Neurobiology of Aging
Volume 30, Issue 4 , Pages 549-560 , April 2009

DNA methylation impacts on learning and memory in aging

  • Liang Liu

      Affiliations

    • Department of Biology, University of Alabama at Birmingham, 175 Campbell Hall, 1300 University Boulevard, Birmingham, AL 35294-1170, United States
    • Center for Aging, University of Alabama at Birmingham, AL, United States
    • Corresponding Author InformationCorresponding author at: University of Alabama at Birmingham, Department of Biology, 175 Campbell Hall, 1300 University Boulevard, Birmingham, AL 35294-1170, United States. Tel.: +1 205 934 4587; fax: +1 205 975 6097.
  • ,
  • Thomas van Groen

      Affiliations

    • Department of Cell Biology, University of Alabama at Birmingham, AL, United States
  • ,
  • Inga Kadish

      Affiliations

    • Department of Cell Biology, University of Alabama at Birmingham, AL, United States
  • ,
  • Trygve O. Tollefsbol

      Affiliations

    • Department of Biology, University of Alabama at Birmingham, 175 Campbell Hall, 1300 University Boulevard, Birmingham, AL 35294-1170, United States
    • Center for Aging, University of Alabama at Birmingham, AL, United States
    • Comprehensive Cancer Center, University of Alabama at Birmingham, AL, United States

Received 19 March 2007 ,Revised 19 June 2007 ,Accepted 24 July 2007.

