Fetal alcohol spectrum disorders and their transmission through genetic and epigenetic mechanisms

Frontiers in Genetics

Volumn 5, Issue JUN, 2014, Pages

  Mead, Edward A ^a   Sarkar, Dipak K ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

FASD; Fetal alcohol; HPA axis; Proopiomelanocortin; Transgenerational epigenetic

Indexed keywords

ARGIPRESSIN; BETA ENDORPHIN; CATECHOLAMINE; MICRORNA; PROOPIOMELANOCORTIN;

ALCOHOL CONSUMPTION; ALLELE; DISEASE PREDISPOSITION; DNA METHYLATION; DNA SEQUENCE; FETAL ALCOHOL SYNDROME; GENE EXPRESSION; GENE FUNCTION; HISTONE MODIFICATION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INHERITANCE; LOSS OF FUNCTION MUTATION; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; PRENATAL EXPOSURE; REVIEW; TRANSCRIPTION ELONGATION;

EID: 84906235060     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00154     Document Type: Review

References (113)

1. Abel, E. (1984). "Is fetal alcohol syndrome a new discovery?" in Fetal Alcohol Syndrome and Fetal Alcohol Effects , ed. E. Abel (New York, NY: Springer Press), 1-28. doi: 10.1007/978-1-4613-2669-4_1
2. Abel, E. (2004). Paternal contribution to fetal alcohol syndrome. Addict. Biol. 9, 127-133. doi: 10.1080/13556210410001716980
3. Adams, J. (2008). Imprinting and genetic disease: Angelman, Prader-Willi and Beckwith-Weidemann syndromes. Nat. Educ. 1, 129.
4. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., and Walter, P. (2002). Molecular Biology of the Cell , 4th Edn. New York: Garland Science.
5. Anway, M. D., Cupp, A. S., Uzumcu, M., and Skinner, M. K. (2005). Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308, 1466-1469. doi: 10.1126/science.1108190
6. Armant, D. R., and Saunders, D. E. (1996). Exposure of embryonic cells to alcohol: contrasting effects during preimplantation and postimplantation development. Semin. Perinatol. 20, 127-139. doi: 10.1016/S0146-0005(96)80080-2
7. Arney, K. L., and Fisher, A. G. (2004). Epigenetic aspects of differentiation. J. Cell. Sci. 117, 4355-4363. doi: 10.1242/jcs.01390
8. Barak, A. J., Beckenhauer, H. C., Junnila, M., and Tuma, D. J. (1993). Dietary betaine promotes generation of hepatic S-adenosylmethionine and protects the liver from ethanol-induced fatty infiltration. Alcohol Clin. Exp. Res. 17, 552-555. doi: 10.1111/j.1530-0277.1993.tb00798.x
9. Bekdash, R. A., Zhang, C., and Sarkar, D. K. (2013). Gestational choline supplementation normalized fetal alcohol-induced alterations in histone modifications, DNA methylation, and proopiomelanocortin (POMC) gene expression in ß-endorphin-producing POMC neurons of the hypothalamus. Alcohol Clin. Exp. Res. 37, 1133-1142. doi: 10.1111/acer.12082
10. Berezikov, E. (2011). Evolution of microRNA diversity and regulation in animals. Nat. Rev. Genet. 12, 846-860. doi: 10.1038/nrg3079
11. Bestor, T. H. (2000). The DNA methyltransferases of mammals. Hum. Mol. Genet. 9, 2395-2402. doi: 10.1093/hmg/9.16.2395
