What choline metabolism can tell us about the underlying mechanisms of fetal alcohol spectrum disorders

Molecular Neurobiology

Volumn 44, Issue 2, 2011, Pages 185-191

  Zeisel, Steven H ^a  

^a University of North Carolina   (United States)

Author keywords

Alcohol; Choline; Epigenetics; Methyl donor; Nutrition; Single nucleotide polymorphism

Indexed keywords

CHOLINE; PHOSPHATIDYLCHOLINE;

ALCOHOL CONSUMPTION; ANGIOGENESIS; ARTICLE; BRAIN DEVELOPMENT; DIETARY INTAKE; DNA METHYLATION; DRUG METABOLISM; ENDOTHELIAL PROGENITOR CELL; EPIGENETICS; FETAL ALCOHOL SPECTRUM DISORDER; FETUS DEVELOPMENT; FETUS DISEASE; GENE EXPRESSION; HIPPOCAMPUS; HISTONE METHYLATION; HUMAN; MATERNAL NUTRITION; MOUSE; NONHUMAN; RAT;

EID: 80054870870     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-011-8165-5     Document Type: Article

References (81)

1. HE Hoyme PA May WO Kalberg P Kodituwakku JP Gossage PM Trujillo DG Buckley JH Miller AS Aragon N Khaole DL Viljoen KL Jones LK Robinson 2005 A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 institute of medicine criteria Pediatrics 115 39 47 15629980 10.1542/peds.2005-0702 (Pubitemid 43843193)
2. JD Chaudhuri 2000 Alcohol and the developing fetus-a review Med Sci Monit 6 1031 1041 11208451 1:CAS:528:DC%2BD3cXosVWktbw%3D
3. PC Haycock 2009 Fetal alcohol spectrum disorders: the epigenetic perspective Biol Reprod 81 607 617 19458312 10.1095/biolreprod.108.074690 1:CAS:528:DC%2BD1MXhtFyhsLjN
4. SH Zeisel 2009 Epigenetic mechanisms for nutrition determinants of later health outcomes Am J Clin Nutr 89 1488S 1493S 19261726 10.3945/ajcn.2009.27113B 1:CAS:528:DC%2BD1MXlt1OrtLs%3D
5. W Reik W Dean J Walter 2001 Epigenetic reprogramming in mammalian development Science 293 1089 1093 11498579 10.1126/science.1063443 1:CAS:528:DC%2BD3MXmtVWltL8%3D (Pubitemid 32758081)
6. CH Halsted JA Villanueva AM Devlin O Niemela S Parkkila TA Garrow LM Wallock MK Shigenaga S Melnyk SJ James 2002 Folate deficiency disturbs hepatic methionine metabolism and promotes liver injury in the ethanol-fed micropig Proc Natl Acad Sci USA 99 10072 10077 12122204 10.1073/pnas.112336399 1:CAS:528:DC%2BD38XlslKgtL8%3D (Pubitemid 34831174)
7. C Goncalves Rde MM Vasconcelos LO Faleiros LC Cruz Jr RC Domingues AR Brito J Werner Jr GV Herdy 2009 Proton magnetic resonance spectroscopy in children with fetal alcohol spectrum disorders Arq Neuropsiquiatr 67 254 261 19547818 10.1590/S0004-282X2009000200015
8. JD Thomas EJ Abou HD Dominguez 2009 Prenatal choline supplementation mitigates the adverse effects of prenatal alcohol exposure on development in rats Neurotoxicol Teratol 31 303 311 19616089 10.1016/j.ntt.2009.07.002 1:CAS:528:DC%2BD1MXhtFSntrvE
9. Institute of Medicine, and National Academy of Sciences USA (1998) Choline. In: Dietary reference intakes for folate, thiamin, riboflavin, niacin, vitamin B12, panthothenic acid, biotin, and choline Vol. 1. National Academy Press, Washington DC, pp 390-422
10. SH Zeisel 2006 Choline: critical role during fetal development and dietary requirements in adults Annu Rev Nutr 26 229 250 16848706 10.1146/annurev.nutr.26.061505.111156 1:CAS:528:DC%2BD28Xpt1Cltr4%3D
11. SH Zeisel MH Mar JC Howe JM Holden 2003 Concentrations of choline-containing compounds and betaine in common foods J Nutr 133 1302 1307 12730414 1:CAS:528:DC%2BD3sXjs1Oqt78%3D (Pubitemid 36548698)
