Fetal alcohol spectrum disorders: The epigenetic perspective

Biology of Reproduction

Volumn 81, Issue 4, 2009, Pages 607-617

  Haycock, Philip C ^a  

^a UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

Epigenetics; Ethanol; Fetal alcohol spectrum disorders; Teratogenesis; Toxicology

Indexed keywords

ALCOHOL;

ANIMAL; FEMALE; FETAL ALCOHOL SYNDROME; GENETIC EPIGENESIS; GENETICS; HUMAN; MALE; PREGNANCY; REVIEW;

ANIMALS; EPIGENESIS, GENETIC; ETHANOL; FEMALE; FETAL ALCOHOL SYNDROME; HUMANS; MALE; PREGNANCY;

EID: 70149095265     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.074690     Document Type: Short Survey

References (115)

1. Astley SJ. Fetal alcohol syndrome prevention in Washington State: evidence of success. Paediatr Perinat Epidemiol 2004; 18: 344-351.
2. Hoyme HE, May PA, Kalberg WO, Kodituwakku P, Gossage JP, Trujillo PM, Buckley DG. Miller JH, Aragon AS, Khaole N, Viljoen DL, Jones KL, et al. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 institute of medicine criteria. Pediatrics 2005; 115: 39-47.
3. Jones KL, Smith DW. Recognition of the fetal alcohol syndrome in early infancy. Lancet 1973; 2: 999-1001.
4. Jones KL, Smith DW, Ulleland CN, Streissguth P. Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1973; 1: 1267-1271.
5. Chaudhuri JD. Alcohol and the developing fetus-a review. Med Sci Monit 2000; 6: 1031-1041.
6. Resnicoff M, Rubini M, Baserga R, Rubin R. Ethanol inhibits insulinlike growth factor-1-mediated signalling and proliferation of C6 rat glioblastoma cells. Lab Invest 1994; 71: 657-662.
7. Goodlett CR, Horn KH. Mechanisms of alcohol-induced damage to the developing nervous system. Alcohol Res Health 2001; 25: 175-184.
8. Armant DR. Saunders DE. Exposure of embryonic cells to alcohol: contrasting effects during preimplantation and postimplantation development. Semin Perinatol 1996; 20: 127-139.
9. Wozniak DF, Hartman RE, Boyle MP, Vogt SK, Brooks AR, Tenkova T, Young C, Olney JW, Muglia LJ. Apoptotic neurodegeneration induced by ethanol in neonatal mice is associated with profound learning/memory deficits in juveniles followed by progressive functional recovery in adults. Neurobiol Dis 2004; 17: 403-414.
10. Warren KR, Li TK. Genetic polymorphisms: impact on the risk of fetal alcohol spectrum disorders. Birth Defects Res A Clin Mol Teratol 2005; 73: 195-203.
11. Jablonka E, Lamb MJ. Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life. Cambridge, MA: MIT Press; 2005.
12. Arney KL, Fisher AG. Epigenetic aspects of differentiation. J Cell Sci 2004; 117: 4355-4363.
13. Shukla SD, Velazquez J, French SW, Lu SC, Ticku MK, Zakhari S. Emerging role of epigenetics in the actions of alcohol. Alcohol Clin Exp Res 2008; 32: 1525-1534.
14. Hsieh J, Gage FH. Epigenetic control of neural stem cell fate. Curr Opin Genet Dev 2004; 14: 461-469.
15. Cheung P, Lau P. Epigenetic regulation by histone methylation and histone variants. Mol Endocrinol 2005; 19: 563-573.
16. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001; 293: 1089-1093.
17. Kurukuti S, Tiwari VK, Tavoosidana G, Pugacheva E, Murrell A, Zhao Z, Lobanenkov V, Reik W, Ohlsson R. CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc Natl Acad Sci U S A 2006; 103: 10684-10689.
18. Lopes S, Lewis A, Hajkova P, Dean W, Oswald J, Forne T, Murrell A, Constancia M, Bartolomei M, Walter J, Reik W. 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.
19. Murrell A, Heeson S, Reik W. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat Genet 2004; 36: 889-893.
20. Guy J, Hendrich B, Holmes M, Martin JE, Bird A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 2001; 27: 322-326.
21. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 2002; 3: 662-673.
