Folate/vitamin-B12 prevents chronic hyperhomocysteinemia-Induced tau hyperphosphorylation and memory deficits in aged rats

Journal of Alzheimer's Disease

Volumn 27, Issue 3, 2011, Pages 639-650

  Wei, Wei ^a,b   Liu, Ying Hua ^a   Zhang, Chang E ^a   Wang, Qun ^a   Wei, Zelan ^c   Mousseau, Darrell D ^c   Wang, Jian Zhi ^a   Tian, Qing ^a   Liu, Gong Ping ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b JINAN UNIVERSITY   (China)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Aged rat; Alzheimer's disease; folate; hyperhomocysteinemia; vitamin B12

Indexed keywords

CYANOCOBALAMIN; CYCLIN DEPENDENT KINASE 5; DRINKING WATER; FOLIC ACID; GLYCOGEN SYNTHASE KINASE 3BETA; HOMOCYSTEINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOPROTEIN PHOSPHATASE 2A; TAU PROTEIN;

AGED; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; BRAIN CORTEX; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVATION; ENZYME INHIBITION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; HYPERHOMOCYSTEINEMIA; MALE; MAZE TEST; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; WESTERN BLOTTING;

EID: 82555195174     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-110770     Document Type: Article

References (58)

1. Loscalzo J (2002) Homocysteine and dementias. N Engl J Med 346, 466-468.
2. Brattström L, Israelsson B, Lindgärde F, Hultberg B (1988) Higher total plasma homocysteine in vitamin B12 deficiency than in heterozygosity for homocystinuria due to cystathionine beta-synthase deficiency. Metabolism 37, 175-178. (Pubitemid 18055235)
3. Gottfries CG, Lehmann W, Regland B (1998) Early diagnosis of cognitive impairment in the elderly with the focus on Alzheimer's disease. J Neural Transm 105, 773-786. (Pubitemid 28539829)
4. Miller JW (1999) Homocysteine and Alzheimer's disease. Nutr Rev 57, 126-129.
5. Sacco RL, Roberts JK, Jacobs BS (1998) Homocysteine as a risk factor for ischemic stroke: An epidemiological story in evolution. Neuroepidemiology 17, 167-173. (Pubitemid 28341655)
6. Seshadri S, Beiser A, Selhub. J, Jacques PF, Rosenberg IH, D'Agostino RB, Wilson PW, Wolf PA (2002) Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N Engl J Med 346, 476-483. (Pubitemid 34441738)
7. Watkins D, Rosenblatt DS (1989) Functional methionine synthase deficiency (cblE and cblG): Clinical and biochemical heterogeneity. Am J Med Genet 34, 427-434. (Pubitemid 19284633)
8. Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS, Wisniewski HM (1986) Microtubule-associated protein tau A component of Alzheimer paired helical filaments. J Biol Chem 261, 6084-6089. (Pubitemid 17207447)
9. Lauckner J, Frey P, Geula C (2003) Comparative distribution of tau phosphorylated at Ser262 in pre-tangles and tangles. Neurobiol Aging 24, 767-776. (Pubitemid 37303986)
10. Wood JG, Mirra SS, Pollock NJ, Binder LI (1986) Neurofibrillary tangles of Alzheimer disease share antigenic determinants with the axonal microtubule-associated protein tau (tau). Proc Natl Acad Sci U S A 83, 4040-4043. (Pubitemid 16062418)
11. Billingsley ML, Kincaid RL (1997) Regulated phosphorylation and dephosphorylation of tau protein: Effects on microtubule interaction, intracellular trafficking and neurodegeneration. Biochem J 323, 577-591. (Pubitemid 27202326)