12. HH Jensen SP Batres-Marquez A Carriquiry KL Schalinske 2007 Choline in the diets of the U.S. population: NHANES, 2003-2004 FASEB J 21 lb219
13. SH Zeisel RJ Wurtman 1981 Developmental changes in rat blood choline concentration Biochem J 198 565 570 7034731 1:CAS:528:DyaL38XkvFKitQ%3D%3D
14. Y Ozarda Ilcol G Uncu IH Ulus 2002 Free and phospholipid-bound choline concentrations in serum during pregnancy, after delivery and in newborns Arch Physiol Biochem 110 393 399 12530624 10.1076/apab.110.5.393.11832 1:STN:280:DC%2BD3s%2FitlKrtQ%3D%3D (Pubitemid 35454399)
15. JH Sweiry KR Page CG Dacke DR Abramovich DL Yudilevich 1986 Evidence of saturable uptake mechanisms at maternal and fetal sides of the perfused human placenta by rapid paired-tracer dilution: studies with calcium and choline J Devel Physiol 8 435 445 1:CAS:528:DyaL2sXhtFOhsrc%3D (Pubitemid 17221246)
16. HE Banns NL Stephens 1974 Proceedings: investigation of choline acetylase from various tissues by use of ionizing radiation J Physiol 242 16P 18P 4455805 1:CAS:528:DyaE2MXot1Whtw%3D%3D
17. DL Yudilevich JH Sweiry 1985 Membrane carriers and receptors at maternal and fetal sides of the placenta by single circulation paired-tracer dilution: evidence for a choline transport system Contrib Gynecol Obstet 13 158 161 3888526 1:CAS:528:DyaL2MXksFSkt7o%3D (Pubitemid 15120232)
18. SH Zeisel D Char NF Sheard 1986 Choline, phosphatidylcholine and sphingomyelin in human and bovine milk and infant formulas J Nutr 116 50 58 3944656 1:CAS:528:DyaL28XhtVyis7c%3D (Pubitemid 16212055)
19. MQ Holmes-McNary WL Cheng MH Mar S Fussell SH Zeisel 1996 Choline and choline esters in human and rat milk and in infant formulas Am J Clin Nutr 64 572 576 8839502 1:CAS:528:DyaK28XmsFWmsLs%3D (Pubitemid 26334236)
20. M Resseguie J Song MD Niculescu KA da Costa TA Randall SH Zeisel 2007 Phosphatidylethanolamine N-methyltransferase (PEMT) gene expression is induced by estrogen in human and mouse primary hepatocytes FASEB J 21 2622 2632 17456783 10.1096/fj.07-8227com 1:CAS:528:DC%2BD2sXptFKhu7c%3D (Pubitemid 47230690)
21. CD Albright AY Tsai CB Friedrich MH Mar SH Zeisel 1999 Choline availability alters embryonic development of the hippocampus and septum in the rat Brain Res 113 13 20 10.1016/S0165-3806(98)00183-7 1:CAS:528: DyaK1MXht1OhtLg%3D (Pubitemid 29125266)
22. CD Albright CB Friedrich EC Brown MH Mar SH Zeisel 1999 Maternal dietary choline availability alters mitosis, apoptosis and the localization of TOAD-64 protein in the developing fetal rat septum Brain Res 115 123 129 10.1016/S0165-3806(99)00057-7 1:CAS:528:DyaK1MXkt1Cqsrk%3D (Pubitemid 29336131)
23. JP Jones W Meck CL Williams WA Wilson HS Swartzwelder 1999 Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation Brain Res 118 159 167 10.1016/S0165-3806(99)00103-0 1:CAS:528:DyaK1MXotVOjs74%3D (Pubitemid 30009649)
24. RK Cheng CJ MacDonald CL Williams WH Meck 2008 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 Lear Mem 15 153 162 10.1101/lm.729408 1:CAS:528: DC%2BD1cXotFGnsrg%3D (Pubitemid 351439145)
25. W Meck C Williams 1997 Perinatal choline supplementation increases the threshold for chunking in spatial memory NeuroReport 8 3053 3059 9331913 10.1097/00001756-199709290-00010 1:CAS:528:DyaK2sXms12rt7w%3D (Pubitemid 27421730)