22. Hendrich B, Guy J, Ramsahoye B, Wilson VA, Bird A. Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev 2001; 15: 710-723.
23. Moazed D. Small RNAs in transcriptional gene silencing and genome defence. Nature 2009; 457: 413-420.
24. Pelissier T, Wassenegger M. A DNA target of 30 bp is sufficient for RNA-directed DNA methylation. RNA 2000; 6: 55-65.
25. Wassenegger M, Heimes S, Riedel L, Sanger HL. RNA-directed de novo methylation of genomic sequences in plants. Cell 1994; 76: 567-576.
26. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caeno-rhabditis elegans. Nature 1998; 391: 806-811.
27. Cooney CA, Dave AA, Wolff GL. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr 2002; 132: 2393S-2400S.
28. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 2003; 23: 5293-5300.
29. Garro AJ, McBeth DL, Lima V, Lieber CS. Ethanol consumption inhibits fetal DNA methylation in mice: implications for the fetal alcohol syndrome. Alcohol Clin Exp Res 1991; 15: 395-398.
30. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic trans-generational actions of endocrine disrupters and male fertility. Science 2005; 308: 1466-1469.
31. Newbold RR, Padilla-Banks E, Jefferson WN. Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology 2006; 147:S11-S17.
32. Thompson SL, Konfortova G, Gregory RI, Reik W, Dean W, Feil R. Environmental effects on genomic imprinting in mammals. Toxicol Lett 2001; 120: 143-150.
33. Wu Q, Ohsako S, Ishimura R, Suzuki JS, Tohyama C. Exposure of mouse preimplantation embryos to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) alters the methylation status of imprinted genes H19 and Igf2. Biol Reprod 2004; 70: 1790-1797.
34. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7: 847-854.
35. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, Walter J, Surani MA. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 2002; 117: 15-23.
36. Bai S, Ghoshal K, Datta J, Majumder S, Yoon SO, Jacob ST. DNA methyltransferase 3b regulates nerve growth factor-induced differentia-tion of PC 12 cells by recruiting histone deacetylase 2. Mol Cell Biol 2005; 25: 751-766.
37. Fan G, Martinowich K, Chin MH, He F, Fouse SD, Hutnick L, Hattori D, Ge W, Shen Y, Wu H, ten Hoeve J, Shuai K, et al. DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 2005; 132: 3345-3356.
38. Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M, Burton J, Cox TV, Davies R, Down TA, Haefliger C, Horton R, et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 2006; 38: 1378-1385.
39. Halsted CH, Villanueva JA, Devlin AM, Niemela O, Parkkila S, Garrow TA, Wallock LM, Shigenaga MK, Melnyk S, James SJ. Folate deficiency disturbs hepatic methionine metabolism and promotes liver injury in the ethanol-fed micropig. Proc Natl Acad Sci U S A 2002; 99: 10072-10077.
40. Bielawski DM, Zaher FM, Svinarich DM, Abel EL. Paternal alcohol exposure affects sperm cytosine methyltransferase messenger RNA levels. Alcohol Clin Exp Res 2002; 26: 347-351.
41. Pietrzykowski AZ, Friesen RM, Martin GE, Puig SI, Nowak CL, Wynne PM, Siegelmann HT, Treistman SN. Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 2008; 59: 274-287.
42. Cravo ML, Gloria LM, Selhub J, Nadeau MR, Camilo ME, Resende MP, Cardoso JN, Leitao CN, Mira FC. Hyperhomocysteinemia in chronic alcoholism: correlation with folate, vitamin B-12, and vitamin B-6 status. Am J Clin Nutr 1996; 63: 220-224.
43. Park PH, Lim RW, Shukla SD. Involvement of histone acetyltransferase (HAT) in ethanol-induced acetylation of histone H3 in hepatocytes: potential mechanism for gene expression. Am J Physiol Gastrointest Liver Physiol 2005; 289: G1124-G1136.