References 

  1. Abdolmaleky HM, Cheng KH, Russo A, Smith CL, Faraone SV, Wilcox M, et al. Hypermethylation of the reelin (RELN) promoter in the brain of schizophrenic patients: a preliminary report. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2005;134:60–66
  2. Alarcon JM, Malleret G, Touzani K, Vronskaya S, Ishii S, Kandel ER, et al. Chromatin acetylation, memory, and LTP are impaired in CBP+/− mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron. 2004;42:947–959
  3. Albright CD, Friedrich CB, Brown EC, Mar MH, Zeisel SH. Maternal dietary choline availability alters mitosis, apoptosis and the localization of TOAD-64 protein in the developing fetal rat septum. Brain Res. Dev. Brain Res. 1999;115:123–129
  4. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 1999;23:185–188
  5. Andria ML, Simon EJ. Localization of promoter elements in the human mu-opioid receptor gene and regulation by DNA methylation. Brain Res. Mol. Brain Res. 1999;70:54–65
  6. Barresi V, Condorelli DF, Giuffrida Stella AM. GFAP gene methylation in different neural cell types from rat brain. Int. J. Dev. Neurosci. 1999;17:821–828
  7. Bienvenu T, Chelly J. Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat. Rev. Genet. 2006;7:415–426
  8. Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 1973;232:331–356
  9. Bonsch D, Lenz B, Kornhuber J, Bleich S. DNA hypermethylation of the alpha synuclein promoter in patients with alcoholism. Neuroreport. 2005;16:167–170
  10. Bonsch D, Lenz B, Reulbach U, Kornhuber J, Bleich S. Homocysteine associated genomic DNA hypermethylation in patients with chronic alcoholism. J. Neural. Transm. 2004;111:1611–1616
  11. Brehm A, Miska EA, McCance DJ, Reid JL, Bannister AJ, Kouzarides T. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature. 1998;391:597–601
  12. Brooks PJ, Marietta C, Goldman D. DNA mismatch repair and DNA methylation in adult brain neurons. J. Neurosci. 1996;16:939–945
  13. Cameron HA, McKay RD. Restoring production of hippocampal neurons in old age. Nat. Neurosci. 1999;2:894–897
  14. Chan HM, La Thangue NB. p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J. Cell. Sci. 2001;114:2363–2373
  15. Chen WG, Chang Q, Lin Y, Meissner A, West AE, Griffith EC, et al. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science. 2003;302:885–889
  16. Cheung P, Lau P. Epigenetic regulation by histone methylation and histone variants. Mol. Endocrinol. 2005;19:563–573
  17. Collins AL, Levenson JM, Vilaythong AP, Richman R, Armstrong DL, Noebels JL, et al. Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum. Mol. Genet. 2004;13:2679–2689
  18. Condorelli DF, Nicoletti VG, Barresi V, Caruso A, Conticello S, de Vellis J, et al. Tissue-specific DNA methylation patterns of the rat glial fibrillary acidic protein gene. J. Neurosci. Res. 1994;39:694–707
  19. Costa E, Davis J, Pesold C, Tueting P, Guidotti A. The heterozygote reeler mouse as a model for the development of a new generation of antipsychotics. Curr. Opin. Pharmacol. 2002;2:56–62
  20. Craciunescu CN, Albright CD, Mar MH, Song J, Zeisel SH. Choline availability during embryonic development alters progenitor cell mitosis in developing mouse hippocampus. J. Nutr. 2003;133:3614–3618
  21. Craciunescu CN, Brown EC, Mar MH, Albright CD, Nadeau MR, Zeisel SH. Folic acid deficiency during late gestation decreases progenitor cell proliferation and increases apoptosis in fetal mouse brain. J. Nutr. 2004;134:162–166
  22. Davis CD, Uthus EO. Dietary folate and selenium affect dimethylhydrazine-induced aberrant crypt formation, global DNA methylation and one-carbon metabolism in rats. J. Nutr. 2003;133:2907–2914
  23. Dong E, Agis-Balboa RC, Simonini MV, Grayson DR, Costa E, Guidotti A. Reelin and glutamic acid decarboxylase67 promoter remodeling in an epigenetic methionine-induced mouse model of schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 2005;102:12578–12583
  24. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat. Med. 1998;4:1313–1317
  25. Espeland MA, Coker LH, Wallace R, Rapp SR, Resnick SM, Limacher M, et al. Association between alcohol intake and domain-specific cognitive function in older women. Neuroepidemiology. 2006;27:1–12
  26. Fan G, Beard C, Chen RZ, Csankovszki G, Sun Y, Siniaia M, et al. DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J. Neurosci. 2001;21:788–797
