The cognitive impact of nutritional homocysteinemia in Apolipoprotein-E deficient mice

Journal of Alzheimer's Disease

Volumn 9, Issue 4, 2006, Pages 381-392

  Troen, Aron M ^a   Shukitt Hale, Barbara ^a   Chao, Wei Hsun ^a   Albuquerque, Bina ^a   Smith, Donald E ^a   Selhub, Jacob ^a   Rosenberg, Irwin H ^a,b  

^a TUFTS UNIVERSITY   (United States)

^b NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

ApoE; Behavior; Cognition; Dementia; Folate; Homocysteine; Methionine; Model; Neurodegeneration; Nutrition

Indexed keywords

APOLIPOPROTEIN E; CYANOCOBALAMIN; FOLIC ACID; HOMOCYSTEINE; METHIONINE; PYRIDOXINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAGE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ASSOCIATION; HISTOLOGY; HOMOCYSTEINE BLOOD LEVEL; HYPERLIPOPROTEINEMIA TYPE 3; LEARNING; MALE; MAZE TEST; METABOLIC DISORDER; METHYLATION; MOUSE; NERVE DEGENERATION; NONHUMAN; NUTRITIONAL SUPPORT; PRIORITY JOURNAL; PSYCHOMOTOR PERFORMANCE; SPATIAL MEMORY; VITAMIN DEFICIENCY;

EID: 33747397304     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2006-9403     Document Type: Article

References (80)