44. Mistilis SP, Birchall A. Induction of alcohol dehydrogenase in the rat. Nature 1969; 223: 199-200.
45. Kim JS, Shukla SD. Acute in vivo effect of ethanol (binge drinking) on histone H3 modifications in rat tissues. Alcohol Alcohol 2006; 41: 126-132.
46. Pal-Bhadra M, Bhadra U, Jackson DE, Mamatha L, Park PH, Shukla SD. Distinct methylation patterns in histone H3 at Lys-4 and Lys-9 correlate with up- & down-regulation of genes by ethanol in hepatocytes. Life Sci 2007; 81: 979-987.
47. Lee YJ, Shukla SD. Histone H3 phosphorylation at serine 10 and serine 28 is mediated by p38 MAPK in rat hepatocytes exposed to ethanol and acetaldehyde. Eur J Pharmacol 2007; 573: 29-38.
48. Becker HC, Diaz-Granados JL, Randall CL. Teratogenic actions of ethanol in the mouse: a minireview. Pharmacol Biochem Behav 1996; 55: 501-513.
49. May PA, Gossage JP, Brooke LE, Snell CL, Marais AS, Hendricks LS, Croxford JA, Viljoen DL. Maternal risk factors for fetal alcohol syndrome in the Western cape province of South Africa: a population-based study. Am J Public Health 2005; 95: 1190-1199.
50. Lindblad B, Olsson R. Unusually high levels of blood alcohol? JAMA 1976; 236: 1600-1602.
51. Gohlke JM, Griffith WC, Faustman EM. A systems-based computational model for dose-response comparisons of two mode of action hypotheses for ethanol-induced neurodevelopmental toxicity. Toxicol Sci 2005; 86: 470-484.
52. Pantazis NJ, Dohrman DP, Luo J, Goodlett CR, West JR. Alcohol reduces the number of pheochromocytoma (PC12) cells in culture. Alcohol 1992; 9: 171-180.
53. Hanson F, Florence H. The effects of alcohol on birth weight and litter size in the albino rat. Am Nat 1927; 61: 503-519.
54. Hanson F, Florence H. Do albino rats having ten generations of alcoholic ancestry inherit resistance to alcohol fumes? Am Nat 1927 61: 43-53.
55. Hanson F, Handy V. The effects of alcohol fumes on the albino rat: introduction and sterility data for the first treated generation. Am Nat 1923; 57: 532-544.
56. MacDowell E. Experiments with alcohol and white rats. Am Nat 1922; 56: 289-311.
57. Nice L. Further observations on the effects of alcohol on white mice. Am Nat 1917; 51: 596-607.
58. Pearl R. Some effects of the continued administration of alcohol to the domestic fowl, with special reference to the progeny. Proc Natl Acad Sci USA 1916; 2: 675-683.
59. Whitney D. The effects of alcohol not inherited in hydatina senta. Am Nat 1912; 46: 41-56.
60. Stockard C. The effect on the offspring of intoxicating the male parent and the transmission of the defects to subsequent generations. Am Nat 1913; 47: 641-682.
61. Little RE, Sing CF. Father's drinking and infant birth weight: report of an association. Teratology 1987; 36: 59-65.
62. Hegedus AM, Tarter RE, Hill SY, Jacob T, Winsten NE. Static ataxia: a possible marker for alcoholism. Alcohol Clin Exp Res 1984; 8: 580-582.
63. Tarter RE, Hegedus AM, Goldstein G, Shelly C, Alterman AI. Adolescent sons of alcoholics: neuropsychological and personality characteristics. Alcohol Clin Exp Res 1984; 8: 216-222.
64. Abel E. Paternal contribution to fetal alcohol syndrome. Addict Biol 2004; 9: 127-133; discussion 135-136.
65. Anderson RA Jr, Furby JE, Oswald C, Zaneveld LJ. Tetratological evaluation of mouse fetuses after paternal alcohol ingestion. Neurobehav Toxicol Teratol 1981; 3: 117-120.
66. Cicero TJ, Adams ML, O'Connor L, Nock B, Meyer ER, Wozniak D. Influence of chronic alcohol administration on representative indices of puberty and sexual maturation in male rats and the development of their progeny. J Pharmacol Exp Ther 1990; 255: 707-715.
67. Mankes RF, LeFevre R, Benitz KF, Rosenblum T, Bates H, Walker AI, Abraham R, Rockwood W. Paternal effects of ethanol in the long-evans rat. J Toxicol Environ Health 1982; 10: 871-878.