  27. Fan G, Martinowich K, Chin MH, He F, Fouse SD, Hutnick L, et al. DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development. 2005;132:3345–3356
  28. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature. 1983;301:89–92
  29. Feng J, Chang H, Li E, Fan G. Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. J. Neurosci. Res. 2005;79:734–746
  30. Fuso A, Seminara L, Cavallaro RA, D’Anselmi F, Scarpa S. S-Adenosylmethionine/homocysteine cycle alterations modify DNA methylation status with consequent deregulation of PS1 and BACE and beta-amyloid production. Mol. Cell. Neurosci. 2005;28:195–204
  31. Gage FH. Mammalian neural stem cells. Science. 2000;287:1433–1438
  32. Gemelli T, Berton O, Nelson ED, Perrotti LI, Jaenisch R, Monteggia LM. Postnatal loss of methyl-CpG binding protein 2 in the forebrain is sufficient to mediate behavioral aspects of Rett syndrome in mice. Biol. Psychiatry. 2006;59:468–476
  33. Gordon N. Nutrition and cognitive function. Brain Dev. 1997;19:165–170
  34. Grayson DR, Jia X, Chen Y, Sharma RP, Mitchell CP, Guidotti A, et al. Reelin promoter hypermethylation in schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 2005;102:9341–9346
  35. Guy J, Gan J, Selfridge J, Cobb S, Bird A. Reversal of neurological defects in a mouse model of Rett syndrome. Science. 2007;315:1143–1147
  36. Haan MN, Miller JW, Aiello AE, Whitmer RA, Jagust WJ, Mungas DM, et al. Homocysteine, B vitamins, and the incidence of dementia and cognitive impairment: results from the Sacramento Area Latino Study on Aging. Am. J. Clin. Nutr. 2007;85:511–517
  37. Hassan YI, Zempleni J. Epigenetic regulation of chromatin structure and gene function by biotin. J. Nutr. 2006;136:1763–1765
  38. Hendrich B, Bird A. Mammalian methyltransferases and methyl-CpG-binding domains: proteins involved in DNA methylation. Curr. Top. Microbiol. Immunol. 2000;249:55–74
  39. Holliday R. Is there an epigenetic component in long-term memory?. J. Theor. Biol. 1999;200:339–341
  40. Holliday R. Francis Crick (1916–2004). Cell. 2004;119:1–2
  41. Honein MA, Paulozzi LJ, Mathews TJ, Erickson JD, Wong LY. Impact of folic acid fortification of the US food supply on the occurrence of neural tube defects. JAMA. 2001;285:2981–2986
  42. 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
  43. Huang YY, Li XC, Kandel ER. cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell. 1994;79:69–79
  44. Huang YY, Pittenger C, Kandel ER. A form of long-lasting, learning-related synaptic plasticity in the hippocampus induced by heterosynaptic low-frequency pairing. Proc. Natl. Acad. Sci. U.S.A. 2004;101:859–864
  45. Iizuka M, Smith MM. Functional consequences of histone modifications. Curr. Opin. Genet. Dev. 2003;13:154–160
  46. Impagnatiello F, Guidotti AR, Pesold C, Dwivedi Y, Caruncho H, Pisu MG, et al. A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 1998;95:15718–15723
  47. Inano K, Suetake I, Ueda T, Miyake Y, Nakamura M, Okada M, et al. Maintenance-type DNA methyltransferase is highly expressed in post-mitotic neurons and localized in the cytoplasmic compartment. J. Biochem. (Tokyo). 2000;128:315–321
  48. Jacques PF, Selhub J, Bostom AG, Wilson PW, Rosenberg IH. The effect of folic acid fortification on plasma folate and total homocysteine concentrations. N. Engl. J. Med. 1999;340:1449–1454
  49. Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293:1074–1080
  50. Jones KR, Farinas I, Backus C, Reichardt LF. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell. 1994;76:989–999
  51. Jones PA, Laird PW. Cancer epigenetics comes of age. Nat. Genet. 1999;21:163–167
  52. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 1998;19:187–191
  53. Jorgenson LA, Sun M, O’Connor M, Georgieff MK. Fetal iron deficiency disrupts the maturation of synaptic function and efficacy in area CA1 of the developing rat hippocampus. Hippocampus. 2005;15:1094–1102
  54. Kelz MB, Chen J, Carlezon WA, Whisler K, Gilden L, Beckmann AM, et al. Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature. 1999;401:272–276
  55. Kim M, Campeau S, Falls WA, Davis M. Infusion of the non-NMDA receptor antagonist CNQX into the amygdala blocks the expression of fear-potentiated startle. Behav. Neural. Biol. 1993;59:5–8
  56. Kretchmer N, Beard JL, Carlson S. The role of nutrition in the development of normal cognition. Am. J. Clin. Nutr. 1996;63:997S–1001S
  57. Kruman II, Mouton PR, Emokpae R, Cutler RG, Mattson MP. Folate deficiency inhibits proliferation of adult hippocampal progenitors. Neuroreport. 2005;16:1055–1059
