Improved spatial learning strategy and memory in aged Alzheimer AβPPswe/PS1dE9 mice on a multi-nutrient diet

Journal of Alzheimer's Disease

Volumn 37, Issue 1, 2013, Pages 233-245

  Wiesmann, Maximilian ^a   Jansen, Diane ^a   Zerbi, Valerio ^a   Broersen, Laus M ^b   Garthe, Alexander ^c   Kiliaan, Amanda J ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b DANONE RESEARCH   (Netherlands)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Alzheimer's disease; cognition; docosahexaenoic acids; learning; memory; transgenic mice

Indexed keywords

ALPHA TOCOPHEROL; AMYLOID PRECURSOR PROTEIN; ASCORBIC ACID; CHOLINE; CYANOCOBALAMIN; DOCOSAHEXAENOIC ACID; FOLIC ACID; ICOSAPENTAENOIC ACID; PHOSPHOLIPID; PYRIDOXINE; SELENIUM; URIDINE PHOSPHATE;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DIET THERAPY; HIPPOCAMPUS; LATENT PERIOD; MALE; MAZE TEST; MEMORY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPATIAL LEARNING; SWIMMING; TASK PERFORMANCE; TRANSGENIC MOUSE; TREATMENT DURATION; WILD TYPE;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; DIET; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; PRESENILIN-1; SPATIAL BEHAVIOR;

EID: 84883199083     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-130179     Document Type: Article

References (69)