68. Abel EL. Rat offspring sired by males treated with alcohol. Alcohol 1993; 10: 237-242.
69. Randall CL, Burling TA, Lochry EA, Sutker PB. The effect of paternal alcohol consumption on fetal development in mice. Drug Alcohol Depend 1982; 9: 89-95.
70. Abel EL. A surprising effect of paternal alcohol treatment on rat fetuses. Alcohol 1995; 12: 1-6.
71. Abel EL. Effects of physostigmine on male offspring sired by alcohol-treated fathers. Alcohol Clin Exp Res 1994; 18: 648-652.
72. Abel EL, Lee JA. Paternal alcohol exposure affects offspring behavior but not body or organ weights in mice. Alcohol Clin Exp Res 1988: 12: 349-355.
73. Abel EL, Bilitzke P. Paternal alcohol exposure: paradoxical effect in mice and rats. Psychopharmacology (Berl) 1990; 100: 159-164.
74. Abel EL, Tan SE. Effects of paternal alcohol consumption on pregnancy outcome in rats. Neurotoxicol Teratol 1988; 10: 187-192.
75. Bielawski DM, Abel EL. Acute treatment of paternal alcohol exposure produces malformations in offspring. Alcohol 1997; 14: 397-401.
76. Cicero TJ, Nock B, O'Connor LH, Sewing BN, Adams ML, Meyer ER. Acute paternal alcohol exposure impairs fertility and fetal outcome. Life Sci 1994; 55: PL33-PL36.
77. Livy DJ, Maier SE, West JR. Long-term alcohol exposure prior to conception results in lower fetal body weights. Birth Defects Res B Dev Reprod Toxicol 2004; 71: 135-141.
78. Becker HC, Randall CL. Two generations of maternal alcohol consumption in mice: effect on pregnancy outcome. Alcohol Clin Exp Res 1987; 11: 240-242.
79. Little RE, Streissguth AP, Barr HM, Herman CS. Decreased birth weight in infants of alcoholic women who abstained during pregnancy. J Pediatr 1980; 96: 974-977.
80. Anway MD, Skinner MK. Epigenetic transgenerational actions of endocrine disrupters. Endocrinology 2006; 147: S43-S49.
81. Cropley JE, Suter CM, Beckman KB, Martin DI. Germ-line epigenetic modification of the murine A vy allele by nutritional supplementation. Proc Natl Acad Sci U S A 2006; 103: 17308-17312.
82. Bygren LO, Kaati G, Edvinsson S. Longevity determined by paternal ancestors' nutrition during their slow growth period. Acta Biotheor 2001; 49: 53-59.
83. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjostrom M, Golding J. Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 2006; 14: 159-166.
84. Padmanabhan R, Hameed MS. Effects of acute doses of ethanol administered at pre-implantation stages on fetal development in the mouse. Drug Alcohol Depend 1988; 22: 91-100.
85. Mitchell JA. Effects of alcohol on blastocyst implantation and fecundity in the rat. Alcohol Clin Exp Res 1994; 18: 29-34.
86. Checiu M, Sandor S. The effect of ethanol upon early development in mice and rats. IX. Late effect of acute preimplantation intoxication in mice. Morphol Embryol (Bucur) 1986; 32: 5-11.
87. Clarren SK, Astley SJ. Pregnancy outcomes after weekly oral administration of ethanol during gestation in the pig-tailed macaque: comparing earlv gestational exposure to full gestational exposure. Teratology 1992; 45: 1-9.
88. Stacheeki JJ, Yelian FD, Leach RE, Armant DR. Mouse blastocyst outgrowth and implantation rates following exposure to ethanol or A23187 during culture in vitro. J Reprod Fertil 1994; 101: 611-617.
89. Sinclair K, Young L, Wilmut I, McEvoy T. In-utero overgrowth in ruminants following embryo culture: lessons from mice and a warning to men. Hum Reprod 2000; 15(suppl 5): 68-86.
90. Walker S, Hartwich K, Seamark R. The production of unusually large offspring following embryo manipulation: concepts and challenges. Theriogenology 1996; 45: 111-120.
91. Young LE, Sinclair KD, Wilmut I. Large offspring syndrome in cattle and sheep. Rev Reprod 1998; 3: 155-163.
