Neurobiology of Aging
Volume 28, Issue 8 , Pages 1195-1205 , August 2007

Impaired spatial memory in APP-overexpressing mice on a homocysteinemia-inducing diet

  • Alexandra Bernardo

      Affiliations

    • Department of Pharmacology, Vanderbilt University, Nashville, TN 37232-0325, United States
    • Program in Neuroscience, Vanderbilt University, Nashville, TN 37232-0325, United States
  • ,
  • Meghan McCord

      Affiliations

    • Department of Pharmacology, Vanderbilt University, Nashville, TN 37232-0325, United States
  • ,
  • Aron M. Troen

      Affiliations

    • USDA Human Nutrition Research Center on Aging, Tufts University, Boston, MA 02111, United States
  • ,
  • John D. Allison

      Affiliations

    • Program in Neuroscience, Vanderbilt University, Nashville, TN 37232-0325, United States
    • John F. Kennedy Center for Research in Human Development, Vanderbilt University, Nashville, TN 37232-0325, United States
  • ,
  • Michael P. McDonald

      Affiliations

    • Department of Pharmacology, Vanderbilt University, Nashville, TN 37232-0325, United States
    • Program in Neuroscience, Vanderbilt University, Nashville, TN 37232-0325, United States
    • John F. Kennedy Center for Research in Human Development, Vanderbilt University, Nashville, TN 37232-0325, United States
    • Corresponding Author InformationCorresponding author at: Vanderbilt University, 851 Light Hall, Mail Stop #0325, Nashville, TN 37232-0325, United States. Tel.: +1 615 936 1082; fax: +1 615 936 1137.

Received 6 April 2006 ,Revised 19 May 2006 ,Accepted 30 May 2006.

