Choline Supplementation and DNA Methylation in the Hippocampus and Prefrontal Cortex of Rats Exposed to Alcohol During Development

Alcoholism: Clinical and Experimental Research

Volumn 36, Issue 10, 2012, Pages 1701-1709

  Otero, Nicha K H ^a   Thomas, Jennifer D ^b   Saski, Christopher A ^c   Xia, Xiaoxia ^c   Kelly, Sandra J ^a,d  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b SAN DIEGO STATE UNIVERSITY   (United States)

^c CLEMSON UNIVERSITY   (United States)

^d UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Choline; DNA methylation; Fetal alcohol spectrum disorder; Hippocampus; Prefrontal cortex

Indexed keywords

ALCOHOL; CHOLINE; DNA;

ALCOHOL CONSUMPTION; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CHEMOLUMINESCENCE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DNA METHYLATION; FEMALE; FETAL ALCOHOL SYNDROME; HIPPOCAMPUS; NEWBORN; NONHUMAN; PREFRONTAL CORTEX; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; CHOLINE; DIETARY SUPPLEMENTS; DNA METHYLATION; ETHANOL; FEMALE; HIPPOCAMPUS; MALE; PREFRONTAL CORTEX; PREGNANCY; RANDOM ALLOCATION; RATS; RATS, LONG-EVANS;

ANIMALIA; RATTUS;

EID: 84866980461     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2012.01784.x     Document Type: Article

References (86)