  58. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 1996;16:2027–2033
  59. Kumar A, Choi KH, Renthal W, Tsankova NM, Theobald DE, Truong HT, et al. Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron. 2005;48:303–314
  60. Landsberger N, Wolffe AP. Remodeling of regulatory nucleoprotein complexes on the Xenopus hsp70 promoter during meiotic maturation of the Xenopus oocyte. EMBO J. 1997;16:4361–4373
  61. Laurin D, Verreault R, Lindsay J, Dewailly E, Holub BJ. Omega-3 fatty acids and risk of cognitive impairment and dementia. J. Alzheimers Dis. 2003;5:315–322
  62. Lauterborn JC, Rivera S, Stinis CT, Hayes VY, Isackson PJ, Gall CM. Differential effects of protein synthesis inhibition on the activity-dependent expression of BDNF transcripts: evidence for immediate-early gene responses from specific promoters. J. Neurosci. 1996;16:7428–7436
  63. Lee H, Kim JJ. Amygdalar NMDA receptors are critical for new fear learning in previously fear-conditioned rats. J. Neurosci. 1998;18:8444–8454
  64. Lee WJ, Zhu BT. Inhibition of DNA methylation by caffeic acid and chlorogenic acid, two common catechol-containing coffee polyphenols. Carcinogenesis. 2006;27:269–277
  65. Lehmann M, Gottfries CG, Regland B. Identification of cognitive impairment in the elderly: homocysteine is an early marker. Dement. Geriatr. Cogn. Disord. 1999;10:12–20
  66. Levenson JM, Choi S, Lee SY, Cao YA, Ahn HJ, Worley KC, et al. A bioinformatics analysis of memory consolidation reveals involvement of the transcription factor c-rel. J. Neurosci. 2004;24:3933–3943
  67. Levenson JM, O’Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 2004;279:40545–40559
  68. Levenson JM, Sweatt JD. Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 2005;6:108–118
  69. Li E, Bestor TH, Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell. 1992;69:915–926
  70. Lieberman HR. Nutrition, brain function and cognitive performance. Appetite. 2003;40:245–254
  71. Lippa CF. Familial Alzheimer's disease: genetic influences on the disease process (review). Int. J. Mol. Med. 1999;4:529–536
  72. Liu L, Wylie RC, Andrews LG, Tollefsbol TO. Aging, cancer and nutrition: the DNA methylation connection. Mech. Ageing Dev. 2003;124:989–998
  73. Lois C, Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science. 1994;264:1145–1148
  74. Luikenhuis S, Giacometti E, Beard CF, Jaenisch R. Expression of MeCP2 in postmitotic neurons rescues Rett syndrome in mice. Proc. Natl. Acad. Sci. U.S.A. 2004;101:6033–6038
  75. Lukas RJ. Diversity and patterns of regulation of nicotinic receptor subtypes. Ann. N.Y. Acad. Sci. 1995;757:153–168
  76. Luskin MB. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron. 1993;11:173–189
  77. Magnaghi-Jaulin L, Groisman R, Naguibneva I, Robin P, Lorain S, Le Villain JP, et al. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature. 1998;391:601–605
  78. Mani ST, Thakur MK. In the cerebral cortex of female and male mice, amyloid precursor protein (APP) promoter methylation is higher in females and differentially regulated by sex steroids. Brain Res. 2006;1067:43–47
  79. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science. 2003;302:890–893
  80. McCaddon A, Davies G, Hudson P, Tandy S, Cattell H. Total serum homocysteine in senile dementia of Alzheimer type. Int. J. Geriatr. Psychiatry. 1998;13:235–239
  81. Meck WH, Williams CL. Simultaneous temporal processing is sensitive to prenatal choline availability in mature and aged rats. Neuroreport. 1997;8:3045–3051
  82. Mellott, T.J., Follettie, M.T., Diesl, V., Hill, A.A., Lopez-Coviella, I., Krzysztof Blusztajn, J., 2007. Prenatal choline availability modulates hippocampal and cerebral cortical gene expression. FASEB J. (epub ahead of print).
  83. Miller JW. Assessing the association between vitamin B-12 status and cognitive function in older adults. Am. J. Clin. Nutr. 2006;84:1259–1260
  84. Misner DL, Jacobs S, Shimizu Y, de Urquiza AM, Solomin L, Perlmann T, et al. Vitamin A deprivation results in reversible loss of hippocampal long-term synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A. 2001;98:11714–11719
  85. Mullaney BC, Johnston MV, Blue ME. Developmental expression of methyl-CpG binding protein 2 is dynamically regulated in the rodent brain. Neuroscience. 2004;123:939–949
  86. Nan X, Campoy FJ, Bird A. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell. 1997;88:471–481