12. Bond, D. M., and Finnegan, E. J. (2007). Passing the message on: inheritance of epigenetic traits. Trends Plant Sci. 12, 211-216. doi: 10.1016/j.tplants.2007.03.010
13. Bönsch, D., Lenz, B., Fiszer, R., Frieling H., Kornhuber, J., and Bleich, S. (2006). Lowered DNA methyltransferase (DNMT-3b) mRNA expression is associated with genomic DNA hypermethylation in patients with chronic alcoholism. J. Neural Transm. 113, 1299-1304. doi: 10.1007/s00702-005-0413-2
14. Borgel, J., Guibert, S., Li, Y., Chiba, H., Schübeler, D., Sasaki, H., et al. (2010). Targets and dynamics of promoter DNA methylation during early mouse development. Nat. Genet. 42, 1093-1100. doi: 10.1038/ng.708
15. Boyadjieva, N. I., Ortigüela, M., Arjona, A., Cheng, X., and Sarkar, D. K. (2009). Β-Endorphin neuronal cell transplant reduces corticotropin releasing hormone hyperresponse to lipopolysaccharide and eliminates natural killer cell functional deficiencies in fetal alcohol exposed rats. Alcohol Clin. Exp. Res. 33, 931-937. doi: 10.1111/j.1530-0277.2009.00911.x
16. Brykczynska, U., Hisano, M., Erkek, S., Ramos, L., Oakeley, E. J., Roloff, T. C., et al. (2010). Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17, 679-687. doi: 10.1038/nsmb.1821
17. Chen, C. P., Kuhn, P., Chaturvedi, K., Boyadjieva, N., and Sarkar, D. K. (2006). Ethanol induces apoptotic death of developing beta-endorphin neurons via suppression of cyclic adenosine monophosphate production and activation of transforming growth factor-beta1-linked apoptotic signaling. Mol. Pharm. 69, 706-717. doi: 10.1124/mol.105.017004
18. Chu, Y. H., Tzeng, S. L., Lin, C. W., Chien, M. H., Chen, M. K., and Yang, S. F. (2012). Impacts of MicroRNA gene polymorphisms on the susceptibility of environmental factors leading to carcinogenesis in oral cancer. PLoS ONE 7:e39777. doi: 10.1371/journal.pone.0039777
19. Clarren, S. K. (1986). "Neuropathology in fetal alcohol syndrome," in Alcohol and Brain Development , ed. J. R. West (New York: Oxford University Press), 158-166.
20. Clarren, S. K., Alvord, E. C. Jr., Sumi, S. M., Streissguth, A. P., and Smith, D. W. (1978). Brain malformations related to prenatal exposure to ethanol. J. Pediatr. 92, 64-67. doi: 10.1016/S0022-3476(78)80072-9
21. Deaton, A. M., and Bird, A. (2011). CpG islands and the regulation of transcription. Genes Dev. 25, 1010-1022. doi: 10.1101/gad.2037511
22. Doerfler, W. (1983). DNA methylation and gene activity. Annu. Rev. Biochem. 52, 93-124. doi: 10.1146/annurev.bi.52.070183.000521
23. Douzgou, S., Breen, C., Crow, Y. J., Chandler, K., Metcalfe, K., Jones, E., et al. (2012). Diagnosing fetal alcohol syndrome: new insights from newer genetic technologies. Arch. Dis. Child. 97, 812-817. doi: 10.1136/archdischild-2012-302125
24. Eberwine, J. H., and Roberts, J. L. (1984). Glucocorticoid regulation of pro-opiomelanocortin gene transcription in the rat pituitary. J. Biol. Chem. 259, 2166-2170.