1. Mattson MP (2004) Pathways towards and away from Alzheimer's disease. Nature 430, 631-639. (Pubitemid 39061671)
2. Albert MS (1996) Cognitive and neurobiologic markers of early Alzheimer disease. Proc Natl Acad Sci USA 93, 13547-13551. (Pubitemid 26424155)
3. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356. (Pubitemid 34790756)
4. Selkoe DJ (1997) Alzheimer's disease-genotypes, phenotype, and treatments. Science 275, 630-631.
5. Selkoe DJ (2002) Deciphering the genesis and fate of amyloid-protein yields novel therapies for Alzheimer disease. J Clin Invest 110, 1375-1381. (Pubitemid 35396905)
6. Braak H, Braak E (1995) Staging of alzheimer's diseaserelated neurofibrillary changes. Neurobiol Aging 16, 271-278.
7. Braak H, Braak E (1997) Diagnostic criteria for neuropathologic assessment of Alzheimer's disease. Neurobiol Aging 18, S85-S88. (Pubitemid 27454703)
8. Hooijmans CR, Kiliaan AJ (2008) Fatty acids, lipid metabolism and Alzheimer pathology. Eur J Pharmacol 585, 176-196.
9. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K (1985) Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci USA 82, 4245-4249. (Pubitemid 15053619)
10. de la Torre JC (2004) Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 3, 184-190. (Pubitemid 38232669)
11. Fernando MS, Ince PG (2004) Vascular pathologies and cognition in a population-based cohort of elderly people. J Neurol Sci 226, 13-17. (Pubitemid 39505399)
12. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: Lessons from the Alzheimer's amyloid [beta]-peptide. Nat Rev Mol Cell Biol 8, 101-112. (Pubitemid 46432529)
13. Salminen A, Kauppinen A, Suuronen T, Kaarniranta K, Ojala J (2009) ER stress in Alzheimer's disease: A novel neuronal trigger for inflammation and Alzheimer's pathology. J Neuroinflammation 6, 41.
14. Breteler MMB, Claus JJ, Grobbee DE, HofmanA(1994) Cardiovascular disease and distribution of cognitive function in elderly people: The Rotterdam study. BMJ 308, 1604-1608. (Pubitemid 24181869)
15. de la Torre JC, Mussivand T (1993) Can disturbed brain microcirculation cause Alzheimer's disease? Neurol Res 15, 146-153. (Pubitemid 23166998)
16. Hofman A, Ott A, Breteler MMB, Bots ML, Slooter AJC, van Harskamp F, van Duijn CN,Van BroeckhovenC, GrobbeeDE (1997) Atherosclerosis, apolipoprotein E, and prevalence of dementia and Alzheimer's disease in the Rotterdam Study. Lancet 349, 151-154. (Pubitemid 27039193)
17. Hirao K, Ohnishi T, HirataY,Yamashita F, Mori T, Moriguchi Y, Matsuda H, Nemoto K, Imabayashi E,Yamada M, Iwamoto T, Arima K, Asada T (2005) The prediction of rapid conversion to Alzheimer's disease in mild cognitive impairment using regional cerebral blood flow SPECT. NeuroImage 28, 1014-1021. (Pubitemid 41713635)
18. Ruitenberg A, den Heijer T, Bakker SL, van Swieten JC, Koudstaal PJ, Hofman A, Breteler MM (2005) Cerebral hypoperfusion and clinical onset of dementia: The Rotterdam Study. Ann Neurol 57, 789-794. (Pubitemid 40798616)
19. de la Torre JC (2000) Critically attained threshold of cerebral hypoperfusion: The CATCH hypothesis of Alzheimer's pathogenesis. Neurobiol Aging 21, 331-342. (Pubitemid 30387092)
20. Gillette Guyonnet S, Abellan Van Kan G, Andrieu S, Barberger Gateau P, Berr C, BonnefoyM, Dartigues JF, de Groot L, Ferry M, Galan P, Hercberg S, Jeandel C, Morris MC, Nourhashemi F, Payette H, Poulain JP, Portet F, Roussel AM, Ritz P, Rolland Y, Vellas B (2007) IANA task force on nutrition and cognitive decline with aging. J Nutr Health Aging 11, 132-152. (Pubitemid 46725290)
21. Dosunmu R, Wu J, Basha MR, Zawia NH (2007) Environmental and dietary risk factors in Alzheimer's disease. Expert Rev Neurother 7, 887-900. (Pubitemid 47037728)
22. Gardener H, Scarmeas N, Gu Y, Boden-Albala B, Elkind MSV, Sacco RL, DeCarli C, Wright CB (2012) Mediterranean diet and white matter hyperintensity volume in the northern Manhattan study. Arch Neurol 69, 251-256.
23. Scarmeas N, Stern Y, Tang M-X, Mayeux R, Luchsinger JA (2006) Mediterranean diet and risk for Alzheimer's disease. Ann Neurol 59, 912-921. (Pubitemid 43830923)
24. Morris MC, Evans DA, Bienias JL, Scherr PA, Tangney CC, Hebert LE, Bennett DA, Wilson RS, Aggarwal N (2004) Dietary niacin and the risk of incident Alzheimer's disease and of cognitive decline. J Neurol Neurosurg Psychiatry 75, 1093-1099. (Pubitemid 39005762)
25. Kalmijn S, Launer LJ, Ott A, Witteman JCM, Hofman A, Breteler MMB (1997) Dietary fat intake and the risk of incident dementia in the Rotterdam study. Ann Neurol 42, 776-782. (Pubitemid 27481550)