References 

  1. Araki A, Sako Y. Determination of free and total homocysteine in human plasma by high-performance liquid chromatography with fluorescence detection. J Chromatogr. 1987;422:43–52
  2. Blaizot X, Meguro K, Millien I, Baron JC, Chavoix C. Correlations between visual recognition memory and neocortical and hippocampal glucose metabolism after bilateral rhinal cortex lesions in the baboon: implications for Alzheimer's disease. J Neurosci. 2002;22:9166–9170
  3. Bobinski M, Wegiel J, Tarnawski M, Bobinski M, Reisberg B, de Leon MJ, et al. Relationships between regional neuronal loss and neurofibrillary changes in the hippocampal formation and duration and severity of Alzheimer disease. J Neuropathol Exp Neurol. 1997;56:414–420
  4. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, et al. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci. 1999;2:271–276
  5. Chen Z, Karaplis AC, Ackerman SL, Pogribny IP, Melnyk S, Lussier-Cacan S, et al. Mice deficient in methylenetetrahydrofolate reductase exhibit hyperhomocysteinemia and decreased methylation capacity, with neuropathology and aortic lipid deposition. Hum Mol Genet. 2001;10:433–443
  6. Clarke R, Smith AD, Jobst KA, Refsum H, Sutton L, Ueland PM. Folate, vitamin B12, and serum total homocysteine levels in confirmed Alzheimer disease. Arch Neurol. 1998;55:1449–1455
  7. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, et al. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci. 2005;8:79–84
  8. Duan W, Ladenheim B, Cutler RG, Kruman II, Cadet JL, Mattson MP. Dietary folate deficiency and elevated homocysteine levels endanger dopaminergic neurons in models of Parkinson's disease. J Neurochem. 2002;80:101–110
  9. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, et al. Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature. 1995;373:523–527
  10. Gerlai R. Behavioral tests of hippocampal function: simple paradigms complex problems. Behav Brain Res. 2001;125:269–277
  11. Ho L, Purohit D, Haroutunian V, Luterman JD, Willis F, Naslund J, et al. Neuronal cyclooxygenase 2 expression in the hippocampal formation as a function of the clinical progression of Alzheimer disease. Arch Neurol. 2001;58:487–492
  12. Hof PR, Young WG, Bloom FE, Belichenko PV, Celio MR. Comparative cytoarchitectonic atlas of the C57BL6 and 129Sv mouse brains. New York: Elsevier; 2000;
  13. Home DW, Patterson D. Lactobacillus casei microbiological assay of folic acid derivatives in 96-well microtiter plates. Clin Chem. 1988;34:2357–2359
  14. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, et al. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science. 1996;274:99–102
  15. Irizarry MC, Gurol ME, Raju S, Diaz-Arrastia R, Locascio JJ, Tennis M, et al. Association of homocysteine with plasma amyloid beta protein in aging and neurodegenerative disease. Neurology. 2005;65:1402–1408
  16. Jacques PF, Bostom AG, Wilson PW, Rich S, Rosenberg IH, Selhub J. Determinants of plasma total homocysteine concentration in the Framingham offspring cohort. Am J Clin Nutr. 2001;73:613–621
  17. Jarrard LE. Selective hippocampal lesions and behavior: effects of kainic acid lesions on performance of place and cue tasks. Behav Neurosci. 1983;97:873–889
  18. Kruman II, Kumaravel TS, Lohani A, Pedersen WA, Cutler RG, Kruman Y, et al. Folic acid deficiency and homocysteine impair DNA repair in hippocampal neurons and sensitize them to amyloid toxicity in experimental models of Alzheimer's disease. J Neurosci. 2002;22:1752–1762
  19. Kruman II, Mouton PR, Emokpae R, Cutler RG, Mattson MP. Folate deficiency inhibits proliferation of adult hippocampal progenitors. Neuroreport. 2005;16:1055–1059
  20. Lijam N, Paylor R, McDonald MP, Crawley JN, Deng CX, Herrup K, et al. Social interaction and sensorimotor gating abnormalities in mice lacking Dvl1. Cell. 1997;90:895–905
  21. McDonald MP, Crawley JN. Galanin receptor antagonist M40 blocks galanin-induced choice accuracy deficits on a delayed-nonmatching-to-position task. Behav Neurosci. 1996;110:1025–1032
  22. 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
  23. 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
  24. McDonald MP, Overmier JB, Bandyopadhyay S, Babcock D, Cleary J. Reversal of beta-amyloid-induced retention deficit after exposure to training and state cues. Neurobiol Learn Mem. 1996;65:35–47
  25. 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
  26. 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
  27. McDonald RJ, White NM. Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. Behav Neural Biol. 1994;61:260–270
  28. Miller JW. Homocysteine and Alzheimer's disease. Nutr Rev. 1999;57:126–129
  29. Miyakawa T, Yared E, Pak JH, Huang FL, Huang KP, Crawley JN. Neurogranin null mutant mice display performance deficits on spatial learning tasks with anxiety related components. Hippocampus. 2001;11:763–775
  30. Moechars D, Dewachter I, Lorent K, Reverse D, Baekelandt V, Naidu A, et al. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J Biol Chem. 1999;274:6483–6492
  31. Reiserer RS, Harrison FE, Syverud DC, McDonald MP. Impaired spatial learning in the APPSwe+PSEN1ΔE9 bigenic mouse model of Alzheimer's disease.. Genes, Brain Behav. 2007;6:54–65
  32. Roozendaal B, Phillips RG, Power AE, Brooke SM, Sapolsky RM, McGaugh JL. Memory retrieval impairment induced by hippocampal CA3 lesions is blocked by adrenocortical suppression. Nat Neurosci. 2001;4:1169–1171
  33. Sahgal A, Galloway PH, McKeith IG, Lloyd S, Cook JH, Ferrier IN, et al. Matching-to-sample deficits in patients with senile dementias of the Alzheimer and Lewy body types. Arch Neurol. 1992;49:1043–1046
  34. Seshadri S, Beiser A, Selhub J, Jacques PF, Rosenberg IH, D’Agostino RB, et al. Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N Engl J Med. 2002;346:476–483
  35. Steffenach HA, Sloviter RS, Moser El, Moser MB. Impaired retention of spatial memory after transection of longitudinally oriented axons of hippocampal CA3 pyramidal cells. Proc Natl Acad Sci USA. 2002;99:3194–3198
  36. Stubley-Weatherly L, Harding JW, Wright JW. Effects of discrete kainic acid-induced hippocampal lesions on spatial and contextual learning and memory in rats. Brain Res. 1996;716:29–38
  37. Su JH, Deng G, Cotman CW. Transneuronal degeneration in the spread of Alzheimer's disease pathology: immunohistochemical evidence for the transmission of tau hyperphosphorylation. Neurobiol Dis. 1997;4:365–375
  38. 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
  39. Troen A, Rosenberg I. Homocysteine and cognitive function. Semin Vase Med. 2005;5:209–214
  40. Troen AM. The central nervous system in animal models of hyperhomocysteinemia. Prog Neuropsychopharmacol Biol Psychiatry. 2005;29:1140–1151
  41. Troen AM, Lutgens E, Smith DE, Rosenberg IH, Selhub J. The atherogenic effect of excess methionine intake. Proc Natl Acad Sci USA. 2003;100:15089–15094
  42. Vyssotski AL, DeN’Omo G, Poletaeva II, Vyssotsk DL, Minichiello L, Klein R, et al. Long-term monitoring of hippocampus-dependent behavior in naturalistic settings: mutant mice lacking neurotrophin receptor TrkB in the forebrain show spatial learning but impaired behavioral flexibility. Hippocampus. 2002;12:27–38
  43. Wang L, Chen X, Tang B, Hua X, Klein-Szanto A, Kruger WD. Expression of mutant human cystathionine beta-synthase rescues neonatal lethality but not homocystinuria in a mouse model. Hum Mol Genet. 2005;14:2201–2208
  44. Watanabe M, Osada J, Aratani Y, Kluckman K, Reddick R, Malinow MR, et al. Mice deficient in cystathionine beta-synthase: animal models for mild and severe homocyst(e)inemia. Proc Natl Acad Sci USA. 1995;92:1585–1589
  45. Wengenack TM, Whelan S, Curran GL, Duff KE, Poduslo JF. Quantitative histological analysis of amyloid deposition in Alzheimer's double transgenic mouse brain. Neuroscience. 2000;101:939–944
  46. Wolfer DP, Stagljar-Bozicevic M, Errington ML, Lipp HP. Spatial memory and learning in transgenic mice: fact or artifact?. News Physiol Sci. 1998;13:118–123
  47. Yankner BA, Duffy LK, Kirschner DA. Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. Science. 1990;250:279–282

PII: S0197-4580(06)00190-4

doi: 10.1016/j.neurobiolaging.2006.05.035

Neurobiology of Aging
Volume 28, Issue 8 , Pages 1195-1205 , August 2007