1. B. Akesson, C. Fehling, M. Jagerstad and U. Stenram, Effect of experimental folate deficiency on lipid metabolism in liver and brain, Br J Nutr 47 (1982), 505-520.
2. R. Anderson and G.A. Higgins, Absence of central cholinergic deficits in ApoE knockout mice, Psychopharmacology (Berl) 132 (1997), 135-144.
3. R. Anderson, J.C. Barnes, T.V. Bliss, D.P. Cain, K. Cambon, H.A. Davies, M.L. Errington, L.A. Fellows, R.A. Gray, T. Hoh, M. Stewart, C.H. Large and G.A. Higgins, Behavioural, physiological and morphological analysis of a line of apolipoprotein E knockout mouse, Neuroscience 85 (1998), 93-110.
4. T. Bottiglieri, Folate, vitamin B12, and neuropsychiatric disorders, Nutr Rev 54 (1996), 382-390.
5. M. Buttini, M. Orth, S. Bellosta, H. Akeefe, R.E. Pitas, T. Wyss-Coray, L. Mucke and R.W. Mahley, Expression of human apolipoprotein E3 or E4 in the brains of Apoe-/- mice: isoform-specific effects on neurodegeneration, J Neurosci 19 (1999), 4867-4880.
6. G. Casadesus, B. Shukitt-Hale and J.A. Joseph, Automated measurement of age-related changes in the locomotor response to environmental novelty and home-cage activity, Mech Ageing Dev 122 (2001), 1887-1897.
7. D. Champagne, J.B. Dupuy, J. Rochford and J. Poirier, Apolipoprotein E knockout mice display procedural deficits in the Morris water maze: analysis of learning strategies in three versions of the task, Neuroscience 114 (2002), 641-654.
8. Y. Chen, L. Lomnitski, D.M. Michaelson and E. Shohami, Motor and cognitive deficits in apolipoprotein E-deficient mice after closed head injury, Neuroscience 80 (1997), 1255-1262.
9. L.A. Christie, G. Riedel, S.A. Algaidi, L.J. Whalley and B. Platt, Enhanced hippocampal long-term potentiation in rats after chronic exposure to homocysteine, Neurosci Lett 373 (2005), 119-124.
10. J.N. Crawley, Behavioral phenotyping of rodents, Comp Med 53 (2003), 140-146.
11. S. Dayal, A.M. Devlin, R.B. McCaw, M.L. Liu, E. Arning, T. Bottiglieri, B. Shane, F.M. Faraci and S.R. Lentz, Cerebral vascular dysfunction in methionine synthase-deficient mice, Circulation 112 (2005), 737-744.
12. W. Duan, B. Ladenheim, R.G. Cutler, I.I. Kruman, J.L. Cadet and M.P. Mattson, Dietary folate deficiency and elevated homocysteine levels endanger dopaminergic neurons in models of Parkinson's disease, J Neurochem 80 (2002), 101-110.
13. C. Dufouil, A. Alperovitch, V. Ducros and C. Tzourio, Homocysteine, white matter hyperintensities, and cognition in healthy elderly people, Ann Neurol 53 (2003), 214-221.
14. S.J. Duthie, L.J. Whalley, A.R. Collins, S. Leaper, K. Berger and I.J. Deary, Homocysteine, B vitamin status, and cognitive function in the elderly, Am J Clin Nutr 75 (2002), 908-913.
15. L.F. Eng and R.S. Ghirnikar, GFAP and astrogliosis, Brain Pathol 4 (1994), 229-237.
16. A. Fisher, R. Brandeis, S. Chapman, Z. Pittel and D.M. Michaelson, M1 muscarinic agonist treatment reverses cognitive and cholinergic impairments of apolipoprotein E-deficient mice, J Neurochem 70 (1998), 1991-1997.
17. M. Gallagher and M.M. Nicolle, Animal models of normal aging: relationship between cognitive decline and markers in hippocampal circuitry, Behav Brain Res 57 (1993), 155-162.
18. A. Garcia, Y. Haron, K. Pulman, L. Hua and M. Freedman, Increases in homocysteine are related to worsening of stroop scores in healthy elderly persons: a prospective follow-up study, J Gerontol A Biol Sci Med Sci 59 (2004), 1323-1327.
19. I. Genis, I. Gordon, E. Sehayek and D.M. Michaelson, Phosphorylation of tau in apolipoprotein E-deficient mice, Neurosci Lett 199 (1995), 5-8.
20. I. Genis, A. Fisher, E. Shohami and D.M. Michaelson, Modulation of Tau Hyperphosphorylation in apoE-deficient Mice by Muscarinic Activation and Closed Head Injury, in: Alzhemer's Disease and Related Disorders: Etiology, Pathogenesis and Therapeutics, H.M. Wisniewski, ed., John Wiley & Sons Ltd., Chichester, England, 1999, pp. 733-740.