92. Dean W, Bowden L, Aitchison A, Klose J, Moore T, Meneses JJ, Reik W, Feil R. Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes. Development 1998; 125: 2273-2282.
93. Khosla S, Dean W, Brown D, Reik W, Feil R. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol Reprod 2001; 64: 918-926.
94. McLaren A. Cloning: pathways to a pluripotent future. Science 2000; 288: 1775-1780.
95. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci U S A 1993; 90: 8424-8428.
96. Khosla S, Dean W, Reik W, Feil R. Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. Hum Reprod Update 2001; 7: 419-427.
97. Haycock PC, Ramsay M. Exposure of mouse embryos to ethanol during preimplantation development: effect on DNA methylation in the HI 9 imprinting control region. Biol Reprod 2009; 81: 618-627.
98. Spadoni AD, McGee CL, Fryer SL, Riley EP. Neuroimaging and fetal alcohol spectrum disorders. Neurosci Biobehav Rev 2007; 31: 239-245.
99. Nixon K, Crews FT. Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J Neurochem 2002; 83: 1087-1093.
100. He J, Nixon K, Shetty AK, Crews FT. Chronic alcohol exposure reduces hippocampal neurogenesis and dendritic growth of newborn neurons. Eur J Neurosci 2005; 21: 2711-2720.
101. Tateno M, Ukai W, Yamamoto M, Hashimoto E, Ikeda H, Saito T. The effect of ethanol on cell fate determination of neural stem cells. Alcohol Clin Exp Res 2005; 29: 225S-229S.
102. Ballas N, Grunseich C, Lu DD, Speh JC, Mandel G. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 2005; 121: 645-657.
103. Kuwabara T, Hsieh J, Nakashima K, Taira K, Gage FH. A small modulatory dsRNA specifies the fate of adult neural stem cells. Cell 2004; 116: 779-793.
104. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M, Taga T. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 2001; 1: 749-758.
105. Song MR, Ghosh A. FGF2-induced chromatin remodeling regulates CNTF-mediated gene expression and astrocyte differentiation. Nat Neurosci 2004; 7: 229-235.
106. Hagberg B, Aicardi J, Dias K, Ramos O. A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett's syndrome: report of 35 cases. Ann Neurol 1983; 14: 471-479
107. Jung BP, Jugloff DG, Zhang G, Logan R, Brown S, Eubanks JH. The expression of methyl CpG binding factor MeCP2 correlates with cellular differentiation in the developing rat brain and in cultured cells. J Neurobiol 2003; 55: 86-96.
108. Mill J, Petronis A. Molecular studies of major depressive disorder: the epigenetic perspective. Mol Psychiatry 2007; 12: 799-814.
109. Mill J, Petronis A. 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 2008; 49: 1020-1030.
110. Oh G, Petronis A. Environmental studies of schizophrenia through the prism of epigenetics. Schizophr Bull 2008; 34: 1122-1129.
111. Petronis A. Human morbid genetics revisited: relevance of epigenetics. Trends Genet 2001; 17: 142-146.
112. Petronis A. Epigenetics and bipolar disorder: new opportunities and challenges. Am J Med Genet C Semin Med Genet 2003; 123: 65-75.
113. Mill J, Tang T, Kaminsky Z, Khare T, Yazdanpanah S, Bouchard L, Jia P, Assadzadeh A, Flanagan J, Schumacher A, Wang SC, Petronis A. Epigenomic profiling reveals DNA-methylation changes associated with major psychosis. Am J Hum Genet 2008; 82: 696-711.
114. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharrna S, Pearson D, Plotsky PM, Meaney MJ. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adre-nal responses to stress. Science 1997; 277: 1659-1662.
115. Webster WS, Walsh DA, McEwen SE, Lipson AH. Some teratogenic properties of ethanol and acetaldehyde in C57BL/6J mice: implications for the study of the fetal alcohol syndrome. Teratology 1983; 27: 231-243.