Vitamin C reduces spatial learning deficits in middle-aged and very old APP/PSEN1 transgenic and wild-type mice

Pharmacology Biochemistry and Behavior

Volumn 93, Issue 4, 2009, Pages 443-450

  Harrison, F E ^a   Hosseini, A H ^b   McDonald, M P ^c   May, J M ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

Acetylcholinesterase; Aging; Alzheimer's disease; Amyloid ; APP PSEN1; Ascorbic acid; Cognition; Oxidative stress; Vitamin C

Indexed keywords

ACETYLCHOLINESTERASE; AMYLOID BETA PROTEIN; ASCORBIC ACID;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLINERGIC SYSTEM; COGNITION; CONTROLLED STUDY; DATA ANALYSIS; DEGENERATIVE DISEASE; DISEASE MODEL; DRUG EFFECT; DRUG MECHANISM; DRUG MEGADOSE; ENZYME ACTIVITY; LEARNING DISORDER; MAZE TEST; MENTAL TASK; MIDDLE AGED; MOUSE; NEUROTRANSMISSION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SENILE PLAQUE; SHORT COURSE THERAPY; SWIMMING; TRANSGENIC MOUSE; VERY ELDERLY; WILD TYPE;

ACETYLCHOLINESTERASE; AGING; AMYLOID BETA-PEPTIDES; ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; BRAIN CHEMISTRY; MALONDIALDEHYDE; MAZE LEARNING; MICE; MICE, TRANSGENIC; OXIDATIVE STRESS; PRESENILIN-1;

MUS;

EID: 67849132395     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2009.06.006     Document Type: Article

References (50)