1. Abel EL, Jacobson S, Sherwin BT (1983) In utero alcohol exposure: functional and structural brain damage. Neurobehav Toxicol Teratol 5:363-366.
2. Albright CD, Friedrich CB, Brown EC, Mar MH, Zeisel SH (1999) 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 115:123-129.
3. Albuquerque EX, Pereira EF, Braga MF, Alkondon M (1998) Contribution of nicotinic receptors to the function of synapses in the central nervous system: the action of choline as a selective agonist of α7 receptors. J Physiol Paris 92:309-316.
4. Alkondon M, Pereira EF, Cortes WS, Maelicke A, Albuquerque EX (1997) Choline is a selective agonist of α7 nicotinic acetylcholine receptors in the rat brain neurons. Eur J Neurosci 9:2734-2742.
5. Alkondon M, Pereira EFR, Eisenberg HM, Albuquerque EX (1999) Choline and selective antagonists identify two subtypes of nicotinic actylcholine receptors that modulate GABA release from CA1 interneurons in rat hippocampal slices. J Neurosci 19:2693-2705.
6. Anisowicz A, Huang H, Braunschweiger K, Liu Z, Giese H, Wang H, Mamaev S, Olejnik J, Massion P, Mastro R (2008) A high-throughput and sensitive method to measure global DNA methylation: application in lung cancer. BMC Cancer 8:222.
7. Archibald SL, Fennema-Notestine C, Gamst A, Riley EP, Mattson SN, Jernigan TL (2001) Brain dysmorphology in individuals with severe prenatal alcohol exposure. Dev Med Child Neurol 43:148-154.
8. Autti-Ramo I, Autti T, Korkman M, Kettunen S, Salonen O, Valanne L (2002) MRI findings in children with school problems who had been exposed prenatally to alcohol. Dev Med Child Neurol 44:98-106.
9. Ba A, Seri BV, Han SH (1996) Thiamine administration during chronic alcohol intake in pregnant and lactating rats: effects on the offspring neurobehavioural development. Alcohol Alcohol 31:27-40.
10. Barnes DE, Walker DW (1981) Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in rat hippocampus. Brain Res 227:333-340.
11. Bayer SA, Altman J, Russo RJ, Zhang X (1993) Timtables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14:83-144.
12. Berman RF, Hannigan JH (2000) Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy. Hippocampus 10:94-110.
13. Blusztajn JK (1998) Choline, a vital amine. Science 281:794-795.
14. Cermak JM, Holler T, Jackson DA, Blusztajn JK (1998) Prenatal availability of choline modifies development of the hippocampal cholinergic system. FASEB J 12:349-357.
15. Connor PD, Sampson PD, Bookstein FL, Barr HM, Streissguth AP (2000) Direct and indirect effects of prenatal alcohol damage on executive function. Dev Neuropsychol 18:331-354.
16. Davies DL, Smith DE (1981) A golgi study of mouse hippocampal CA1 pyramidal neurons following perinatal alcohol exposure. Neurosci Lett 26:49-54.
17. Davison JM, Mellott TJ, Kovacheva VP, Blusztajn JK (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.
18. Diaz-Granados JL, Greene PL, Amsel A (1993) Mitigating effects of combined prenatal and postnatal exposure to ethanol on learned persistence in the weanling rat: a replication under high-peak conditions. Behav Neurosci 107:1059-1066.
19. Dobbing J, Sands J (1979) Comparative aspects of the brain growth spurt. Early Hum Dev 3:79-83.
20. Driscoll CD, Streissguth AP, Riley EP (1990) Prenatal alcohol exposure: comparability of effects on humans and animal models. Neurotoxicol Teratol 12:231-238.
21. Dudek BC, Abbott ME (1984) A biometrical genetic analysis of ethanol response in selectively bred long-sleep and short-sleep mice. Behav Genet 14:1-19.
22. Ferrer I, Galofre F, Lopez-Tejero D, Llobera M (1988) Morphological recovery of hippocampal pyramidal neurons in the adult rat exposed in utero to ethanol. Toxicology 48:191-197.
23. Garro AJ, McBeth DL, Lima V, Lieber CS (1991) Ethanol consumption inhibits DNA methylation in mice: implication for the fetal alcohol syndrome. Alcohol Clin Exp Res 15:395-398.
24. Greene PL, Diaz-Granados JL, Amsel A (1992) Blood ethanol concentration from early postnatal exposure: effects on memory-based learning and hippocampal neuroanatomy in infant and adult rats. Behav Neurosci 106:51-61.
25. Hannigan JH (1996) What research with animals is telling us about alcohol-related neurodevelopmental disorder. Pharmacol Biochem Behav 55:489-499.
26. Hannigan JH, Abel EL (1996) Animal models for the study of alcohol-related birth defects, in Alcohol Pregnancy and Child Development (Spohr H-L, Steinhaussen H-C eds), pp 77-102. Cambridge University Press, Cambridge.
27. Haycock PC (2009) Fetal alcohol spectrum disorders: the epigenetic perspective. Biol Reprod 81:607-617.
28. Inomata K, Nasu F, Tanaka H (1987) Decreased density of synaptic formation in the frontal cortex of neonatal rats exposed to ethanol in utero. Int J Dev Neurosci 5:455-460.
29. Jhaveri MS, Wagner C, Trepel JB (2001) Impact of extracellular folate levels on global gene expression. Mol Pharmacol 60:1288-1295.