  87. Nelson ED, Kavalali ET, Monteggia LM. MeCP2-dependent transcriptional repression regulates excitatory neurotransmission. Curr. Biol. 2006;16:710–716
  88. Nguyen PV, Abel T, Kandel ER. Requirement of a critical period of transcription for induction of a late phase of LTP. Science. 1994;265:1104–1107
  89. Nguyen PV, Kandel ER. Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn. Mem. 1997;4:230–243
  90. Nicholson JM, Wood CM, Reynolds CD, Brown A, Lambert SJ, Chantalat L, et al. Histone structures: targets for modifications by molecular assemblies. Ann. N.Y. Acad. Sci. 2004;1030:644–655
  91. Niculescu MD, Craciunescu CN, Zeisel SH. Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains. FASEB J. 2006;20:43–49
  92. Noh JS, Sharma RP, Veldic M, Salvacion AA, Jia X, Chen Y, et al. DNA methyltransferase 1 regulates reelin mRNA expression in mouse primary cortical cultures. Proc. Natl. Acad. Sci. U.S.A. 2005;102:1749–1754
  93. Numachi Y, Yoshida S, Yamashita M, Fujiyama K, Naka M, Matsuoka H, et al. Psychostimulant alters expression of DNA methyltransferase mRNA in the rat brain. Ann. N.Y. Acad. Sci. 2004;1025:102–109
  94. Peterson CL, Laniel MA. Histones and histone modifications. Curr. Biol. 2004;14:R546–R551
  95. Picciotto MR, Caldarone BJ, King SL, Zachariou V. Nicotinic receptors in the brain. Links between molecular biology and behavior. Neuropsychopharmacology. 2000;22:451–465
  96. Pollwein P, Masters CL, Beyreuther K. The expression of the amyloid precursor protein (APP) is regulated by two GC-elements in the promoter. Nucleic Acids. Res. 1992;20:63–68
  97. Poo MM. Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2001;2:24–32
  98. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD. Programmed cell death and the control of cell survival: lessons from the nervous system. Science. 1993;262:695–700
  99. Ramos MI, Allen LH, Mungas DM, Jagust WJ, Haan MN, Green R, et al. Low folate status is associated with impaired cognitive function and dementia in the Sacramento Area Latino Study on Aging. Am. J. Clin. Nutr. 2005;82:1346–1352
  100. Refsum H, Ueland PM, Nygard O, Vollset SE. Homocysteine and cardiovascular disease. Annu. Rev. Med. 1998;49:31–62
  101. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992;255:1707–1710
  102. Roberson ED, Sweatt JD. A biochemical blueprint for long-term memory. Learn. Mem. 1999;6:381–388
  103. Rogaev EI, Lukiw WJ, Lavrushina O, Rogaeva EA, St George-Hyslop PH. The upstream promoter of the beta-amyloid precursor protein gene (APP) shows differential patterns of methylation in human brain. Genomics. 1994;22:340–347
  104. Rogers SW, Gahring LC, Collins AC, Marks M. Age-related changes in neuronal nicotinic acetylcholine receptor subunit alpha4 expression are modified by long-term nicotine administration. J. Neurosci. 1998;18:4825–4832
  105. Rumble B, Retallack R, Hilbich C, Simms G, Multhaup G, Martins R, et al. Amyloid A4 protein and its precursor in Down's syndrome and Alzheimer's disease. N. Engl. J. Med. 1989;320:1446–1452
  106. Rusted JM, Newhouse PA, Levin ED. Nicotinic treatment for degenerative neuropsychiatric disorders such as Alzheimer's disease and Parkinson's disease. Behav. Brain Res. 2000;113:121–129
  107. Schwartz PM, Borghesani PR, Levy RL, Pomeroy SL, Segal RA. Abnormal cerebellar development and foliation in BDNF−/− mice reveals a role for neurotrophins in CNS patterning. Neuron. 1997;19:269–281
  108. Scott TM, Peter I, Tucker KL, Arsenault L, Bergethon P, Bhadelia R, et al. The Nutrition, Aging, and Memory in Elders (NAME) Study: design and methods for a study of micronutrients and cognitive function in a homebound elderly population. Int. J. Geriatr. Psychiatry. 2006;21:519–528
  109. Shahbazian MD, Antalffy B, Armstrong DL, Zoghbi HY. Insight into Rett syndrome: MeCP2 levels display tissue- and cell-specific differences and correlate with neuronal maturation. Hum. Mol. Genet. 2002;11:115–124
  110. Sibani S, Melnyk S, Pogribny IP, Wang W, Hiou-Tim F, Deng L, et al. Studies of methionine cycle intermediates (SAM, SAH), DNA methylation and the impact of folate deficiency on tumor numbers in Min mice. Carcinogenesis. 2002;23:61–65
  111. Snowdon DA, Tully CL, Smith CD, Riley KP, Markesbery WR. Serum folate and the severity of atrophy of the neocortex in Alzheimer disease: findings from the Nun study. Am. J. Clin Nutr. 2000;71:993–998