1. Alzheimer's Association. Alzheimer's disease facts and figures. Alzheimers Dement 4 (2008) 110-133
2. Agus D.B., Gambhir S.S., Pardridge W.M., Spielholz C., Baselga J., Vera J.C., et al. Vitamin C crosses the blood-brain barrier in the oxidized form through the glucose transporters. J Clin Invest 100 (1997) 2842-2848
3. Arzi A., Hemmati A.A., and Razian A. Effect of vitamins C and E on cognitive function in mouse. Pharmacol Res 49 (2004) 249-252
4. Bernardo A., Harrison F.E., McCord M., Zhao J., Bruchey A., Davies S.S., et al. Elimination of GD3 synthase improves memory and reduces amyloid-beta plaque load in transgenic mice. Neurobiol Aging (2008) 10.1016/j.neurobiolaging.2007.12.022
5. Bernardo A., McCord M., Troen A.M., Allison J.D., and McDonald M.P. Impaired spatial memory in APP- overexpressing mice on a homocysteinemia-inducing diet. Neurobiol Aging 28 (2007) 1195-1205
6. Burk R.F., Christensen J.M., Maguire M.J., Austin L.M., Whetsell Jr. W.O., May J.M., et al. A combined deficiency of vitamins E and C causes severe central nervous system damage in guinea pigs. J Nutr 136 (2006) 1576-1581
7. Cammack J., Ghasemzadeh B., and Adams R.N. The pharmacological profile of glutamate-evoked ascorbic acid efflux measured by in vivo electrochemistry. Brain Res 565 (1991) 17-22
8. Charlton K.E., Rabinowitz T.L., Geffen L.N., and Dhansay M.A. Lowered plasma vitamin C, but not vitamin E, concentrations in dementia patients. J Nutr Health Aging 8 (2004) 99-107
9. Chen Q., Espey M.G., Sun A.Y., Lee J.H., Krishna M.C., Shacter E., et al. Ascorbate in pharmacologic concentrations selectively generates ascorbate radical and hydrogen peroxide in extracellular fluid in vivo. Proc Natl Acad Sci U S A 104 (2007) 8749-8754
10. Christen Y. Oxidative stress and Alzheimer disease. Am J Clin Nutr 71 (2000) 621S-629S
11. de Angelis L., and Furlan C. The effects of ascorbic acid and oxiracetam on scopolamine-induced amnesia in a habituation test in aged mice. Neurobiol Learn Mem 64 (1995) 119-124
12. Dhingra D., Parle M., and Kulkarni S.K. Comparative brain cholinesterase-inhibiting activity of Glycyrrhiza glabra, Myristica fragrans, ascorbic acid, and metrifonate in mice. J Med Food 9 (2006) 281-283
13. Ellman G.L., Courtney K.D., Andres Jr. V., and Feather-Stone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7 (1961) 88-95
14. Engelhart M.J., Geerlings M.I., Ruitenberg A., van Swieten J.C., Hofman A., Witteman J.C., et al. Dietary intake of antioxidants and risk of Alzheimer disease. JAMA 287 (2002) 3223-3229
15. Gallagher M., Burwell R., and Burchinal M. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav Neurosci 107 (1993) 618-626
16. Gallagher M., and Rapp P.R. The use of animal models to study the effects of aging on cognition. Annu Rev Psychol 48 (1997) 339-370
17. Garcia-Alloza M., Robbins E.M., Zhang-Nunes S.X., Purcell S.M., Betensky R.A., Raju S., et al. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24 (2006) 516-524
18. Harman D. The aging process. Proc Natl Acad Sci U S A 78 (1981) 7124-7128
19. Harrison F.E., Yu S.S., Van Den Bossche K.L., Li L., May J.M., and McDonald M.P. Elevated oxidative stress and sensorimotor deficits but normal cognition in mice that cannot synthesize ascorbic acid. J Neurochem 106 (2008) 1198-1208
20. Hodges R.E., Hood J., Canham J.E., Sauberlich H.E., and Baker E.M. Clinical manifestations of ascorbic acid deficiency in man. Am J Clin Nutr 24 (1971) 432-443
21. Joseph J.A., Denisova N.A., Arendash G., Gordon M., Diamond D., Shukitt-Hale B., et al. Blueberry supplementation enhances signaling and prevents behavioral deficits in an Alzheimer disease model. Nutr Neurosci 6 (2003) 153-162
22. Keppel G. Design and analysis : a researcher's handbook. Englewood Cliffs, N.J.: Prentice Hall, 1991.
23. Kim H.K., Kim M., Kim S., Kim M., and Chung J.H. Effects of green tea polyphenol on cognitive and acetylcholinesterase activities. Biosci Biotechnol Biochem 68 (2004) 1977-1979
24. Lalonde R., Kim H.D., Maxwell J.A., and Fukuchi K. Exploratory activity and spatial learning in 12-month-old APP(695)SWE/co+PS1/DeltaE9 mice with amyloid plaques. Neurosci Lett 390 (2005) 87-92
25. Lee L., Kang S.A., Lee H.O., Lee B.H., Jung I.K., Lee J.E., et al. Effect of supplementation of vitamin E and vitamin C on brain acetylcholinesterase activity and neurotransmitter levels in rats treated with scopolamine, an inducer of dementia. J Nutr Sci Vitaminol 47 (2001) 323-328