25. Eger, G., Liang, G., Aparcio, A., and Jones, P. A. (2004). Epigenetics in human disease and prospects for epigenetic therapy. Nature 429, 457-463. doi: 10.1038/nature02625
26. Fitch, K. R., Yasuda, G. K., Owens, K. N., and Wakimoto, B. T. (1998). Paternal effects in Drosophila: implications for mechanisms of early development. Curr. Top. Dev. Biol. 38, 1-34. doi: 10.1016/S0070-2153(08)60243-4
27. Fratta, W., Rossetti, Z. L., Poggioli, R., and Gessa, G. L. (1981). Reciprocal antagonism between ACTH1-24 and beta-endorphin in rats. Neurosci. Lett. 24, 71-74. doi: 10.1016/0304-3940(81)90361-X
28. Fulka, H., Mrazek, M., Tepla, O., and Fulka, J. (2004). DNA methylation pattern in human zygotes and developing embryos. Reproduction 128, 703-708. doi: 10.1530/rep.1.00217
29. Gardiner-Garden, M., and Frommer, M. (1987). CpG islands in vertebrate genomes. J. Mol. Biol. 196, 261-282. doi: 10.1016/0022-2836(87)90689-9
30. Garro, A. J., McBeth, D. L., Lima, V., and Lieber, C. S. (1991). Ethanol consumption inhibits fetal DNA methylation in mice: implications for the fetal alcohol syndrome. Alcohol Clin. Exp. Res. 15, 395-398. doi: 10.1111/j.1530-0277.1991.tb00536.x
31. Govorko, D., Bekdash, R. A., Zhang, C., and Sarkar, D. K. (2012). Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations. Biol. Psychiatry 72, 378-388. doi: 10.1016/j.biopsych.2012.04.006
32. Guerrero-Bosagna, C., Settles, M., Lucker, B., and Skinner, M. K. (2010). Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS ONE 5:e13100. doi: 10.1371/journal.pone.0013100
33. Haley, D. W., Handmaker, N. S., and Lowe, J. (2006). Infant stress reactivity and prenatal alcohol exposure. Alcohol Clin. Exp. Res. 30, 2055-2064. doi: 10.1111/j.1530-0277.2006.00251.x
34. Halsted, C. H., Villanueva, J. A., Devlin, A. M., and Chandler, C. J. (2002). Metabolic interactions of alcohol and folate. J. Nutrit. 132(8 Suppl.), S2367-S2372.
35. Hamid, A., Wani, N. A., and Kaur, J. (2009). New perspectives on folate transport in relation to alcoholism-induced folate malabsorption--association with epigenome stability and cancer development. FEBS J. 276, 2175-2191. doi: 10.1111/j.1742-4658.2009.06959.x
36. Hammoud, S. S., Nix, D. A., Zhang, H., Purwar, J., Carrell, D. T., and Cairns, B. R. (2009). Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473-478. doi: 10.1038/nature08162
37. Haycock, P. C. (2009). Fetal alcohol spectrum disorders: the epigenetic perspective. Biol. Reprod. 81, 607-617. doi: 10.1095/biolreprod.108.074690
38. Hellemans, K. G., Verma, P., Yoon, E., Yu, W., and Weinberg, J. (2008). Prenatal alcohol exposure increases vulnerability to stress and anxiety-like disorders in adulthood. Ann. N. Y. Acad. Sci. 1144, 154-175. doi: 10.1196/annals.1418.016
39. Hidiroglou, N., Camilo, M. E., Beckenhauer, H. C., Tuma, D. J., Barak, A. J., Nixon, P. F., et al. (1994). Effect of chronic alcohol ingestion on hepatic folate distribution in the rat. Biochem. Pharmacol. 47, 1561-1566. doi: 10.1016/0006-2952(94)90532-0
40. Hillemacher, T., Frieling, H., Hartl, T., Wilhelm, J., Kornhuber, J., and Bleich, S. (2009). Promoter specific methylation of the dopamine transporter gene is altered in alcohol dependence and associated with craving. J. Psychol. Res. 43, 388-392. doi: 10.1016/j.jpsychires.2008.04.006
41. Hsieh, J., and Gage, F. H. (2005). Chromatin remodeling in neural development and plasticity. Curr. Opin. Cell Biol. 17, 664-671. doi: 10.1016/j.ceb.2005.09.002
42. Illingworth, R. S., Gruenewald-Schneider, U., Webb, S., Kerr, A. R. W., James, K. D., Turner, D. J., et al. (2010). Orphan CpG islands identify numerous conserved promoters in the mammalian genome. PLoS Genet. 6:e1001134. doi: 10.1371/journal.pgen.1001134
43. Jacobson, S. W., Carr, L. G., Croxford, J., Sokol, R. J., Li, T. K., and Jacobson, J. L. (2006). Protective effects of the alcohol dehydrogenase-ADH1B allele in children exposed to alcohol during pregnancy. J. Pediatr. 148, 30-37. doi: 10.1016/j.jpeds.2005.08.023
