Neuroprotective actions of perinatal choline nutrition

References

1. FNB. Dietary reference intakes for thiamin, riboflavin, niacin, vitamin B₆, folate, vitamin B₁₂, panthotenic acid, biotin, and choline. Washington, DC: National Academy Press, 1998.Search in Google Scholar

2. Garner SC, Mar MH, Zeisel SH. Choline distribution and metabolism in pregnant rats and fetuses are influenced by the choline content of the maternal diet. J Nutr 1995;125:2851–8.Search in Google Scholar

3. Holmes-McNary MQ, Cheng WL, Mar MH, Fussell S, Zeisel SH. Choline and choline esters in human and rat milk and in infant formulas. Am J Clin Nutr 1996;64:572–6.10.1093/ajcn/64.4.572Search in Google Scholar PubMed

4. Zeisel SH, Char D, Sheard NF. Choline, phosphatidylcholine and sphingomyelin in human and bovine milk and infant formulas. J Nutr 1986;116:50–8.10.1093/jn/116.1.50Search in Google Scholar PubMed

5. Zeisel SH, Da Costa K-A, Franklin PD, Alexander EA, Lamont JT, Sheard NF, et al. Choline, an essential nutrient for humans. FASEB J 1991;5:2093–8.10.1096/fasebj.5.7.2010061Search in Google Scholar

6. da Costa KA, Badea M, Fischer LM, Zeisel SH. Elevated serum creatine phosphokinase in choline-deficient humans: mechanistic studies in C2C12 mouse myoblasts. Am J Clin Nutr 2004;80:163–70.10.1093/ajcn/80.1.163Search in Google Scholar PubMed

7. da Costa KA, Niculescu MD, Craciunescu CN, Fischer LM, Zeisel SH. Choline deficiency increases lymphocyte apoptosis and DNA damage in humans. Am J Clin Nutr 2006;84:88–94.10.1093/ajcn/84.1.88Search in Google Scholar PubMed PubMed Central

8. Patterson KY, Bhagwat AS, Williams JR, Howe JC, Holden JM, Zeisel SH, et al. USDA database for the choline content of common foods. Release two. Available from: http://www.ars.usda.gov/Services/docs.htm?docid=6232. Accessed 15 August, 2011.Search in Google Scholar

9. Jensen HH, Batres-Marquez SP, Carriquiry A, Schalinske KL. Choline in the diets of the US population: NHANES, 2003–2004. FASEB J 2007;21:LB219.10.1096/fasebj.21.6.LB46-cSearch in Google Scholar

10. Xu X, Gammon MD, Zeisel SH, Lee YL, Wetmur JG, Teitelbaum SL, et al. Choline metabolism and risk of breast cancer in a population-based study. FASEB J 2008;22:2045–52.10.1096/fj.07-101279Search in Google Scholar PubMed PubMed Central

11. Cho E, Holmes MD, Hankinson SE, Willett WC. Choline and betaine intake and risk of breast cancer among post-menopausal women. Br J Cancer 2010;102:489–94.10.1038/sj.bjc.6605510Search in Google Scholar PubMed PubMed Central

12. Poly C, Massaro JM, Seshadri S, Wolf PA, Cho E, Krall E, et al. The relation of dietary choline to cognitive performance and white-matter hyperintensity in the Framingham Offspring Cohort. Am J Clin Nutr 2011;94:1584–91.10.3945/ajcn.110.008938Search in Google Scholar PubMed PubMed Central

13. Cho E, Willett WC, Colditz GA, Fuchs CS, Wu K, Chan AT, et al. Dietary choline and betaine and the risk of distal colorectal adenoma in women. J Natl Cancer Inst 2007;99:1224–31.10.1093/jnci/djm082Search in Google Scholar PubMed PubMed Central

14. Ibiebele TI, Hughes MC, Pandeya N, Zhao Z, Montgomery G, Hayward N, et al. High intake of folate from food sources is associated with reduced risk of esophageal cancer in an Australian population. J Nutr 2011;141:274–83.10.3945/jn.110.131235Search in Google Scholar