  112. Squire LR, Emanuel CA, Davis HP, Deutsch JA. Inhibitors of cerebral protein synthesis: dissociation of aversive and amnesic effects. Behav. Biol. 1975;14:335–341
  113. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, et al. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev. Cell. 2001;1:749–758
  114. Tawa R, Ono T, Kurishita A, Okada S, Hirose S. Changes of DNA methylation level during pre- and postnatal periods in mice. Differentiation. 1990;45:44–48
  115. Teather LA, Wurtman RJ. Dietary CDP-choline supplementation prevents memory impairment caused by impoverished environmental conditions in rats. Learn. Mem. 2005;12:39–43
  116. Teter B, Osterburg HH, Anderson CP, Finch CE. Methylation of the rat glial fibrillary acidic protein gene shows tissue-specific domains. J. Neurosci. Res. 1994;39:680–693
  117. Teter B, Rozovsky I, Krohn K, Anderson C, Osterburg H, Finch C. Methylation of the glial fibrillary acidic protein gene shows novel biphasic changes during brain development. Glia. 1996;17:195–205
  118. Tohgi H, Utsugisawa K, Yoshimura M, Nagane Y, Mihara M. Age-related changes in nicotinic acetylcholine receptor subunits alpha4 and beta2 messenger RNA expression in postmortem human frontal cortex and hippocampus. Neurosci. Lett. 1998;245:139–142
  119. Tohgi H, Utsugisawa K, Nagane Y, Yoshimura M, Genda Y, Ukitsu M. Reduction with age in methylcytosine in the promoter region −224 approximately −101 of the amyloid precursor protein gene in autopsy human cortex. Brain Res. Mol. Brain Res. 1999;70:288–292
  120. Tremolizzo L, Carboni G, Ruzicka WB, Mitchell CP, Sugaya I, Tueting P, et al. An epigenetic mouse model for molecular and behavioral neuropathologies related to schizophrenia vulnerability. Proc. Natl. Acad. Sci. U.S.A. 2002;99:17095–17100
  121. Tsankova N, Renthal W, Kumar A, Nestler EJ. Epigenetic regulation in psychiatric disorders. Nat. Rev. Neurosci. 2007;8:355–367
  122. Ulrey CL, Liu L, Andrews LG, Tollefsbol TO. The impact of metabolism on DNA methylation. Hum. Mol. Genet. 2005;14(Spec. No. 1):R139–R147
  123. Veldic M, Caruncho HJ, Liu WS, Davis J, Satta R, Grayson DR, et al. DNA-methyltransferase 1 mRNA is selectively overexpressed in telencephalic GABAergic interneurons of schizophrenia brains. Proc. Natl. Acad. Sci. U.S.A. 2004;101:348–353
  124. Watanabe H, Zoli M, Changeux JP. Promoter analysis of the neuronal nicotinic acetylcholine receptor alpha4 gene: methylation and expression of the transgene. Eur. J. Neurosci. 1998;10:2244–2253
  125. Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ, et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J. Neurosci. 2005;25:11045–11054
  126. West RL, Lee JM, Maroun LE. Hypomethylation of the amyloid precursor protein gene in the brain of an Alzheimer's disease patient. J. Mol. Neurosci. 1995;6:141–146
  127. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ, et al. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. U.S.A. 2001;98:11024–11031
  128. Wilson VL, Smith RA, Ma S, Cutler RG. Genomic 5-methyldeoxycytidine decreases with age. J. Biol. Chem. 1987;262:9948–9951
  129. Woodruff-Pak DS. Mecamylamine reversal by nicotine and by a partial alpha7 nicotinic acetylcholine receptor agonist (GTS-21) in rabbits tested with delay eyeblink classical conditioning. Behav. Brain Res. 2003;143:159–167
  130. Yonelinas AP, Kroll NE, Quamme JR, Lazzara MM, Sauve MJ, Widaman KF, et al. Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nat. Neurosci. 2002;5:1236–1241
  131. Zawia NH, Basha MR. Environmental risk factors and the developmental basis for Alzheimer's disease. Rev. Neurosci. 2005;16:325–337
  132. Zeisel SH, Blusztajn JK. Choline and human nutrition. Annu. Rev. Nutr. 1994;14:269–296
  133. Zeisel SH. Choline: critical role during fetal development and dietary requirements in adults. Annu. Rev. Nutr. 2006;26:229–250
  134. Zhu X, Mar MH, Song J, Zeisel SH. Deletion of the Pemt gene increases progenitor cell mitosis, DNA and protein methylation and decreases calretinin expression in embryonic day 17 mouse hippocampus. Brain Res. Dev. Brain Res. 2004;149:121–129
  135. Zimmerman L, Parr B, Lendahl U, Cunningham M, McKay R, Gavin B, et al. Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors. Neuron. 1994;12:11–24

PII: S0197-4580(07)00297-7

doi: 10.1016/j.neurobiolaging.2007.07.020

Neurobiology of Aging
Volume 30, Issue 4 , Pages 549-560 , April 2009