26. WH Meck RA Smith CL Williams 1988 Pre- and postnatal choline supplementation produces long-term facilitation of spatial memory Dev Psychobiol 21 339 353 3378679 10.1002/dev.420210405 1:STN:280:DyaL1c3kt12ntA%3D%3D
27. WH Meck CL Williams 1999 Choline supplementation during prenatal development reduces proactive interference in spatial memory Brain Res 118 51 59 10.1016/S0165-3806(99)00105-4 1:CAS:528:DyaK1MXotVKqu7Y%3D (Pubitemid 30009637)
28. MC Fisher SH Zeisel MH Mar TW Sadler 2001 Inhibitors of choline uptake and metabolism cause developmental abnormalities in neurulating mouse embryos Teratology 64 114 122 11460263 10.1002/tera.1053 1:CAS:528:DC%2BD3MXls1GmtLk%3D (Pubitemid 32705492)
29. MC Fisher SH Zeisel MH Mar TW Sadler 2002 Perturbations in choline metabolism cause neural tube defects in mouse embryos in vitro FASEB J 16 619 621 11919173 1:CAS:528:DC%2BD38XivVOjurc%3D
30. HJ Blom GM Shaw M den Heijer RH Finnell 2006 Neural tube defects and folate: case far from closed Nat rev 7 724 731 10.1038/nrn1986 1:CAS:528:DC%2BD28XotlCgtrg%3D (Pubitemid 44267496)
31. GM Shaw SL Carmichael W Yang S Selvin DM Schaffer 2004 Periconceptional dietary intake of choline and betaine and neural tube defects in offspring Am J Epidemiol 160 102 109 15234930 10.1093/aje/kwh187 (Pubitemid 38962995)
32. E Alonso-Aperte G Varela-Moreiras 1996 Brain folates and DNA methylation in rats fed a choline deficient diet or treated with low doses of methotrexate Int J Vitam Nutr Res 66 232 236 8899457 1:CAS:528:DyaK28XmsFeqsr4%3D (Pubitemid 26369561)
33. MG Mehedint MD Niculescu CN Craciunescu SH Zeisel 2010 Choline deficiency alters global histone methylation and epigenetic marking at the Re1 site of the calbindin 1 gene FASEB J 24 184 195 19752176 10.1096/fj.09-140145
34. MD Niculescu CN Craciunescu SH Zeisel 2006 Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains FASEB J 20 43 49 16394266 10.1096/fj.05-4707com 1:CAS:528:DC%2BD28XislSntA%3D%3D (Pubitemid 43100474)
35. MD Niculescu Y Yamamuro SH Zeisel 2004 Choline availability modulates human neuroblastoma cell proliferation and alters the methylation of the promoter region of the cyclin-dependent kinase inhibitor 3 gene J Neurochem 89 1252 1259 15147518 10.1111/j.1471-4159.2004.02414.x 1:CAS:528: DC%2BD2cXkvFOkurg%3D (Pubitemid 38715843)
36. JA Chong J Tapia-Ramirez S Kim JJ Toledo-Aral Y Zheng MC Boutros YM Altshuller MA Frohman SD Kraner G Mandel 1995 REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons Cell 80 949 957 7697725 10.1016/0092-8674(95)90298-8 1:CAS:528:DyaK2MXkslOmur0%3D
37. N Ballas C Grunseich DD Lu JC Speh G Mandel 2005 REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis Cell 121 645 657 15907476 10.1016/j.cell.2005.03.013 1:CAS:528:DC%2BD2MXkslelsLY%3D (Pubitemid 40720016)
38. A Roopra R Qazi B Schoenike TJ Daley JF Morrison 2004 Localized domains of G9a-mediated histone methylation are required for silencing of neuronal genes Mol Cell 14 727 738 15200951 10.1016/j.molcel.2004.05.026 1:CAS:528: DC%2BD2cXlslemtr4%3D (Pubitemid 38780847)
39. N Ballas G Mandel 2005 The many faces of REST oversee epigenetic programming of neuronal genes Curr Opin Neurobiol 15 500 506 16150588 10.1016/j.conb.2005.08.015 1:CAS:528:DC%2BD2MXhtVynurnP (Pubitemid 41394393)
40. MG Mehedint CN Craciunescu SH Zeisel 2010 Maternal dietary choline deficiency alters angiogenesis in fetal mouse hippocampus Proc Natl Acad Sci USA 107 12834 12839 20624989 10.1073/pnas.0914328107 1:CAS:528:DC%2BC3cXpsVCrsr8%3D