12. Wang JZ, Grundke-Iqbal I, Iqbal K (1996) Glycosylation of microtubule-associated protein tau: An abnormal posttranslational modification in Alzheimer's disease. Nat Med 2, 871-875. (Pubitemid 26296756)
13. Clarke R, Smith AD, Jobst KA, Refsum H, Sutton L, Ueland PM (1998) Folacin, vitamin B12, and serum total homocysteine levels in confirmed Alzheimer disease. Arch Neurol 55, 1449-1455. (Pubitemid 28525506)
14. McCaddon A, Davies G, Hudson P, Tandy S, Cattell H (1998) Total serumhomocysteine in senile dementia of Alzheimer type. Int J Geriatr Psychiatry 13, 235-239. (Pubitemid 28194997)
15. Nilsson K, Gustafson L, Hultberg B (2006) Plasma homocysteine, cobalamin/folate status, and vascular disease in a large population of psychogeriatric patients. Dement Geriatr Cogn Disord 22, 358-366. (Pubitemid 44651452)
16. Tabet N, Rafi H, Weaving G, Lyons B, Iversen SA (2006) Behavioural and psychological symptoms of Alzheimer type dementia are not correlated with plasma homocysteine concentration. Dement Geriatr Cogn Disord 22, 432-438. (Pubitemid 44726013)
17. Pacheco-Quinto J, Rodriguez de Turco EB, DeRosa S, Howard A, Cruz-Sanchez F, Sambamurti K, Refolo L, Petanceska S, Pappolla MA (2006) Hyperhomocysteinemic Alzheimer's mouse model of amyloidosis shows increased brain amyloid peptide levels. Neurobiol Dis 22, 651-656. (Pubitemid 43832135)
18. Fuso A, Nicolia V, Cavallaro RA, Ricceri L, D'Anselmi F, Coluccia P, Calamandrei G, Scarpa S (2008) Bvitamin ndeprivation induces hyperhomocysteinemia and brain S-adenosylhomocysteine, depletes brain S-adenosylmethionine, and enhances PS1 and BACE expression and amyloidbeta deposition in mice. Mol Cell Neurosci 37, 731-746.
19. Kruman II, Kumaravel TS, Lohani A, Pedersen WA, Cutler RG, Kruman Y, Haughey N, Lee J, Evans M, Mattson MP (2002) 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, 1752-1762. (Pubitemid 35386293)
20. Poddar R, Paul S (2009) Homocysteine-NMDA receptormediated activation of extracellular signal-regulated kinase leads to neuronal cell death. J Neurochem 110, 1095-1106.
21. Leoncini G, Bruzzese D, Signorello MG (2006) Activation of p38 MAPKinase/cPLA2 pathway in homocysteine-treated platelets. J Thromb Haemost 4, 209-216.
22. Kruman II, Culmsee C, Chan SL, Kruman Y, Guo Z, Penix L, Mattson MP (2000) Homocysteine elicits a DNA damage response in neurons that promotes apoptosis and hypersensitivity to excitotoxicity. J Neurosci 20, 6920-6926.
23. Zhang CE, Tian Q,WeiW, Peng JH, Liu GP, ZhouXW,Wang Q, Wang DW, Wang JZ (2008) Homocysteine induces tau phosphorylation by inactivating protein phosphatase 2A in rat hippocampus. Neurobiol Aging 29, 1654-1665.
24. Zhang CE,WeiW, Liu YH, Peng JH, Tian Q, LiuGP, ZhangY, Wang JZ (2009) Hyperhomocysteinemia increasesβ-amyloid by enhancing expression of gamma-secretase and phosphorylation of amyloid precursor protein in rat brain. Am J Pathol 174, 1481-1491.
25. Ritchie K, KildeaD(1995) Is senile dementia 'age-related' or 'ageing related' ? Evidence from meta-analysis of dementia prevalence in the oldest-old. Lancet 346, 931-934.
26. Sasaki K, Duan J, Murohara T, Ikeda H, Shintani S, Shimada T, Akita T, Egami K, Imaizumi T (2003) Rescue of hypercholesterolemia-related impairment of angiogenesis by oral folate supplementation. J Am Coll Cardiol 42, 364-372. (Pubitemid 36851431)