15. Shaw GM, Carmichael SL, Yang W, Selvin S, Schaffer DM. Periconceptional dietary intake of choline and betaine and neural tube defects in offspring. Am J Epidemiol 2004;160:102–9.10.1093/aje/kwh187Search in Google Scholar

16. Shaw GM, Finnell RH, Blom HJ, Carmichael SL, Vollset SE, Yang W, et al. Choline and risk of neural tube defects in a folate-fortified population. Epidemiology 2009;20:714–9.10.1097/EDE.0b013e3181ac9fe7Search in Google Scholar

17. Meck WH, Williams CL. Simultaneous temporal processing is sensitive to prenatal choline availability in mature and aged rats. Neuroreport 1997;8:3045–51.10.1097/00001756-199709290-00009Search in Google Scholar

18. Meck WH, Williams CL. Metabolic imprinting of choline by its availability during gestation: implications for memory and attentional processing across the lifespan. Neurosci Biobehav Rev 2003;27:385–99.10.1016/S0149-7634(03)00069-1Search in Google Scholar

19. Meck WH, Williams CL, Cermak JM, Blusztajn JK. Developmental periods of choline sensitivity provide an ontogenetic mechanism for regulating memory capacity and age-related dementia. Front Integr Neurosci 2007;1:7.Search in Google Scholar

20. Yang Y, Liu Z, Cermak JM, Tandon P, Sarkisian MR, Stafstrom CF, et al. Protective effects of prenatal choline supplementation on seizure-induced memory impairment. J Neurosci 2000;20:RC109.10.1523/JNEUROSCI.20-22-j0006.2000Search in Google Scholar

21. Holmes GL, Yang Y, Liu Z, Cermak JM, Sarkisian MR, Stafstrom CE, et al. Seizure-induced memory impairment is reduced by choline supplementation before or after status epilepticus. Epilepsy Res 2002;48:3–13.10.1016/S0920-1211(01)00321-7Search in Google Scholar

22. Wong-Goodrich SJ, Mellott TJ, Glenn MJ, Blusztajn JK, Williams CL. Prenatal choline supplementation attenuates neuropathological response to status epilepticus in the adult rat hippocampus. Neurobiol Dis 2008;30:255–69.10.1016/j.nbd.2008.01.008Search in Google Scholar

23. Wong-Goodrich SJ, Mellott TJ, Liu B, Blusztajn JK, Williams CL. Water maze experience and prenatal choline supplementation differentially promote long-term hippocampal recovery from seizures in adulthood. Hippocampus 2011;21:584–608.10.1002/hipo.20783Search in Google Scholar

24. Thomas JD, La Fiette MH, Quinn VR, Riley EP. Neonatal choline supplementation ameliorates the effects of prenatal alcohol exposure on a discrimination learning task in rats. Neurotoxicol Teratol 2000;22:703–11.10.1016/S0892-0362(00)00097-0Search in Google Scholar

25. Thomas JD, Biane JS, O’Bryan KA, O’Neill TM, Dominguez HD. Choline supplementation following third-trimester-equivalent alcohol exposure attenuates behavioral alterations in rats. Behav Neurosci 2007;121:120–30.10.1037/0735-7044.121.1.120Search in Google Scholar PubMed

26. Ryan SH, Williams JK, Thomas JD. Choline supplementation attenuates learning deficits associated with neonatal alcohol exposure in the rat: effects of varying the timing of choline administration. Brain Res 2008;1237:91–100.10.1016/j.brainres.2008.08.048Search in Google Scholar PubMed PubMed Central

27. Thomas JD, Abou EJ, Dominguez HD. Prenatal choline supplementation mitigates the adverse effects of prenatal alcohol exposure on development in rats. Neurotoxicol Teratol 2009;31:303–11.10.1016/j.ntt.2009.07.002Search in Google Scholar PubMed PubMed Central

28. Thomas JD, Idrus NM, Monk BR, Dominguez HD. Prenatal choline supplementation mitigates behavioral alterations associated with prenatal alcohol exposure in rats. Birth Defects Res 2010;88:827–37.10.1002/bdra.20713Search in Google Scholar PubMed PubMed Central

29. Thomas JD, Tran TD. Choline supplementation mitigates trace, but not delay, eyeblink conditioning deficits in rats exposed to alcohol during development. Hippocampus 2011;22: 619–30.Search in Google Scholar