26. Lykkesfeldt J., and Moos T. Age-dependent change in Vitamin C status: a phenomenon of maturation rather than of ageing. Mech Ageing Dev 126 (2005) 892-898
27. Lykkesfeldt J., Trueba G.P., Poulsen H.E., and Christen S. Vitamin C deficiency in weanling guinea pigs: differential expression of oxidative stress and DNA repair in liver and brain. Br J Nutr 98 (2007) 1116-1119
28. Machova E., Jakubik J., Michal P., Oksman M., Iivonen H., Tanila H., et al. Impairment of muscarinic transmission in transgenic APPswe/PS1dE9 mice. Neurobiol Aging 29 (2008) 368-378
29. May J.M., Qu Z.C., and Mendiratta S. Protection and recycling of alpha-tocopherol in human erythrocytes by intracellular ascorbic acid. Arch Biochem Biophys 349 (1998) 281-289
30. McDonald M.P., Dahl E.E., Overmier J.B., Mantyh P., and Cleary J. Effects of an exogenous beta-amyloid peptide on retention for spatial learning. Behav Neural Biol 62 (1994) 60-67
31. Miyakawa T., Yared E., Pak J.H., Huang F.L., Huang K.P., and Crawley J.N. Neurogranin null mutant mice display performance deficits on spatial learning tasks with anxiety related components. Hippocampus 11 (2001) 763-775
32. Morris M.C., Beckett L.A., Scherr P.A., Hebert L.E., Bennett D.A., Field T.S., et al. Vitamin E and vitamin C supplement use and risk of incident Alzheimer disease. Alzheimer Dis Assoc Disord 12 (1998) 121-126
33. Morse C.K. Does variability increase with age? An archival study of cognitive measures. Psychol Aging 8 (1993) 156-164
34. O'Neill R.D., Fillenz M., Sundstrom L., and Rawlins J.N. Voltammetrically monitored brain ascorbate as an index of excitatory amino acid release in the unrestrained rat. Neurosci Lett 52 (1984) 227-233
35. Pachla L.A., and Kissinger P.T. Analysis of ascorbic acid by liquid chromatography with amperometric detection. Methods Enzymol 62 (1979) 15-24
36. Parle M., and Dhingra D. Ascorbic Acid: a promising memory-enhancer in mice. J Pharmacol Sci 93 (2003) 129-135
37. Pettenuzzo L.F., Schuck P.F., Fontella F., Wannmacher C.M., Wyse A.T., Dutra-Filho C.S., et al. Ascorbic acid prevents cognitive deficits caused by chronic administration of propionic acid to rats in the water maze. Pharmacol Biochem Behav 73 (2002) 623-629
38. Pierce R.C., and Rebec G.V. Intraneostriatal administration of glutamate antagonists increases behavioral activation and decreases neostriatal ascorbate via nondopaminergic mechanisms. J Neurosci 13 (1993) 4272-4280
39. Reiserer R.S., Harrison F.E., Syverud D.C., and McDonald M.P. Impaired spatial learning in the APPSwe + PSEN1DeltaE9 bigenic mouse model of Alzheimer's disease. Genes Brain Behav 6 (2007) 54-65
40. Rikans L.E., and Moore D.R. Effect of aging on aqueous-phase antioxidants in tissues of male Fischer rats. Biochim Biophys Acta 966 (1988) 269-275
41. Riviere S., Birlouez-Aragon I., Nourhashemi F., and Vellas B. Low plasma vitamin C in Alzheimer patients despite an adequate diet. Int J Geriatr Psychiatry 13 (1998) 749-754
42. Sabharwal A.K., and May J.M. alpha-Lipoic acid and ascorbate prevent LDL oxidation and oxidant stress in endothelial cells. Mol Cell Biochem 309 (2008) 125-132
43. Savonenko A., Xu G.M., Melnikova T., Morton J.L., Gonzales V., Wong M.P., 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 18 (2005) 602-617
44. Shah R.S., Lee H.G., Xiongwei Z., Perry G., Smith M.A., and Castellani R.J. Current approaches in the treatment of Alzheimer's disease. Biomed Pharmacother 62 (2008) 199-207
45. Shahidi S., Komaki A., Mahmoodi M., Atrvash N., and Ghodrati M. Ascorbic acid supplementation could affect passive avoidance learning and memory in rat. Brain Res Bull 76 (2008) 109-113
46. Sotiriou S., Gispert S., Cheng J., Wang Y., Chen A., Hoogstraten-Miller S., et al. Ascorbic-acid transporter Slc23a1 is essential for vitamin C transport into the brain and for perinatal survival. Nat Med 8 (2002) 514-517
47. Trinh N.H., Hoblyn J., Mohanty S., and Yaffe K. Efficacy of cholinesterase inhibitors in the treatment of neuropsychiatric symptoms and functional impairment in Alzheimer disease: a meta-analysis. JAMA 289 (2003) 210-216
48. Tsukaguchi H., Tokui T., Mackenzie B., Berger U.V., Chen X.Z., Wang Y., et al. A family of mammalian Na+-dependent L-ascorbic acid transporters. Nature 399 (1999) 70-75
49. Tsunekawa H., Noda Y., Mouri A., Yoneda F., and Nabeshima T. Synergistic effects of selegiline and donepezil on cognitive impairment induced by amyloid beta (25-35). Behav Brain Res 190 (2008) 224-232
50. Wilder J. Stimulus and Response: the law of initial value (1967), Wright, Bristol, England