44. Jaenisch, R., and Bird, A. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33, 245-254. doi: 10.1038/ng1089
45. Jin, B., Li, Y., and Robertson, K. D. (2011). DNA methylation: superior or subordinate in the epigenetic hierarchy? Genes Cancer 2, 607-617. doi: 10.1177/1947601910393957
46. Jirtle, R., and Skinner, M. K. (2007). Environmental epigenomics and disease susceptibility. Nat. Rev. 8, 253-262. doi: 10.1038/nrg2045
47. Johnson, C., Drgon, T., Liu, Q. R., Walther, D., Edenberg, H., Rice, J., et al. (2006). Pooled association genome scanning for alcohol dependence using 104,268 SNPs: validation and use to identify alcoholism vulnerability loci in unrelated individuals from the collaborative study on the genetics of alcoholism. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 141B, 844-853. doi: 10.1002/ajmg.b.30346
48. Jones, K. L., Smith, D. W., Ulleland, C. N., and Streissguth, A. P. (1973). Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1, 1267-1271. doi: 10.1016/S0140-6736(73)91291-9
49. Kaminen-Ahola, N., Ahola, A., Maga, M., Mallitt, K. A., Fahey, P., Cox T. C., et al. (2010). Maternal ethanol consumption alters the epigenotype and the phenotype of offspring in a mouse model. PLoS Genet. 6:e1000811. doi: 10.1371/journal.pgen.1000811
50. Kim, J. S., and Shukla, S. D. (2006). Acute in vivo effect of ethanol (binge drinking) on histone H3 modifications in rat tissues. Alcohol Alcohol. 41, 126-132. doi: 10.1093/alcalc/agh248
51. Kim, Y. I., Pogribny, I. P., Basnakian, A. G., Miller, J. W., Selhub, J., James, S. J., et al. (1997). Folate deficiency in rats induces DNA strand breaks and hypomethylation within the p53 tumor suppressor gene. Am. J. Clin. Nutr. 65, 46-52.
52. Kobor, M. S., and Weinberg, J. (2011). Epigenetics and fetal alcohol spectrum disorders. Alcohol Res. Health 34, 15-37.
53. Kraemer, G. W., Moore, C. F., Newman, T. K., Barr, C. S., and Schneider, M. L. (2008). Moderate level fetal alcohol exposure and serotonin transporter gene promoter polymorphism affect neonatal temperament and limbic-hypothalamic-pituitary-adrenal axis regulation in monkeys. Biol. Psychiatry 63, 317-324. doi: 10.1016/j.biopsych.2007.07.017
54. Kuhn, P., and Sarkar, D. K. (2008). Ethanol induces apoptotic death of Β-endorphin neurons in the rat hypothalamus by a TGF-Β1-dependent mechanism. Alcohol Clin. Exp. Res. 32, 706-714. doi: 10.1111/j.1530-0277.2008.00627.x
55. Kvigne, V. L., Leonardson, G. R., Borzelleca, J., and Welty, T. K. (2008). Characteristics of grandmothers who have grandchildren with fetal alcohol syndrome or incomplete fetal alcohol syndrome. Matern. Child Health J. 12, 760-765. doi: 10.1007/s10995-007-0308-y
56. Langevin, F., Crossan, G. P., Rosado, I. V., Arends, M. J., and Patel, K. J. (2011). Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice. Nature 475, 53-58. doi: 10.1038/nature10192
57. Li, E. (2002). Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet. 3, 662-673. doi: 10.1038/nrg887
58. Li, H., Gu, S., Han, Y., Xu, Z., Pakstis, A. J., Jin, L., et al. (2011). Diversification of the ADH1B gene during expansion of modern humans. Ann. Hum. Genet. 75, 497-507. doi: 10.1111/j.1469-1809.2011.00651.x
59. Liu, Y., Balaraman, Y., Wang, G., Nephew, K. P., and Zhou, F. C. (2009). Alcohol exposure alters DNA methylation profiles in mouse embryos at early neurulation. Epigenetics 4, 500-511. doi: 10.4161/epi.4.7.9925
60. Lombard, Z., Tiffin, N., Hofmann, O., Bajic, V. B., Hide, W., and Ramsay, M. (2007). Computational selection and prioritization of candidate genes for fetal alcohol syndrome. BMC Genomics 8:389. doi: 10.1186/1471-2164-8-389
61. Lu, S. C., Huang, Z. Z., Yang, H., Mato, J. M., Avila, M. A., and Tsukamoto, H. (2000). Changes in methionine adenosyltransferase and S-adenosylmethionine homeostasis in alcoholic rat liver. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G178-G185.