27. Liu SJ, Zhang AH, Li HL, Wang Q, Deng HM, Netzer WJ, Xu HX,Wang JZ (2003) Overactivation of glycogen synthase kinase-3 by inhibition of phosphoinositol-3 kinase and protein kinaseCleads to hyperphosphorylation of tau and impairment of spatial memory. J Neurochem 87, 1333-1344. (Pubitemid 38020568)
28. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11, 47-60. (Pubitemid 14088970)
29. Frick B, Schrocksnadel K, Neurauter G,Wirleitner B, Artner- Dworzak E, Fuchs D (2003) Rapid measurement of total lasma homocysteine by HPLC. Clinica Chimica Acta 331, 19-23. (Pubitemid 36412021)
30. Palop JJ, Jones B, Kekonius L, Chin J, Yu GQ, Raber J, Masliah E, Mucke L (2003) Neuronal depletion of calciumdependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc Natl Acad Sci U S A 100, 9572-9577. (Pubitemid 37033969)
31. Blard O, Frebourg T, Campion D, Lecourtois M (2006) Inhibition of proteasome and Shaggy/Glycogen synthase kinase-3beta kinase prevents clearance of phosphorylated tau in Drosophila. J Neurosci Res 84, 1107-1115. (Pubitemid 44521055)
32. Bramblett GT, Goedert M, Jakes R, Merrick SE, Trojanowski JQ, Lee VM (1993) Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10, 1089-1099. (Pubitemid 23194399)
33. Merrick SE, Trojanowski JQ, Lee VM (1997) Selective destruction of stable microtubules and axons by inhibitors of protein serine/threonine phosphatases in cultured human neurons. J Neurosci 17, 5726-5737. (Pubitemid 27310488)
34. Liu R, Zhou XW, Tanila H, Bjorkdahl C, Wang JZ, Guan ZZ, Cao Y, Gustafsson JA, Winblad B, Pei JJ (2008) Phosphorylated PP2A (tyrosine 307) is associated with Alzheimer neurofibrillary pathology. J Cell Mol Med 12, 241-257. (Pubitemid 351430466)
35. Iwatsubo T, Odaka A, Suzuki N, Mizusawa H, Nukina N, Ihara Y (1994) Visualization of Aβ42(43) and Aβ40 in senile plaques with end specific Aβ monoclonals: Evidence that an initially deposited species is Aβ42(43). Neuron 13, 45-53.
36. Herrmann W, Quast S, Ullrich M, Schultze H, Bodis M, Geisel J (1999) Hyperhomocysteinemia in high-aged subjects: Relation of B-vitamins, folic acid, renal function and the methylenetetrahydrofolate reductase mutation. Atherosclerosis 144, 91-101. (Pubitemid 29259970)
37. Obeid R, Schorr H, Eckert R, Herrmann W (2004) Vitamin B12 status in the elderly as judged by available biochemical markers. Clin Chem 50, 238-241. (Pubitemid 38125734)
38. Heijer T, Skoog I, Oudkerk M, de Leeuw FE, de Groot JC, Hofman A, Breteler MM (2003) Association between blood pressure levels over time and brain atrophy in the elderly. Neurobiol Aging 24, 307-313. (Pubitemid 36005410)
39. Ravaglia G, Forti P, Maioli F, Martelli M, Servadei L, Brunetti N, Porcellini E, Licastro F (2005) Homocysteine and folate as risk factors for dementia and Alzheimer disease. Am J Clin Nutr 82, 636-643.
40. Ramos MI, Allen LH, Mungas DM, Jagust WJ, Haan MN, Green R, MillerJW(2005) Lowfolate status is associated with impaired cognitive function and dementia in the Sacramento Area Latino Study on Aging. Am J Clin Nutr 82, 1346-1352. (Pubitemid 43779735)
41. Stewart R, Asonganyi B, Sherwood R (2002) Plasma homocysteine and cognitive impairment in an older British African-Caribbean population. J Am Geriatr Soc 50, 1227-1232. (Pubitemid 34774546)