30. Nag N, Berger-Sweeney JE. Postnatal dietary choline supplementation alters behavior in a mouse model of Rett syndrome. Neurobiol Dis 2007;26:473–80.10.1016/j.nbd.2007.02.003Search in Google Scholar PubMed

31. Nag N, Mellott TJ, Berger-Sweeney JE. Effects of postnatal dietary choline supplementation on motor regional brain volume and growth factor expression in a mouse model of Rett syndrome. Brain Res 2008;1237:101–9.10.1016/j.brainres.2008.08.042Search in Google Scholar PubMed

32. Ward BC, Agarwal S, Wang K, Berger-Sweeney J, Kolodny NH. Longitudinal brain MRI study in a mouse model of Rett Syndrome and the effects of choline. Neurobiol Dis 2008;31:110–9.10.1016/j.nbd.2008.03.009Search in Google Scholar PubMed

33. Ward BC, Kolodny NH, Nag N, Berger-Sweeney JE. Neurochemical changes in a mouse model of Rett syndrome: changes over time and in response to perinatal choline nutritional supplementation. J Neurochem 2009;108:361–71.10.1111/j.1471-4159.2008.05768.xSearch in Google Scholar PubMed

34. Ricceri L, De Filippis B, Fuso A, Laviola G. Cholinergic hypofunction in MeCP2–308 mice: beneficial neurobehavioural effects of neonatal choline supplementation. Behav Brain Res 2011;221:623–9.10.1016/j.bbr.2011.03.051Search in Google Scholar PubMed

35. Moon J, Chen M, Gandhy SU, Strawderman M, Levitsky DA, Maclean KN, et al. Perinatal choline supplementation improves cognitive functioning and emotion regulation in the Ts65Dn mouse model of Down syndrome. Behav Neurosci 2010;124:346–61.10.1037/a0019590Search in Google Scholar PubMed PubMed Central

36. Stevens KE, Adams CE, Yonchek J, Hickel C, Danielson J, Kisley MA. Permanent improvement in deficient sensory inhibition in DBA/2 mice with increased perinatal choline. Psychopharmacology (Berl) 2008;198:413–20.10.1007/s00213-008-1170-3Search in Google Scholar

37. Meck WH, Smith RA, Williams CL. Pre- and postnatal choline supplementation produces long-term facilitation of spatial memory. Dev Psychobiol 1988;21:339–53.10.1002/dev.420210405Search in Google Scholar

38. Schenk F, Brandner C. Indirect effect of peri- and postnatal choline treatment on place-learning abilities in rat. Psychobiology 1995;23:302–13.10.3758/BF03333077Search in Google Scholar

39. Meck WH, Williams CL. Characterization of the facilitative effects of perinatal choline supplementation on timing and temporal memory. Neuroreport 1997;8:2831–5.10.1097/00001756-199709080-00005Search in Google Scholar

40. Meck WH, Williams CL. Perinatal choline supplementation increases the threshold for chunking in spatial memory. Neuroreport 1997;8:3053–9.10.1097/00001756-199709290-00010Search in Google Scholar

41. Meck WH, Williams CL. Choline supplementation during prenatal development reduces proactive interference in spatial memory. Dev Brain Res 1999;118:51–9.10.1016/S0165-3806(99)00105-4Search in Google Scholar

42. Tees RC, Mohammadi E. The effects of neonatal choline dietary supplementation on adult spatial and configural learning and memory in rats. Dev Psychobiol 1999;35:226–40.10.1002/(SICI)1098-2302(199911)35:3<226::AID-DEV7>3.0.CO;2-HSearch in Google Scholar

43. Mellott TJ, Williams CL, Meck WH, Blusztajn JK. Prenatal choline supplementation advances hippocampal development and enhances MAPK and CREB activation. FASEB J 2004;18: NIL412–27.10.1096/fj.03-0877fjeSearch in Google Scholar

44. Buhusi CV, Lamoureux JA, Meck WH. Prenatal choline supplementation increases sensitivity to contextual processing of temporal information. Brain Res 2008;1237: 204–13.10.1016/j.brainres.2008.08.072Search in Google Scholar