62. Lukiw, W. J. (2013). Variability in micro RNA (miRNA) abundance, speciation and complexity amongst different human populations and potential relevance to Alzheimer's disease (AD). Front. Cell. Neurosci. 7:133. doi: 10.3389/fncel.2013.00133
63. Maunakea, A. K., Nagarajan, R. P., Bilenky, M., Ballinger, T. J., D'Souza, C., Fouse, S. D., et al. (2010). Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466, 253-257. doi: 10.1038/nature09165
64. May, P. A., and Gossage, J. P. (2011). Maternal risk factors for fetal alcohol spectrum disorders: not as simple as it might seem. Alcohol Res. Health 34, 15-26.
65. May, P. A., Blankenship, J., Marais, A. S., Gossage, J. P., Kalberg, W. O., Barnard, R., et al. (2013). Approaching the prevalence of the full spectrum of fetal alcohol spectrum disorders in a South African population-based study. Alcohol Clin. Exp. Res. 37, 818-830. doi: 10.1111/acer.12033
66. Maze, I., and Nestler, E. J. (2011). The epigenetic landscape of addiction. Ann. N. Y. Acad. Sci. 1216, 99-113. doi: 10.1111/j.1749-6632.2010.05893.x
67. McCarthy, N., and Eberhart, J. K. (2014). Gene-ethanol interactions underlying fetal alcohol spectrum disorders. Cell Mol. Life Sci. doi: 10.1007/s00018-014-1578-3 [Epub ahead of print].
68. Miranda, R. C. (2012). MicroRNAs and fetal brain development: implications for ethanol teratology during the second trimester period of neurogenesis. Front. Genet. 3:77. doi: 10.3389/fgene.2012.00077
69. Momino, W., Félix, T. M., Abeche, A. M., Zandoná, D. I., Scheibler, G. G., Chambers, C., et al. (2012). Maternal drinking behavior and fetal alcohol spectrum disorders in adolescents with criminal behavior in southern Brazil. Genet. Mol. Biol. 35(Suppl. 4), 960-965. doi: 10.1590/S1415-47572012000600011
70. Morison, I. M., and Reeve, A. E. (1998). A catalogue of imprinted genes and parent-of-origin effects in humans and animals. Hum. Mol. Genet. 7, 1599-1609. doi: 10.1093/hmg/7.10.1599
71. Nestler, E. (2014). Epigenetic mechanisms of drug addiction. Neuropharmacology 76B, 259-268. doi: 10.1016/j.neuropharm.2013.04.004
72. Osier, M. V., Pakstis, A. J., Kidd, J. R., Lee, J. F., Yin, S. J., Ko, H. C., et al. (1999). Linkage disequilibrium at the ADH2 and ADH3 loci and risk of alcoholism. Am. J. Hum. Genet. 64, 1147-1157. doi: 10.1086/302317
73. Oswald, J., Engemann, S., Lane, N., Mayer, W., Olek, A., Fundele, R., et al. (2000). Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10, 475-478. doi: 10.1016/S0960-9822(00)00448-6
74. Ouko, L. A., Shantikumar, K., Knezovich, J., Haycock, P., Schnugh, D. J., and Ramsay, M. (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. doi: 10.1111/j.1530-0277.2009.00993.x