42. Churcher I (2006) Tau therapeutic strategies for the treatment of Alzheimer's disease. Curr Top Med Chem 6, 579-595.
43. Elyaman W, Terro F, Wong NS, Hugon J (2002) In vivo activation and nuclear translocation of phosphorylated glycogen synthase kinase-3beta in neuronal apoptosis: Links to tau phosphorylation. Eur J Neurosci 15, 651-660. (Pubitemid 35471934)
44. Lee CW, Lau KF,Miller CC, Shaw PC (2003) Glycogen synthase kinase-3 beta-mediated tau phosphorylation in cultured cell lines. Neuroreport 14, 257-260. (Pubitemid 36308422)
45. Liu F, Grundke-Iqbal I, Iqbal K, Gong CX (2005) Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation. Eur J Neurosci 22, 1942-1950. (Pubitemid 41579384)
46. Wang JZ, Gong CX, Zaidi T, Grundke-Iqbal I, Iqbal K (1995) Dephosphorylation of Alzheimer paired helical filaments by protein phosphatase-2A and -2B. J Biol Chem 270, 4854-4860.
47. Wang JZ, Liu F (2008) Microtubule-associated protein tau in development, degeneration and protection of neurons. Prog Neurobiol 85, 148-175.
48. Sontag E, Nunbhakdi-Craig V, Sontag JM, Diaz-Arrastia R, Ogris E, Dayal S, Lentz SR, Arning E, Bottiglieri T (2007) Protein phosphatase 2A methyltransferase links homocysteine metabolism with tau and amyloid precursor protein regulation. J Neurosci 27, 2751-2759. (Pubitemid 46438990)
49. Najib S, Sánchez-Margalet V (2005) Homocysteine thiolactone inhibits insulin-stimulated DNA and protein synthesis: Possible role of mitogen-activated protein kinase (MAPK), glycogen synthase kinase-3 (GSK-3) and p70 S6K phosphorylation. J Mol Endocrinol 34, 119-126. (Pubitemid 40305554)
50. Greenberg SG, Davies PA (1990) Preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci U S A 87, 5827-5831.
51. Hanger DP, Brion JP, Gallo JM, Cairns NJ, Luthert PJ, Anderton BH (1991) Tau in Alzheimer's disease and Down's syndrome is insoluble and abnormally phosphorylated. Biochem J 275, 99-104.
52. Garcia A, Zanibbi K (2004) Homocysteine and cognitive function in elderly people. CMAJ 171, 897-904. (Pubitemid 39371559)
53. Miller JW, Green R, Ramos MI, Allen LH, Mungas DM, Jagust WJ, Haan MN (2003) Homocysteine and cognitive function in the Sacramento Area Latino Study on Aging. Am J Clin Nutr 78, 441-447. (Pubitemid 39663511)
54. Avila J, Lim F, Moreno F, Belmonte C, Cuello AC (2002) Tau function and dysfunction in neurons: Its role in neurodegenerative disorders. Mol Neurobiol 25, 213-231. (Pubitemid 34665091)
55. Johnson WG (2000) Late-onset neurodegenerative diseases- the role of protein insolubility. J Anat 196, 609-616. (Pubitemid 30458781)
56. Finkelstein JD (1990) Methionine metabolism in mammalians. J Nutr Biochem 1, 228-237.
57. Troen AM, Shukitt-Hale B, Chao WH, Albuquerque B, Smith DE, Selhub J, Rosenberg J (2006) The cognitive impact of nutritional homocysteinemia in apolipoprotein-E deficient mice. J Alzheimers Dis 9, 381-392. (Pubitemid 44253352)
58. Sontag JM, Nunbhakdi-Craig V, Montgomery L, Arning E, Bottiglieri T, Sontag E (2008) Folate deficiency induces in vitro and mouse brain region-specific downregulation of leucine carboxyl methyltransferase-1 and protein phosphatase 2A B(alpha) subunit expression that correlate with enhanced tau phosphorylation. J Neurosci 28, 11477-11487.