30. Jiang YH, Bressler J, Beaudet AL (2004) Epigenetics and human disease. Annu Rev Genomics Hum Genet 5:479-510.
31. Jones KL, Smith DW (1973) Recognition of fetal alcohol syndrome in early infancy. Lancet 302:999-1001.
32. Kaminen-Ahola N, Ahola A, Maga M, Mallitt K-A, Fahey P, Cox TC, Whitelaw E, Chong S (2010) Maternal ethanol consumption alters the epigenotype and the phenotype of offspring in a mouse model. PLoS Genet 6:e1000811.
33. Kodituwakku PW, Kalberg W, May PA (2001) The effects of prenatal alcohol exposure on executive functioning. Alcohol Res Health 25:192-198.
34. Kovacheva VP, Mellott TJ, Davison JM, Wagner N, Lopez-Coviella I, Schnitzler AC, Blusztajn JK (2007) Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression. J Biol Chem 282:31777-31788.
35. Landesman-Dwyer S, Keller LS, Streissguth AP (1978) Naturalistic observations of newborns: effects of maternal alcohol intake. Alcohol Clin Exp Res 2:171-177.
36. Li Q, Guo-Ross S, Lewis DV, Turner D, White AM, Wilson WA, Swartzwelder HS (2004) Dietary prenatal choline supplementation alters postnatal hippocampal structure and function. J Neurophysiol 91:1545-1555.
37. Liu L, van Groen T, Kadish I, Tollefsbol TO (2009a) DNA methylation impacts on learning and memory in aging. Neurobiol Aging 30:549-560.
38. Liu Y, Balaraman Y, Wang G, Nephew KP, Zhou FC (2009b) Alcohol exposure alters DNA methylation profiles in mouse embryos at early neurulation. Epigenetics 4:500-511.
39. Marino MD, Cronise K, Lugo J, Kelly SJ (2002) Ultrasonic vocalizations and maternal infant interactions in a rat model of fetal alcohol syndrome. Dev Psychobiol 41:341-351.
40. Mattson SN, Riley EP, Gramling L, Delis DC, Jones KL (1997) Heavy prenatal alcohol exposure with or without physical features of fetal alcohol syndrome leads to IQ deficits. J Pediatr 131:718-721.
41. Mehedint MG, Niculescu MD, Craciunescu CN, Zeisel SH (2010) Choline deficiency alters global histone methylation and epigenetic marking at the Rel site of the calbindin 1 gene. FASEB J 24:184-195.
42. Miller MW (1995) Generation of neurons in the rat dentate gyrus and hippocampus: effects of prenatal and postnatal treatment with ethanol. Alcohol Clin Exp Res 19:1500-1509.
43. Monk BR, Leslie FM, Thomas JD (in press) The effects of perinatal choline supplementation on hippocampal cholinergic development in rats exposed to alcohol during the brain growth spurt. Hippocampus doi: 10.1002/hipo.22009 [Epub ahead of print].
44. Montoya D, Swartzwelder HS (2000) Prenatal choline supplementation alters hippocampal N methyl-D-aspartate receptor-mediated neurotransmission in adult rats. Neurosci Lett 296:85-88.
45. Moretti P, Levenson JM, Battaglia F, Atkinson R, Teague R, Antalffy B, Armstrong D, Arancio O, Sweatt JD, Zoghbi HY (2006) Learning and memory and synaptic plasticity are impaired in a mouse model of rett syndrome. J Neurosci 26:319-327.
46. Nagahara AH, Handa RJ (1995) Fetal alcohol exposure alters the induction of immediate early gene mRNA in the rat prefrontal cortex after an alternation task. Alcohol Clin Exp Res 19:1389-1397.
47. Napoli I, Blusztajn JK, Mellott TJ (2008) 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 1237:124-135.
48. Niculescu MD, Craciunescu CN, Zeisel SH (2006) Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains. FASEB J 20:43-49.
49. Niculescu MD, Yamamuro Y, Zeisel SH (2004) Choline availability modulates human neuroblastoma cell proliferation and alters the methylation of the promoter region of the cyclin dependent kinase inhibitor gene. J Neurochem 89:1252-1259.
50. Perez HD, Villanueva JE, Salas JM (1991) Behavioral and hippocampal morphological changes induced by ethanol administration to pregnant rats. Annals N Y Acad Sci 625:300-304.
51. Pogribny IP, Karpf AR, James SR, Melnyk S, Han T, Tryndyak VP (2008) Epigenetic alterations in the brain of Fisher 344 rats induced by long-term administration of folate/methyl-deficient diet. Brain Res 1237:25-34.
52. Pogribny IP, Ross SA, Wise C, Pogribna M, Jones EA, Tryndyak VP, James SJ, Dragan YP, Poirier LA (2006) Irreversible global DNA hypomethylation as a key step in hepatocarcinogenesis induced by dietary methyl deficiency. Mutat Res 593:80-87.
53. Riikonen R, Salonen I, Partanen K, Verho S (1999) Brain perfusion SPECT and MRI in foetal alcohol syndrome. Dev Med Child Neurol 41:652-659.
54. Robertson KD (2005) DNA methylation and human disease. Nat Rev Genet 6:597-610.
55. Ryan SH, Williams JK, Thomas JD (2008) Choline supplementation attenuates learning deficits associated with neonatal alcohol exposure in the rat: effects of varying the timing of choline administration. Brain Res 1237:91-100.
56. Sandstrom NJ, Loy R, Williams CL (2002) Prenatal choline supplementation increases NGF levels in the hippocampus and frontal cortex of young and adult rats. Brain Res 947:9-16.