41. A Eichmann C Corbel NM Le Douarin 1998 Segregation of the embryonic vascular and hemopoietic systems Biochem Cell Biol 76 939 946 10392707 10.1139/o98-106 1:CAS:528:DyaK1MXjvF2rs7Y%3D (Pubitemid 29450562)
42. A Louissaint Jr S Rao C Leventhal SA Goldman 2002 Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain Neuron 34 945 960 12086642 10.1016/S0896-6273(02)00722-5 1:CAS:528:DC%2BD38XltVygu74%3D (Pubitemid 34722284)
43. R Munoz-Chapuli JM Perez-Pomares D Macias L Garcia-Garrido R Carmona M Gonzalez 1999 Differentiation of hemangioblasts from embryonic mesothelial cells? A model on the origin of the vertebrate cardiovascular system Differentiation 64 133 141 10234810 1:STN:280:DyaK1M3ltFWiug%3D%3D (Pubitemid 29213879)
44. SJ Kinder DA Loebel PP Tam 2001 Allocation and early differentiation of cardiovascular progenitors in the mouse embryo Trends Cardiovasc Med 11 177 184 11597828 10.1016/S1050-1738(01)00091-3 1:CAS:528:DC%2BD3MXntlOqtrg%3D (Pubitemid 32946866)
45. W Risau 1997 Mechanisms of angiogenesis Nature 386 671 674 9109485 10.1038/386671a0 1:STN:280:DyaK2s3mtlGksg%3D%3D (Pubitemid 27193480)
46. Y Zhu Y Shwe R Du Y Chen FX Shen WL Young GY Yang 2006 Effects of angiopoietin-1 on vascular endothelial growth factor-induced angiogenesis in the mouse brain Acta Neurochir Suppl 96 438 443 16671501 10.1007/3-211-30714-1-90 1:STN:280:DC%2BD283kslOitw%3D%3D
47. A Zacharek J Chen X Cui A Li Y Li C Roberts Y Feng Q Gao M Chopp 2007 Angiopoietin1/Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke J Cereb Blood Flow Metab 27 1684 1691 17356562 10.1038/sj.jcbfm.9600475 1:CAS:528:DC%2BD2sXhtVKhtrjO (Pubitemid 47476100)
48. S Patan 2004 Vasculogenesis and angiogenesis Cancer Treat Res 117 3 32 15015550 10.1007/978-1-4419-8871-3-1 1:CAS:528:DC%2BD2cXptFKiuro%3D
49. VP Kovacheva TJ Mellott JM Davison N Wagner I Lopez-Coviella AC Schnitzler JK Blusztajn 2007 Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression J Biol Chem 282 31777 31788 17724018 10.1074/jbc.M705539200 1:CAS:528:DC%2BD2sXhtFyku77L (Pubitemid 350044844)
50. JM Davison TJ Mellott VP Kovacheva JK Blusztajn 2009 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 284 1982 1989 19001366 10.1074/jbc.M807651200 1:CAS:528:DC%2BD1MXlvFaksA%3D%3D
51. AJ Garro DL McBeth V Lima CS Lieber 1991 Ethanol consumption inhibits fetal DNA methylation in mice: implications for the fetal alcohol syndrome Alcohol Clin Exp Res 15 395 398 1877725 10.1111/j.1530-0277.1991.tb00536.x 1:CAS:528:DyaK3MXlt12rsLg%3D
52. PC Haycock M Ramsay 2009 Exposure of mouse embryos to ethanol during preimplantation development: effect on DNA methylation in the h19 imprinting control region Biol Reprod 81 618 627 19279321 10.1095/biolreprod.108.074682 1:CAS:528:DC%2BD1MXhtFyhsLjO
53. DM Bielawski FM Zaher DM Svinarich EL Abel 2002 Paternal alcohol exposure affects sperm cytosine methyltransferase messenger RNA levels Alcohol Clin Exp Res 26 347 351 11923587 10.1111/j.1530-0277.2002.tb02544.x 1:CAS:528: DC%2BD38XivFyjt74%3D (Pubitemid 34225839)
54. LA Ouko K Shantikumar J Knezovich P Haycock DJ Schnugh M Ramsay 2009 Effect of alcohol consumption on CpG methylation in the differentially methylated regions of H19 and IG-DMR in male gametes: implications for fetal alcohol spectrum disorders Alcohol Clin Exp Res 33 1615 1627 19519716 10.1111/j.1530-0277.2009.00993.x 1:CAS:528:DC%2BD1MXht1WhtL%2FF