26. Barberger-Gateau P, Raffaitin C, Letenneur L, Berr C, Tzourio C, Dartigues JF, Alperovitch A (2007) Dietary patterns and risk of dementia: The Three-City cohort study. Neurology 69, 1921-1930. (Pubitemid 350100350)
27. Hashimoto M, Hossain S, ShimadaT, ShidoO(2006) Docosahexaenoic acid-induced protective effect against impaired learning in amyloid beta-infused rats is associated with increased synaptosomal membrane fluidity. Clin Exp Pharmacol Physiol 33, 934-939. (Pubitemid 44427316)
28. Cansev M, Wurtman RJ (2007) Chronic administration of docosahexaenoic acid or eicosapentaenoic acid, but not arachidonic acid, alone or in combination with uridine, increases brain phosphatide and synaptic protein levels in gerbils. Neuroscience 148, 421-431. (Pubitemid 47364815)
29. Cansev M, Wurtman RJ, Sakamoto T, Ulus IH (2008) Oral administration of circulating precursors for membrane phosphatides can promote the synthesis of new brain synapses. Alzheimers Dement 4, S153-S168.
30. Wurtman RJ, Ulus IH, Cansev M, Watkins CJ, Wang L, Marzloff G (2006) Synaptic proteins and phospholipids are increased in gerbil brain by administering uridine plus docosahexaenoic acid orally. Brain Res 1088, 83-92. (Pubitemid 43729416)
31. Holguin S, Martinez J, Chow C, Wurtman R (2008) Dietary uridine enhances the improvement in learning and memory produced by administering DHA to gerbils. FASEB J 22, 3938-3946.
32. Sakamoto T, Cansev M, Wurtman RJ (2007) Oral supplementation with docosahexaenoic acid and uridine-5-monophosphate increases dendritic spine density in adult gerbil hippocampus. Brain Res 1182, 50-59.
33. Scheltens P, Kamphuis PJGH, Verhey FRJ, Olde Rikkert MGM, Wurtman RJ, Wilkinson D, Twisk JWR, Kurz A (2010) Efficacy of a medical food in mild Alzheimer's disease: A randomized, controlled trial. Alzheimers Dement 6, 1-10.e11.
34. Scheltens P,Twisk JWR, Blesa R, Scarpini E, von ArnimCAF, Bongers A, Harrison J, Swinkels SHN, Stam CJ, de Waal H, Wurtman RJ, Wieggers RL, Vellas B, Kamphuis PJGH (2012) Efficacy of Souvenaid in mild Alzheimer's disease: Results from a randomized, controlled trial. J Alzheimers Dis 31, 225-236.
35. Nitsch RM, Blusztajn JK, Pittas AG, Slack BE, Growdon JH, Wurtman RJ (1992) Evidence for a membrane defect in Alzheimer disease brain. Proc Natl Acad Sci USA 89, 1671-1675.
36. PettegrewJ, Panchalingam K, Hamilton R, McClure R (2001) Brain membrane phospholipid alterations in Alzheimer's disease. Neurochem Res 26, 771-782. (Pubitemid 32845968)
37. S̈oderberg M, Edlund C, Kristensson K, Dallner G (1991) Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids 26, 421-425.
38. Clarke R, Smith AD, Jobst KA, Refsum H, Sutton L, Ueland PM(1998) Folate, vitamin B12, and serum total homocysteine levels in confirmed Alzheimer disease. Arch Neurol 55, 1449-1455. (Pubitemid 28525506)
39. Rinaldi P, Polidori MC, Metastasio A, Mariani E, Mattioli P, Cherubini A, Catani M, Cecchetti R, Senin U, Mecocci P (2003) Plasma antioxidants are similarly depleted in mild cognitive impairment and in Alzheimer's disease. Neurobiol Aging 24, 915-919. (Pubitemid 36962976)
40. Tully AM, Roche HM, Doyle R, Fallon C, Bruce I, Lawlor B, Coakley D, Gibney MJ (2003) Low serum cholesteryl esterdocosahexaenoic acid levels in Alzheimer's disease: A casecontrol study. Br J Nutr 89, 483-489. (Pubitemid 36582118)
41. Morris RGM (1981) Spatial localization does not require the presence of local cues. Learn Motiv 12, 239-260.
42. JanusC(2004) Search strategies used by APP transgenic mice during navigation in the Morris water maze. Learn Mem 11, 337-346. (Pubitemid 38697900)
43. Balschun D, Wolfer DP, Gass P, Mantamadiotis T, Welzl H, Scḧutz G, Frey JU, Lipp H-P (2003) Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? J Neurosci 23, 6304-6314. (Pubitemid 36875632)
44. Wolfer D, Lipp H (2000) Dissecting the behaviour of transgenic mice: Is it the mutation, the genetic background, or the environment? Exp Physiol 85, 627-634.
45. Brody DL, Holtzman DM (2006) Morris water maze search strategy analysis in PDAPP mice before and after experimental traumatic brain injury. Exp Neurol 197, 330-340. (Pubitemid 43077140)
46. Jankowsky JL, Slunt HH, Ratovitski T, Jenkins NA, Copeland NG, Borchelt DR (2001) Co-expression of multiple transgenes in mouse CNS:Acomparison of strategies. Biomol Eng 17, 157-165. (Pubitemid 32409891)
47. Garthe A, Behr J, Kempermann G (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE 4, e5464.
