Halagappa VK, Guo Z, Pearson M et al. Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer's disease. Neurobiol Dis 2007; 26: 212-220.
68. Hashimoto T, Watanabe S. Chronic food restriction enhances memory in mice-analysis with matched drive levels. Neuroreport 2005; 16: 1129-1133.
69. Ward WF, Qi W, Van Remmen H, Zackert WE, Roberts 2nd LJ, Richardson A. Effects of age and caloric restriction on lipid peroxidation: measurement of oxidative stress by F2-isoprostane levels. J Gerontol A Biol Sci Med Sci 2005; 60: 847-851.
70. Arendash GW, Garcia MF, Costa DA, Cracchiolo JR, Wefes IM, Potter H. Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable beta-amyloid deposition. Neuroreport 2004; 15: 1751-1754.
71. Costa DA, Cracchiolo JR, Bachstetter AD et al. Enrichment improves cognition in AD mice by amyloid-related and unrelated mechanisms. Neurobiol Aging 2007; 28: 831-844.
72. Jankowsky JL, Melnikova T, Fadale DJ et al. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J Neurosci 2005; 25: 5217-5224.
73. Hong JH, Kim MJ, Park MR et al. Effects of vitamin E on oxidative stress and membrane fluidity in brain of streptozotocin-induced diabetic rats. Clin Chim Acta 2004; 340: 107-115.
74. Omoi NO, Arai M, Saito M et al. Influence of oxidative stress on fusion of pre-synaptic plasma membranes of the rat brain with phosphatidyl choline liposomes, and protective effect of vitamin E. J Nutr Sci Vitaminol (Tokyo) 2006; 52: 248-255.
75. Castellani RJ, Lee HG, Zhu X, Nunomura A, Perry G, Smith MA. Neuropathology of Alzheimer disease: pathognomonic but not pathogenic. Acta Neuropathol 2006; 111: 503-509.
76. Lee HG, Zhu X, Castellani RJ, Nunomura A, Perry G, Smith MA. Amyloid-beta in Alzheimer disease: the null versus the alternate hypotheses. J Pharmacol Exp Ther 2007; 321: 823-829.
77. Fotuhi M, Zandi PP, Hayden KM et al. Better cognitive performance in elderly taking antioxidant vitamins E and C supplements in combination with nonsteroidal anti-inflammatory drugs: the Cache County Study. Alzheimers Dement 2008; 4: 223-227.
78. Wilder J. Stimulus and Response: The Law Of Initial Value. Bristol: Wright, 1967.
79. McDonald SR, Sohal RS, Forster MJ. Concurrent administration of coenzyme Q10 and alpha-tocopherol improves learning in aged mice. Free Radic Biol Med 2005; 38: 729-736.
80. Stackman RW, Eckenstein F, Frei B, Kulhanek D, Nowlin J, Quinn JF. Prevention of age-related spatial memory deficits in a transgenic mouse model of Alzheimer's disease by chronic Ginkgo biloba treatment. Exp Neurol 2003; 184: 510-520.
81. Jensen MT, Mottin MD, Cracchiolo JR, Leighty RE, Arendash GW. Lifelong immunization with human beta-amyloid (1-42) protects Alzheimer's transgenic mice against cognitive impairment throughout aging. Neuroscience 2005; 130: 667-684.
82. Leighty RE, Nilsson LN, Potter H et al. Use of multimetric statistical analysis to characterize and discriminate between the performance of four Alzheimer's transgenic mouse lines differing in Abeta deposition. Behav Brain Res 2004; 153: 107-121.
83. McDonald MP, Dahl EE, Overmier JB, Mantyh P, Cleary J. Effects of an exogenous beta-amyloid peptide on retention for spatial learning. Behav Neural Biol 1994; 62: 60-67.
84. Sweeney WA, Luedtke J, McDonald MP, Overmier JB. Intrahippocampal injections of exogenous beta-amyloid induce postdelay errors in an eight-arm radial maze. Neurobiol Learn Mem 1997; 68: 97-101.