55. Y-I Kim JW Miller K-A da Costa M Nadeau D Smith J Selhub SH Zeisel JB Mason 1994 Severe folate deficiency causes secondary depletion of choline and phosphocholine in liver J Nutr 124 2197 2203 7965204 1:CAS:528: DyaK2cXmvF2rsrg%3D (Pubitemid 24365246)
56. J Selhub E Seyoum EA Pomfret SH Zeisel 1991 Effects of choline deficiency and methotrexate treatment upon liver folate content and distribution Cancer Res 51 16 21 1988081 1:CAS:528:DyaK3MXnsVygtg%3D%3D
57. G Varela-Moreiras J Selhub K da Costa SH Zeisel 1992 Effect of chronic choline deficiency in rats on liver folate content and distribution J Nutr Biochem 3 519 522 10.1016/0955-2863(92)90073-R 1:CAS:528:DyaK38XmtlarsLs%3D
58. AJ Barak HC Beckenhauer DJ Tuma 1996 Betaine, ethanol, and the liver: a review Alcohol 13 395 398 8836329 10.1016/0741-8329(96)00030-4 1:CAS:528:DyaK28XlsV2rsrk%3D (Pubitemid 26286256)
59. A Biller AJ Bartsch G Homola L Solymosi M Bendszus 2009 The effect of ethanol on human brain metabolites longitudinally characterized by proton MR spectroscopy J Cereb Blood Flow Metab 29 891 902 19240741 10.1038/jcbfm.2009.12 1:CAS:528:DC%2BD1MXlt1SksL4%3D
60. JA Villanueva CH Halsted 2004 Hepatic transmethylation reactions in micropigs with alcoholic liver disease Hepatology 39 1303 1310 15122759 10.1002/hep.20168 1:CAS:528:DC%2BD2cXks1SjtLk%3D (Pubitemid 38569052)
61. N Martinez-Lopez M Varela-Rey U Ariz N Embade M Vazquez-Chantada D Fernandez-Ramos L Gomez-Santos SC Lu JM Mato ML Martinez-Chantar 2008 S-adenosylmethionine and proliferation: new pathways, new targets Biochem Soc Trans 36 848 852 18793149 10.1042/BST0360848 1:CAS:528:DC%2BD1cXhtlSrt77F
62. AP Manari VR Preedy TJ Peters 2003 Nutritional intake of hazardous drinkers and dependent alcoholics in the UK Addict Biol 8 201 210 12850779 10.1080/1355621031000117437 (Pubitemid 36859661)
63. R Jiang FB Hu EL Giovannucci EB Rimm MJ Stampfer D Spiegelman BA Rosner WC Willett 2003 Joint association of alcohol and folate intake with risk of major chronic disease in women Am J Epidemiol 158 760 771 14561666 10.1093/aje/kwg221 (Pubitemid 37237240)
64. CH Halsted EA Robles E Mezey 1973 Intestinal malabsorption in folate-deficient alcoholics Gastroenterology 64 526 532 4700768 1:STN:280:DyaE3s7mslCisQ%3D%3D
65. KE McMartin TD Collins BH Eisenga T Fortney WR Bates L Bairnsfather 1989 Effects of chronic ethanol and diet treatment on urinary folate excretion and development of folate deficiency in the rat J Nutr 119 1490 1497 2585139 1:CAS:528:DyaK3cXhslKmtA%3D%3D (Pubitemid 20001512)
66. C Ji N Kaplowitz 2003 Betaine decreases hyperhomocysteinemia, endoplasmic reticulum stress, and liver injury in alcohol-fed mice Gastroenterology 124 1488 1499 12730887 10.1016/S0016-5085(03)00276-2 1:CAS:528:DC%2BD3sXktVSktLo%3D (Pubitemid 36531821)
67. AJ Barak HC Beckenhauer ME Mailliard KK Kharbanda DJ Tuma 2003 Betaine lowers elevated s-adenosylhomocysteine levels in hepatocytes from ethanol-fed rats J Nutr 133 2845 2848 12949375 1:CAS:528:DC%2BD3sXntlaksrY%3D (Pubitemid 37099769)
68. CN Craciunescu CD Albright MH Mar J Song SH Zeisel 2003 Choline availability during embryonic development alters progenitor cell mitosis in developing mouse hippocampus J Nutr 133 3614 3618 14608083 1:CAS:528: DC%2BD3sXovFKgsbw%3D (Pubitemid 37409496)