21. L. Genis, Y. Chen, E. Shohami and D.M. Michaelson, Tau hyperphosphorylation in apolipoprotein E-deficient and control mice after closed head injury, J Neurosci Res 60 (2000), 559-564.
22. I. Gordon, E. Grauer, I. Genis, E. Sehayek and D.M. Michaelson, Memory deficits and cholinergic impairments in apolipoprotein E-deficient mice, Neurosci Lett 199 (1995), 1-4.
23. I. Gordon, I. Genis, E. Grauer, E. Sehayek and D.M. Michaelson, Biochemical and cognitive studies of apolipoprotein-E-deficient mice, Mol Chem Neuropathol 28 (1996), 97-103.
24. S.M. Gospe, D.W. Gietzen, P.J. Summers, J.M. Lunetta, J.W. Miller, J. Selhub, W.G. Ellis and A.J. Clifford, Behavioral and neurochemical changes in folate-deficient mice, Physiology & Behavior 58 (1995), 000.
25. N. Groome, A. Dawkes, R. Barry, S. Hruby and E.J. Alvord, New monoclonal antibodies reactive with defined sequential epitopes in human myelin basic protein, J Neuroimmunol 19 (1988), 305-315.
26. G.M. Halliday, K.M. Cullen, J.J. Kril, A.J. Harding and J. Harasty, Glial fibrillary acidic protein (GFAP) immunohistochemistry in human cortex: a quantitative study using different antisera, Neurosci Lett 209 (1996), 29-32.
27. S.H. Han and S.Y. Chung, Marked hippocampal neuronal damage without motor deficits after mild concussive-like brain injury in apolipoprotein E-deficient mice, Ann N Y Acad Sci 903 (2000), 357-365.
28. Y. Higuchi, G.A. Nelson, M. Vazquez, D.T. Laskowitz, J.M. Slater and R.D. Pearlstein, Apolipoprotein E expression and behavioral toxicity of high charge, high energy (HZE) particle radiation, J Radiat Res (Tokyo) 43(Suppl) (2002), S219-S224.
29. M.A. Hofmann, E. Lalla, Y. Lu, M.R. Gleason, B.M. Wolf, N. Tanji, L.J. Ferran, Jr., B. Kohl, V. Rao, W. Kisiel, D.M. Stern and A.M. Schmidt, Hyperhomocysteinemia enhances vascular inflammation and accelerates atherosclerosis in a murine model, J Clin Invest 107 (2001), 675-683.
30. D. Ingram, M. Jucker and E. Spangler, Behavioral manifestations of aging, in: Pathobiology of the aging rat, C. Capen, ed., ILSI Press, Washington, DC, 1994, pp. 149-170.
31. J.A. Joseph, R.T. Bartus, D. Clody, D. Morgan, C. Finch, B. Beer and S. Sesack, Psychomotor performance in the senescent rodent: reduction of deficits via striatal dopamine receptor up-regulation, Neurobiol Aging 4 (1983), 313-319.
32. J.M. Kim, H. Lee and N. Chang, Hyperhomocysteinemia due to short-term folate deprivation is related to electron microscopic changes in the rat brain, J Nutr 132 (2002), 3418-3421.
33. Y.I. Kim, J.W. Miller, K.A. da Costa, M. Nadeau, D. Smith, J. Selhub, S.H. Zeisel and J.B. Mason, Severe folate deficiency causes secondary depletion of choline and phosphocholine in rat liver, J Nutr 124 (1994), 2197-2203.
34. I.I. Kruman, C. Culmsee, S.L. Chan, Y. Kruman, Z. Guo, L. Penix and M.P. Mattson, Homocysteine elicits a DNA damage response in neurons that promotes apoptosis and hypersensitivity to excitotoxicity, J Neurosci 20 (2000), 6920-6926.
35. I.I. Kruman, T.S. Kumaravel, A. Lohani, W.A. Pedersen, R.G. Cutler, Y. Kruman, N. Haughey, J. Lee, M. Evans and M.P. Mattson, 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 22 (2002), 1752-1762.
36. P. Krzywkowski, O. Ghribi, J. Gagne, C. Chabot, S. Kar, J. Rochford, G. Massicotte and J. Poirier, Cholinergic systems and long-term potentiation in memory-impaired apolipoprotein E-deficient mice, Neuroscience 92 (1999), 1273-1286.
37. H. Lee, H.J. Kim, J.M. Kim and N. Chang, Effects of dietary folic acid supplementation on cerebrovascular endothelial dysfunction in rats with induced hyperhomocysteinemia, Brain Res 996 (2004), 139-147.
38. S.A. Lipton, W.K. Kim, Y.B. Choi, S. Kumar, D.M. D'Emilia, P.V. Rayudu, D.R. Arnelle and J.S. Stamler, Neurotoxicity associated with dual actions of homocysteine at the N-methyl-D-aspartate receptor, Proceedings Of The National Academy Of Sciences Of The United States Of America 94 (1997), 5923-5928.
39. L. Lomnitski, L. Oron, D. Sklan and D.M. Michaelson, Distinct alterations in phospholipid metabolism in brains of apolipoprotein E-deficient mice, J Neurosci Res 58 (1999), 586-592.