48. Wolfer DP, Madani R, Valenti P, Lipp H-P (2001) Extended analysis of path data from mutant mice using the public domain software Wintrack. Physiol Behav 73, 745-753. (Pubitemid 32885563)
49. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR (2004) Mutant presenilins specifically elevate the levels of the 42 residue-amyloid peptide in vivo: Evidence for augmentation of a 42-specific-secretase. Hum Mol Genet 13, 159-170.
50. Reeves PG, Nielsen FH, Fahey GC (1993) AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76A rodent diet. J Nutr 123, 1939-1951. (Pubitemid 23342492)
51. Graziano A, Petrosini L, BartolettiA(2003) Automatic recognition of explorative strategies in the Morris water maze. J Neurosci Methods 130, 33-44. (Pubitemid 37315927)
52. Grootendorst J, de Kloet ER, Dalm S, Oitzl MS (2001) Reversal of cognitive deficit of apolipoproteinEknockout mice after repeated exposure to a common environmental experience. Neuroscience 108, 237-247. (Pubitemid 33152965)
53. Lang UE, Lang F, Richter K, Vallon V, Lipp H-P, Schnermann J, Wolfer DP (2003) Emotional instability but intact spatial cognition in adenosine receptor 1 knock out mice. Behav Brain Res 145, 179-188. (Pubitemid 37188643)
54. Sutherland RJ, Whishaw IQ, Regehr JC (1982) Cholinergic receptor blockade impairs spatial localization by use of distal cues in the rat. J Comp Physiol Psychol 96, 563-573.
55. Eichenbaum H, Stewart C, Morris R (1990) Hippocampal representation in place learning. J Neurosci 10, 3531-3542.
56. de Wilde MC, Farkas E, Gerrits M, Kiliaan AJ, Luiten PGM (2002) The effect of n-3 polyunsaturated fatty acid-rich diets on cognitive and cerebrovascular parameters in chronic cerebral hypoperfusion. Brain Res 947, 166-173.
57. Calon F, Lim GP, Yang F, Morihara T, Teter B, Ubeda O, Rostaing P, Triller A, Salem N, Ashe KH, Frautschy SA, Cole GM (2004) Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 43, 633-645. (Pubitemid 39179724)
58. Cole GM, Frautschy SA (2006) Docosahexaenoic acid protects from amyloid and dendritic pathology in an Alzheimer's disease mouse model. Nutr Health 18, 249-259. (Pubitemid 44844123)
59. Hooijmans CR, Van der Zee CEEM, Dederen PJ, Brouwer KM, Reijmer YD, van Groen T, Broersen LM, L̈utjohann D, Heerschap A, Kiliaan AJ (2009) DHA and cholesterol containing diets influence Alzheimer-like pathology, cognition and cerebral vasculature in APPswe/PS1dE9 mice. Neurobiol Dis 33, 482-498.
60. Arendash GW, King DL, Gordon MN, Morgan D, Hatcher JM, Hope CE, Diamond DM (2001) Progressive, age-related behavioral impairments in transgenic mice carrying both mutant amyloid precursor protein and presenilin-1 transgenes. Brain Res 891, 42-53. (Pubitemid 32115494)
61. Jackson PA, Reay JL, Scholey AB,KennedyDO(2012)DHArich oil modulates the cerebral haemodynamic response to cognitive tasks in healthy young adults: A near IR spectroscopy pilot study. Br J Nutr 107, 1093-1098.
62. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298, 789-791. (Pubitemid 35231524)
63. Terry RD (2006) Alzheimer's disease and the aging brain. J Geriatr Psychiatry Neurol 19, 125-128. (Pubitemid 44154851)
64. Broersen LM,Kuipers AAM, Balvers M, vanWijk N, Savelkoul PJM, de Wilde MC, van der Beek EM, Sijben JWC, Hageman RJJ, Kamphuis PJGH, Kiliaan AJ (2012) A Specific multi-nutrient diet reduces Alzheimer-like pathology in young adult A, PPswe/PS1dE9 mice. J Alzheimers Dis 33, 177-190.
65. Hooijmans CR, Van der Zee CE, Dederen PJ, Brouwer KM, Reijmer YD, van Groen T, Broersen LM, Lutjohann D, Heerschap A, Kiliaan AJ (2009) DHA and cholesterol containing diets influence Alzheimer-like pathology, cognition and cerebral vasculature in APPswe/PS1dE9 mice. Neurobiol Dis 33, 482-498.
66. Lalonde R, Kim HD, Fukuchi K (2004) Exploratory activity, anxiety, and motor coordination in bigenic APPswe + PS1/E9 mice. Neurosci Lett 369, 156-161. (Pubitemid 39265419)
67. Lalonde R, Kim HD, Maxwell JA, Fukuchi K (2005) Exploratory activity and spatial learning in 12-month-old APP695SWE/co + PS1/E9 mice with amyloid plaques. Neurosci Lett 390, 87-92. (Pubitemid 41415812)
68. Puoliv̈ali J,Wang J, Heikkinen T, Heikkil̈a M, Tapiola T, van Groen T, Tanila H (2002) Hippocampal Ar42 levels correlate with spatial memory deficit in APP and PS1 double transgenic mice. Neurobiol Dis 9, 339-347. (Pubitemid 34442081)
69. Pugh PL, Richardson JC, Bate ST, Upton N, Sunter D (2007) Non-cognitive behaviours in an APP/PS1 transgenic model of Alzheimer's disease. Behav Brain Res 178, 18-28.