45. Cheng RK, MacDonald CJ, Williams CL, Meck WH. Prenatal choline supplementation alters the timing, emotion, and memory performance (TEMP) of adult male and female rats as indexed by differential reinforcement of low-rate schedule behavior. Learn Mem 2008;15:153–62.10.1101/lm.729408Search in Google Scholar

46. Cheng RK, Scott AC, Penney TB, Williams CL, Meck WH. Prenatal-choline supplementation differentially modulates timing of auditory and visual stimuli in aged rats. Brain Res 2008;1237:167–75.10.1016/j.brainres.2008.08.062Search in Google Scholar PubMed

47. Lamoureux JA, Meck WH, Williams CL. Prenatal choline availability alters the context sensitivity of Pavlovian conditioning in adult rats. Learn Mem 2008;15:866–75.10.1101/lm.1058708Search in Google Scholar PubMed PubMed Central

48. Meck WH, Smith RA, Williams CL. Organizational changes in cholinergic activity and enhanced visuospatial memory as a function of choline administered prenatally or postnatally or both. Behav Neurosci 1989;103:1234–41.10.1037/0735-7044.103.6.1234Search in Google Scholar

49. Meck WH, Williams CL, Cermak JM, Blusztajn JK. Developmental periods of choline sensitivity provide an ontogenetic mechanism for regulating memory capacity and age-related dementia. Front Integr Neurosci 2008;1:7.10.3389/neuro.07.007.2007Search in Google Scholar PubMed PubMed Central

50. Castro CA, Rudy JW. Early-life malnutrition selectively retards the development of distal- but not proximal-cue navigation. Dev Psychobiol 1987;20:521–37.10.1002/dev.420200506Search in Google Scholar PubMed

51. Acharya MM, Hattiangady B, Shetty AK. Progress in neuroprotective strategies for preventing epilepsy. Prog Neurobiol 2008;84:363–404.10.1016/j.pneurobio.2007.10.010Search in Google Scholar PubMed PubMed Central

52. Glenn MJ, Kirby ED, Gibson EM, Wong-Goodrich SJ, Mellott TJ, Blusztajn JK, et al. Age-related declines in exploratory behavior and markers of hippocampal plasticity are attenuated by prenatal choline supplementation in rats. Brain Res 2008;1237:110–23.10.1016/j.brainres.2008.08.049Search in Google Scholar PubMed PubMed Central

53. Glenn MJ, Gibson EM, Kirby ED, Mellott TJ, Blusztajn JK, Williams CL. Prenatal choline availability modulates hippocampal neurogenesis and neurogenic responses to enriching experiences in adult female rats. Eur J Neurosci 2007;25:2473–82.10.1111/j.1460-9568.2007.05505.xSearch in Google Scholar PubMed PubMed Central

54. Wong-Goodrich SJ, Glenn MJ, Mellott TJ, Blusztajn JK, Meck WH, Williams CL. Spatial memory and hippocampal plasticity are differentially sensitive to the availability of choline in adulthood as a function of choline supply in utero. Brain Res 2008;1237:153–66.10.1016/j.brainres.2008.08.074Search in Google Scholar PubMed PubMed Central

55. Napoli I, Blusztajn JK, Mellott TJ. Prenatal choline supplementation in rats increases the expression of IGF2 and its receptor IGF2R and enhances IGF2-induced acetylcholine release in hippocampus and frontal cortex. Brain Res 2008;1237:124–35.10.1016/j.brainres.2008.08.046Search in Google Scholar PubMed

56. Parker SE, Mai CT, Canfield MA, Rickard R, Wang Y, Meyer RE, et al. Updated National Birth Prevalence estimates for selected birth defects in the United States, 2004–2006. Birth Defects Res 2010;88:1008–16.10.1002/bdra.20735Search in Google Scholar

57. Reeves RH, Irving NG, Moran TH, Wohn A, Kitt C, Sisodia SS, et al. A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat Genet 1995;11:177–84.10.1038/ng1095-177Search in Google Scholar

58. Ricceri L, De Filippis B, Laviola G. Rett syndrome treatment in mouse models: searching for effective targets and strategies. Neuropharmacology 2012 Aug 23. [Epub ahead of print].10.1016/j.neuropharm.2012.08.010Search in Google Scholar