40. E. Masliah, M. Mallory, N. Ge, M. Alford, I. Veinbergs and A.D. Roses, Neurodegeneration in the central nervous system of apoE-deficient mice, Exp Neurol 136 (1995), 107-122.
41. M.P. Mattson and T.B. Shea, Folate and homocysteine metabolism in neural plasticity and neurodegenerative disorders, Trends Neurosci 26 (2003), 137-146.
42. A. McCaddon, P. Hudson, G. Davies, A. Hughes, J.H. Williams and C. Wilkinson, Homocysteine and cognitive decline in healthy elderly, Dement Geriatr Cogn Disord 12 (2001), 309-313.
43. S.M. Mihalick, D. Ortiz, R. Kumar, E. Rogers and T.B. Shea, Folate and vitamin E deficiency impair cognitive performance in mice subjected to oxidative stress: differential impact on normal mice and mice lacking apolipoprotein E, Neuromolecular Med 4 (2003), 197-202.
44. J.W. Miller, J.D. Ribaya-Mercado, R.M. Russell, D.C. Shepard, F.D. Morrow, E.F. Cochary, J.A. Sadowski, S.N. Gershoff and J. Selhub, Effect of vitamin B-6 deficiency on fasting plasma homocysteine concentrations, Am J Clin Nutr 55 (1992), 1154-1160.
45. T.J. Montine, K.S. Montine, S.J. Olson, D.G. Graham, L.J. Roberts, 2nd, J.D. Morrow, M.F. Linton, S. Fazio and L.L. Swift, Increased cerebral cortical lipid peroxidation and abnormal phospholipids in aged homozygous apoE-deficient C57BL/6J mice, Exp Neurol 158 (1999), 234-241.
46. Z. Nagy, M.M. Esiri, M. LeGris and P.M. Matthews, Mitochondrial enzyme expression in the hippocampus in relation to Alzheimer-type pathology, Acta Neuropathol (Berl) 97 (1999), 346-354.
47. T. Ogura, M. Ogata, H. Akita, S. Jitsuki, L. Akiba, K. Noda, S. Hoka and M. Saji, Impaired acquisition of skilled behavior in rotarod task by moderate depletion of striatal dopamine in a pre-symptomatic stage model of Parkinson's disease, Neurosci Res 51 (2005), 299-308.
48. M.S. Oitzl, M. Mulder, P.J. Lucassen, L.M. Havekes, J. Grootendorst and E.R. de Kloet, Severe learning deficits in apolipoprotein E-knockout mice in a water maze task, Brain Res 752 (1997), 189-196.
49. J.A. Piedrahita, S.H. Zhang, J.R. Hagaman, P.M. Oliver and N. Maeda, Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells, Proc Natl Acad Sci USA 89 (1992), 4471-4475.
50. J. Puolivali, R. Miettinen, L. Pradier and P. Riekkinen, Jr., Apolipoprotein E-deficient mice are not more susceptible to the biochemical and memory deficits induced by nucleus basalis lesion, Neuroscience 96 (2000), 291-297.
51. R.L. Reddick, S.H. Zhang and N. Maeda, Atherosclerosis in mice lacking apo E. Evaluation of lesional development and progression, Arterioscler Thromb 14 (1994), 141-147.
52. E.H. Reynolds, Neurological Aspects of Folate and Vitamin B12 Metabolism, Clinics in Haematology 5 (1976), 661-689.
53. K.M. Riggs, A. Spiro, 3rd, K. Tucker and D. Rush, Relations of vitamin B-12, vitamin B-6, folate, and homocysteine to cognitive performance in the Normative Aging Study, Am J Clin Nutr 63 (1996), 306-314.
54. T.A. Robertson, N.S. Dutton, R.N. Martins, A.D. Roses, B.A. Kakulas and J.M. Papadimitriou, Age-related congophilic inclusions in the brains of apolipoprotein E-deficient mice, Neuroscience 82 (1998), 171-180.
55. I.H. Rosenberg and J.W. Miller, Nutritional factors in physical and cognitive functions of elderly people, Am J Clin Nutr 55 (1992), 1237S-1243S.
56. P.S. Sachdev, M.J. Valenzuela, H. Brodaty, X.L. Wang, J. Looi, L. Lorentz, L. Howard, M. Jones, A.S. Zagami, D. Gillies and D.E. Wilcken, Homocysteine as a risk factor for cognitive impairment in stroke patients, Dement Geriatr Cogn Disord 15 (2003), 155-162.
57. H.E. Sauberlich, Relationship of Vitamin B6, Vitamin B12, and Folate to Neurological and Neuropsychiatric Disorders, in: Micronutrients in Health and in Disease Prevention, C.E. Butterworth, eds, Marcel Dekker, New York, 1991, pp. 187-218.
58. J. Schneede, H. Refsum and P.M. Ueland, Biological and environmental determinants of plasma homocysteine, Semin Thromb Hemost 26 (2000), 263-279.