57. Smith DE, Davies DL (1990) Effect of perinatal administration of ethanol on the CA1 pyramidal cell of the hippocampus and Purkinje cell of the cerebellum: an ultrastructural survey. J Neurocytol 19:708-717.
58. Sowell ER, Lu LH, O'Hare ED, McCourt ST, Mattson SN, O'Connor MJ, Bookheimer SY (2007) Functional magnetic resonance imaging of verbal learning in children with heavy prenatal alcohol exposure. Neuroreport 18:635-639.
59. Sowell ER, Thompson PM, Mattson SN, Tessner KD, Jernigan TL, Riley EP, Toga AW (2002) Regional brain shape abnormalities persist into adolescence after heavy prenatal alcohol exposure. Cereb Cortex 12:856-865.
60. Streissguth AP, O'Malley K (2000) Neuropsychiatric implications and long-term consequences of fetal alcohol spectrum disorders. Semin Clin Neuropsychiatry 5:177-190.
61. Tanaka H (1998) Fetal alcohol syndrome: a Japanese perspective. Ann Med 30:21-26.
62. Thomas JD, Abou EJ, Dominguez HD (2009) Prenatal choline supplementation mitigates the adverse effects of prenatal alcohol exposure on development in rats. Neurotoxicol Teratol 31:303-311.
63. Thomas JD, Biane JS, O'Bryan KA, O'Neill TM, Dominguez HD (2007) Choline supplementation following third-trimester-equivalent alcohol exposure attenuates behavioral alterations in rats. Behav Neurosci 121:120-130.
64. Thomas JD, Garrison M, O'Neill TM (2004) Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol 26:35-45.
65. Thomas JD, La Fiette MH, Quinn VRE, Riley EP (2000) Neonatal choline supplementation ameliorates the effects of prenatal alcohol exposure on a discrimination learning task in rats. Neurotoxicol Teratol 22:703-711.
66. Thomas JD, Tran TD (2012) Choline supplementation mitigates trace, but not delay, eyeblink conditioning deficits in rats exposed to alcohol during development. Hippocampus 22:619-630.
67. Tran TD, Kelly SJ (2003) Critical periods for ethanol-induced cell loss in the hippocampal formation. Neurotoxicol Teratol 25:519-528.
68. Uecker A, Nadel L (1998) Spatial but not object memory impairments in children with fetal alcohol syndrome. Am J Ment Retard 103:12-18.
69. Uteshev VV, Meyer EM, Papke RL (2003) Regulation of neuronal function by choline and 4OH GTS-21 through α7 nicotinic receptors. J Neurophysiol 89:1797-1806.
70. Wagner AF, Hunt PS (2006) Impaired trace fear conditioning following neonatal ethanol: reversal by choline. Behav Neurosci 120:482-487.
71. Waterland RA, Dolinoy DC, Lin J-R, Smith CA, Shi X, Tahiliani KG (2006) Maternal methyl supplements increase offspring DNA methylation at axin fused. Genesis 44:401-406.
72. Waterland RA, Jirtle RL (2003) Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23:5293-5300.
73. West JR, Hamre KM, Pierce DR (1984) Delay in brain growth induced by alcohol in artificially reared rat pups. Alcohol 1:213-222.
74. West JR, Hodges CA, Black AC (1981) Prenatal exposure to ethanol alters the organization of hippocampal mossy fibers in rats. Science 211:957-959.
75. West JR, Hodges-Savola CA (1983) Permanent hippocampal mossy fiber hyperdevelopment following prenatal ethanol exposure. Neurobehav Toxicol Teratol 5:139-150.
76. West JR, Pierce DR (1984) The effect of in utero ethanol exposure on hippocampal mossy fibers: an HRP study. Brain Res 317:275-279.
77. Whitcher LT, Klintsova AY (2008) Postnatal binge-like alcohol exposure reduces spine density without affecting dendritic morphology in rat mPFC. Synapse 62:566-573.
78. Wigal T, Amsel A (1990) Behavioral and neuroanatomical effects of prenatal, postnatal, or combined exposure to ethanol in weanling rats. Behav Neurosci 104:116-126.
79. Williams CL, Meck WH, Heyer DD, Loy R (1998) Hypertrophy of basal forebrain neurons and enhanced visuospatial memory in perinatally choline supplemented rats. Brain Res 794:225-238.
80. Willoughby KA, Sheard ED, Nash K, Rovet J (2008) Effects of prenatal alcohol exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood. J Int Neuropsychol Soc 14:1022-1033.
81. Wong-Goodrich SJE, Glenn MJ, Mellott TJ, Blusztajn JK, Meck WH, Williams CL (2008a) 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 1237:153-166.
82. Wong-Goodrich SJE, Mellott TJ, Glenn MJ, Blusztajn JK, Williams CL (2008b) Prenatal choline supplementation attenuates neuropathological response to status epilepticus in the adult rat hippocampus. Neurobiol Dis 30:255-269.
83. Zeisel SH (2011) What choline metabolism can tell us about the underlying mechanisms of fetal alcohol spectrum disorders. Mol Neurobiol 44:185-191.
84. Zeisel SH, Blusztajn JK (1994) Choline and human nutrition. Annu Rev Nutr 14:269-296.
85. Zeisel SH, Niculescu MD (2006) Perinatal choline influences brain structure and function. Nutr Rev 64:197-203.
86. Zhou FC, Zhao Q, Liu Y, Goodlett CR, Lian T, McClintick JN, Edenberg HJ, Li L (2011) Alteration of gene expression by alcohol exposure at early neurulation. BMC Genomics 12: 124.