59. Singer P, Feldon J, Yee BK. Are DBA/2 mice associated with schizophrenia-like endophenotypes? A behavioural contrast with C57BL/6 mice. Psychopharmacology (Berl) 2009;206: 677–98.10.1007/s00213-009-1568-6Search in Google Scholar

60. 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. Dev Brain Res 1999;115:123–9.10.1016/S0165-3806(99)00057-7Search in Google Scholar

61. Albright CD, Tsai AY, Friedrich CB, Mar MH, Zeisel SH. Choline availability alters embryonic development of the hippocampus and septum in the rat. Dev Brain Res 1999;113:13–20.10.1016/S0165-3806(98)00183-7Search in Google Scholar

62. 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;133:3614–8.10.1093/jn/133.11.3614Search in Google Scholar

63. Clelland CD, Choi M, Romberg C, Clemenson GD, J, Fragniere A, Tyers P, et al. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009;325:210–3.10.1126/science.1173215Search in Google Scholar

64. Kitamura T, Saitoh Y, Takashima N, Murayama A, Niibori Y, Ageta H, et al. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 2009;139:814–27.10.1016/j.cell.2009.10.020Search in Google Scholar

65. Williams CL, Meck WH, Heyer D, Loy R. Hypertrophy of basal forebrain neurons and enhanced visuospatial memory in perinatally choline-supplemented rats. Brain Res 1998;794:225–38.10.1016/S0006-8993(98)00229-7Search in Google Scholar

66. Fibiger HC. Cholinergic mechanisms in learning, memory and dementia: a review of recent evidence. TINS 1991;14: 220–3.10.1016/0166-2236(91)90117-DSearch in Google Scholar

67. Sarter M, Parikh V. Choline transporters, cholinergic transmission and cognition. Nat Rev Neurosci 2005;6:48–56.10.1038/nrn1588Search in Google Scholar

68. Cermak JM, Holler T, Jackson DA, Blusztajn JK. Prenatal availability of choline modifies development of the hippocampal cholinergic system. FASEB J 1998;12:349–57.10.1096/fasebj.12.3.349Search in Google Scholar

69. Sweatt JD. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 2001;76:1–10.10.1046/j.1471-4159.2001.00054.xSearch in Google Scholar

70. Jones JP, Meck HW, Williams CL, Wilson WA, Swartzwelder HS. Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation. Dev Brain Res 1999;118:159–67.10.1016/S0165-3806(99)00103-0Search in Google Scholar

71. Pyapali GK, Turner DA, Williams CL, Meck WH, Swartzwelder HS. Prenatal dietary choline supplementation decreases the threshold for induction of long-term potentiation in young adult rats. J Neurophysiol 1998;79:1790–6.10.1152/jn.1998.79.4.1790Search in Google Scholar

72. Montoya D, Swartzwelder HS. Prenatal choline supplementation alters hippocampal N-methyl-D-aspartate receptor-mediated neurotransmission in adult rats. Neurosci Lett 2000;296:85–8.10.1016/S0304-3940(00)01660-8Search in Google Scholar

73. Mellott TJ, Follettie MT, Diesl V, Hill AA, Lopez-Coviella I, Blusztajn JK. Prenatal choline availability modulates hippocampal and cerebral cortical gene expression. FASEB J 2007;21:1311–23.10.1096/fj.06-6597comSearch in Google Scholar PubMed

74. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012;13:484–92.10.1038/nrg3230Search in Google Scholar PubMed

75. Jones PA, Liang G. Rethinking how DNA methylation patterns are maintained. Nat Rev Genet 2009;10:805–11.10.1038/nrg2651Search in Google Scholar PubMed PubMed Central

76. Chen ZX, Riggs AD. DNA methylation and demethylation in mammals. J Biol Chem 2011;286:18347–53.10.1074/jbc.R110.205286Search in Google Scholar PubMed PubMed Central

77. Kovacheva VP, Mellott TJ, Davison JM, Wagner N, Lopez-Coviella I, Schnitzler AC, et al. Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression. J Biol Chem 2007;282:31777–88.10.1074/jbc.M705539200Search in Google Scholar PubMed