59. T.M. Scott, K.L. Tucker, A. Bhadelia, B. Benjamin, S. Patz, R. Bhadelia, E. Liebson, L.L. Price, J. Griffith, I. Rosenberg and M.F. Folstein, Homocysteine and B vitamins relate to brain volume and white-matter changes in geriatric patients with psychiatric disorders, Am J Geriatr Psychiatry 12 (2004), 631-638.
60. J. Selhub, Homocysteine metabolism, Annu Rev Nutr 19 (1999), 217-246.
61. J. Selhub, L.C. Bagley, J. Miller and I.H. Rosenberg, B vitamins, homocysteine, and neurocognitive function in the elderly, Am J Clin Nutr 71 (2000), 614S-620S.
62. T.B. Shea, D. Ortiz and E. Rogers, Differential susceptibity of transgenic mice lacking one or both apolipoprotein alleles to folate and vitamin E deprivation, J Alzheimers Dis 6 (2004), 269-273.
63. H. Sheng, D.T. Laskowitz, G.B. Mackensen, M. Kudo, R.D. Pearlstein and D.S. Warner, Apolipoprotein E deficiency worsens outcome from global cerebral ischemia in the mouse, Stroke 30 (1999), 1118-1124.
64. B. Shukitt-Hale, G. Mouzakis and J.A. Joseph, Psychomotor and spatial memory performance in aging male Fischer 344 rats, Exp Gerontol 33 (1998), 615-624.
65. B. Shukitt-Hale, G. Casadesus, J.J. McEwen, B.M. Rabin and J.A. Joseph, Spatial learning and memory deficits induced by exposure to iron-56-particle radiation, Radiat Res 154 (2000), 28-33.
66. S.P. Stabler and R.H. Allen, Quantification of serum and urinary S-adenosylmethionine and S-adenosylhomocysteine by stable-isotope-dilution liquid chromatography-mass spectrometry, Clin Chem 50 (2004), 365-372.
67. E.L. Streck, C. Matte, P.S. Vieira, T. Calcagnotto, C.M. Wannmacher, M. Wajner and A.T. Wyse, Impairment of energy metabolism in hippocampus of rats subjected to chemically-induced hyperhomocysteinemia, Biochim Biophys Acta 1637 (2003), 187-192.
68. E.L. Streck, C.S. Bavaresco, C.A. Netto and A.T. Wyse, Chronic hyperhomocysteinemia provokes a memory deficit in rats in the Morris water maze task, Behav Brain Res 153 (2004), 377-381.
69. J.W. Taanman, R.E. Hall, C. Tang, M.F. Marusich, N.G. Kennaway and R.A. Capaldi, Tissue distribution of cytochrome c oxidase isoforms in mammals. Characterization with monoclonal and polyclonal antibodies, Biochim Biophys Acta 1225 (1993), 95-100.
70. C.E. Teunissen, A.H. Blom, M.P. Van Boxtel, H. Bosma, C. de Bruijn, J. Jolles, B.A. Wauters, H.W. Steinbusch and J. de Vente, Homocysteine: a marker for cognitive performance? A longitudinal follow-up study, J Nutr Health Aging 7 (2003), 153-159.
71. A. Troen and I. Rosenberg, Homocysteine and cognitive function, Semin Vasc Med 5 (2005), 209-214.
72. A.M. Troen, E. Lutgens, D.E. Smith, I.H. Rosenberg and J. Selhub, The atherogenic effect of excess methionine intake, Proc Natl Acad Sci USA 100 (2003), 15089-15094.
73. A.M. Troen, The central nervous system in animal models of hyperhomocysteinemia, Prog Neuropsychopharmacol Biol Psychiatry 29 (2005), 1140-1151.
74. I. Veinbergs and E. Masliah, Synaptic alterations in apolipoprotein E knockout mice, Neuroscience 91 (1999), 401-403.
75. D.G. Weir and J.M. Scott, The biochemical basis of the neuropathy in cobalamin deficiency, Baillieres Clin Haematol 8 (1995), 479-497.
76. D.G. Weir and J.M. Scott, Brain function in the elderly: role of vitamin B12 and folate, Br Med Bull 55 (1999), 669-682.
77. S.H. Zhang, R.L. Reddick, J.A. Piedrahita and N. Maeda, Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E, Science 258 (1992), 468-471.
78. J. Zhou, J. Moller, C.C. Danielsen, J. Bentzon, H.B. Ravn, R.C. Austin and E. Falk, Dietary supplementation with methionine and homocysteine promotes early atherosclerosis but not plaque rupture in ApoE-deficient mice, Arterioscler Thromb Vasc Biol 21 (2001), 1470-1476.
79. J. Zhou, J. Moller, M. Ritskes-Hoitinga, M.L. Larsen, R.C. Austin and E. Falk, Effects of vitamin supplementation and hyperhomocysteinemia on atherosclerosis in apoE-deficient mice, Atherosclerosis 168 (2003), 255-262.
80. J. Zittoun, Congenital errors of folate metabolism, in: Baillieres Clin Haematol, eds., England, 1995, pp. 603-616.