69. KA Uban JH Sliwowska S Lieblich LA Ellis WK Yu J Weinberg LA Galea 2010 Prenatal alcohol exposure reduces the proportion of newly produced neurons and glia in the dentate gyrus of the hippocampus in female rats Horm Behav 58 835 843 20736015 10.1016/j.yhbeh.2010.08.007 1:CAS:528:DC%2BC3cXhsVWqtL7I
70. FT Crews MW Miller W Ma K Nixon WM Zawada S Zakhari 2003 Neural stem cells and alcohol Alcohol Clin Exp Res 27 324 335 12605082 10.1097/01.ALC. 0000052581.46630.C5 1:STN:280:DC%2BD3s%2FptFOjsw%3D%3D (Pubitemid 36236656)
71. DE Barnes DW Walker 1981 Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in rat hippocampus Brain Res 227 333 340 7260643 1:STN:280:DyaL3M3lsl2jtg%3D%3D (Pubitemid 11032962)
72. SD Hicks FA Middleton MW Miller 2010 Ethanol-induced methylation of cell cycle genes in neural stem cells J Neurochem 114 1767 1780 20626555 10.1111/j.1471-4159.2010.06886.x 1:CAS:528:DC%2BC3cXhtFyksr7F
73. JD Thomas NM Idrus BR Monk HD Dominguez 2010 Prenatal choline supplementation mitigates behavioral alterations associated with prenatal alcohol exposure in rats Birth Defects Res A Clin Mol Teratol 88 827 837 20706995 10.1002/bdra.20713 1:CAS:528:DC%2BC3cXht1yhsL3K
74. WH Meck CL Williams JM Cermak JK Blusztajn 2007 Developmental periods of choline sensitivity provide an ontogenetic mechanism for regulating memory capacity and age-related dementia Front Integr Neurosci 1 7 18958235
75. J Moon M Chen SU Gandhy M Strawderman DA Levitsky KN Maclean BJ Strupp 2010 Perinatal choline supplementation improves cognitive functioning and emotion regulation in the Ts65Dn mouse model of Down syndrome Behav Neurosci 124 346 361 20528079 10.1037/a0019590 1:CAS:528:DC%2BC3cXovVGgsLo%3D
76. B Hagberg J Aicardi K Dias O Ramos 1983 A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett's syndrome: report of 35 cases Ann Neurol 14 471 479 6638958 10.1002/ana.410140412 1:STN:280:DyaL2c%2FltV2mtw%3D%3D (Pubitemid 13010048)
77. BP Jung DG Jugloff G Zhang R Logan S Brown JH Eubanks 2003 The expression of methyl CpG binding factor MeCP2 correlates with cellular differentiation in the developing rat brain and in cultured cells J Neurobiol 55 86 96 12605461 10.1002/neu.10201 1:CAS:528:DC%2BD3sXivVyntbk%3D (Pubitemid 36396964)
78. J Mill A Petronis 2008 Pre- and peri-natal environmental risks for attention-deficit hyperactivity disorder (ADHD): the potential role of epigenetic processes in mediating susceptibility J Child Psychol Psychiatry 49 1020 1030 18492038 10.1111/j.1469-7610.2008.01909.x
79. J Mill T Tang Z Kaminsky T Khare S Yazdanpanah L Bouchard P Jia A Assadzadeh J Flanagan A Schumacher SC Wang A Petronis 2008 Epigenomic profiling reveals DNA-methylation changes associated with major psychosis Am J Hum Genet 82 696 711 18319075 10.1016/j.ajhg.2008.01.008 1:CAS:528:DC%2BD1cXksVGrtbY%3D (Pubitemid 351726115)
80. KA da Costa OG Kozyreva J Song JA Galanko LM Fischer SH Zeisel 2006 Common genetic polymorphisms affect the human requirement for the nutrient choline FASEB J 20 1336 1344 16816108 10.1096/fj.06-5734com (Pubitemid 44943841)
81. M Kohlmeier KA da Costa LM Fischer SH Zeisel 2005 Genetic variation of folate-mediated one-carbon transfer pathway predicts susceptibility to choline deficiency in humans Proc Natl Acad Sci USA 102 16025 16030 16236726 10.1073/pnas.0504285102 1:CAS:528:DC%2BD2MXht1Wqsr%2FN (Pubitemid 41552861)