78. Lopes S, Lewis A, Hajkova P, Dean W, Oswald J, Forne T, et al. Epigenetic modifications in an imprinting cluster are controlled by a hierarchy of DMRs suggesting long-range chromatin interactions. Hum Mol Genet 2003;12:295–305.10.1093/hmg/ddg022Search in Google Scholar PubMed

79. Li E, Beard C, Jaenisch R. Role for DNA methylation in genomic imprinting. Nature 1993;366:362–5.10.1038/366362a0Search in Google Scholar PubMed

80. Chen DY, Stern SA, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D, et al. A critical role for IGF-II in memory consolidation and enhancement. Nature 2011;469:491–7.10.1038/nature09667Search in Google Scholar PubMed PubMed Central

81. 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;20:43–9.10.1096/fj.05-4707comSearch in Google Scholar PubMed PubMed Central

82. Mehedint MG, Niculescu MD, Craciunescu CN, Zeisel SH. Choline deficiency alters global histone methylation and epigenetic marking at the Re1 site of the calbindin 1 gene. FASEB J 2010;24:184–95.10.1096/fj.09-140145Search in Google Scholar PubMed PubMed Central

83. Chen WG, Chang Q, Lin YX, Meissner A, West AE, Griffith EC, et al. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 2003;302:885–9.10.1126/science.1086446Search in Google Scholar PubMed

84. 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;302:890–3.10.1126/science.1090842Search in Google Scholar PubMed

85. Levenson JM, Roth TL, Lubin FD, Miller CA, Huang IC, Desai P, et al. Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J Biol Chem 2006;281:15763–73.10.1074/jbc.M511767200Search in Google Scholar PubMed

86. Nelson ED, Kavalali ET, Monteggia LM. Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation. J Neurosci 2008;28:395–406.10.1523/JNEUROSCI.3796-07.2008Search in Google Scholar PubMed PubMed Central

87. Yossifoff M, Kisliouk T, Meiri N. Dynamic changes in DNA methylation during thermal control establishment affect CREB binding to the brain-derived neurotrophic factor promoter. Eur J Neurosci 2008;28:2267–77.10.1111/j.1460-9568.2008.06532.xSearch in Google Scholar PubMed

88. Miller CA, Sweatt JD. Covalent modification of DNA regulates memory formation. Neuron 2007;53:857–69.10.1016/j.neuron.2007.02.022Search in Google Scholar PubMed

89. Lubin FD, Roth TL, Sweatt JD. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 2008;28:10576–86.10.1523/JNEUROSCI.1786-08.2008Search in Google Scholar PubMed PubMed Central

90. Miller CA, Gavin CF, White JA, Parrish RR, Honasoge A, Yancey CR, et al. Cortical DNA methylation maintains remote memory. Nat Neurosci 2010;13:664–6.10.1038/nn.2560Search in Google Scholar PubMed PubMed Central

91. Gupta S, Kim SY, Artis S, Molfese DL, Schumacher A, Sweatt JD, et al. Histone methylation regulates memory formation. J Neurosci 2010;30:3589–99.10.1523/JNEUROSCI.3732-09.2010Search in Google Scholar PubMed PubMed Central

92. Feng J, Zhou Y, Campbell SL, Le T, Li E, Sweatt JD, et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci 2010;13: 423–30.10.1038/nn.2514Search in Google Scholar PubMed PubMed Central

93. Davison JM, Mellott TJ, Kovacheva VP, Blusztajn JK. Gestational choline supply regulates methylation of histone H3, expression of histone methyltransferases G9a (Kmt1c) and Suv39h1 (Kmt1a) and DNA methylation of their genes in rat fetal liver and brain. J Biol Chem 2009;284:1982–9.10.1074/jbc.M807651200Search in Google Scholar PubMed PubMed Central

94. Kovacheva VP, Davison JM, Mellott TJ, Rogers AE, Yang S, O’Brien MJ, et al. Raising gestational choline intake alters gene expression in DMBA-evoked mammary tumors and prolongs survival. FASEB J 2009;23:1054–63.10.1096/fj.08-122168Search in Google Scholar PubMed PubMed Central