75. Pal-Bhadra, M., Bhadra, U., Jackson, D. E., Mamatha, L., Park, P., and Shukla, S. D. (2007). Distinct methylation patterns in histone H3 at Lys-4 and Lys-9 correlate with up- and down-regulation of genes by ethanol in hepatocytes. Life Sci. 81, 979-987. doi: 10.1016/j.lfs.2007.07.030
76. Pandey, S., Rajesh, U., Zhang, H., Tang, L., and Prakash, A. (2008). Brain chromatin remodeling: a novel mechanism of alcoholism. J. Neurosci. 28, 3729-3737. doi: 10.1523/JNEUROSCI.5731-07.2008
77. Plotsky, P. M. (1986). Opioid inhibition of immunoreactive corticotropin-releasing factor secretion into the hypophysial-portal circulation of rats. Reg. Peptides 16, 235-242. doi: 10.1016/0167-0115(86)90022-4
78. Ponomarev, I. (2013). Epigenetic control of gene expression in the alcoholic brain. Alcohol Res. 35, 69-76.
79. Pritchard, L. E., Turnbull, A. V., and White, A. (2002). Pro-opiomelanocortin processing in the hypothalamus: impact on melanocortin signaling and obesity. J. Endocrinol. 172, 411-421. doi: 10.1677/joe.0.1720411
80. Rachdaoui, N., and Sarkar, D. K. (2013). Effects of alcohol on the endocrine system. Endocrinol. Metab. Clin. N. Am. 42, 593-615. doi: 10.1016/j.ecl.2013.05.008
81. Raffin-sanson, M. L., de Keyser, Y., and Bertagna, X. (2003). Proopiomelanocortin, a polypeptide precursor with multiple functions: from physiology to pathological conditions. Euro J. Endocrinol. 149, 79-90. doi: 10.1530/eje.0.1490079
82. Renthal, W., and Nestler, E. J. (2009). Chromatin regulation in drug addiction and depression. Dialog Clin. Neurosci. 11, 257-268.
83. Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S., and Bale, T. L. (2013). Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J. Neurosci. 33, 9003-9012. doi: 10.1523/JNEUROSCI.0914-13.2013
84. Sakharkar, A. J., Zhang, H., Tang, L., Shi G., and Pandey, S. C. (2012). Histone deacetylases (HDAC)-induced histone modifications in the amygdala: a role in rapid tolerance to the anxiolytic effects of ethanol. Alcohol Clin. Exp. Res. 36, 61-71. doi: 10.1111/j.1530-0277.2011.01581.x
85. Sampson, P. D., Streissguth, A. P., Bookstein, F. L., Little, R. E., Clarren, S. K., Dehaene, P., et al. (1997). Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 56, 317-326. doi: 10.1002/(SICI)1096-9926(199711)56:5<317::AID-TERA5>3.0.CO;2-U
86. Sarkar, D. K. (1996). Neuroendocrine - immune axis of alcoholics. Symposium. Alcohol Clin. Exp. Res. 20, 256A-259A.
87. Sarkar, D. K., Kuhn, P., Marano, J., Chen, C., and Boyadjieva, N. (2007). Alcohol exposure during the developmental period induces ß-endorphin neuronal death and causes alteration in the opioid control of stress axis function. Endocrinology 148, 2828-2834. doi: 10.1210/en.2006-1606
88. Sarkar, D. K., Murugan, S., Zhang, C., and Boyadjieva, N. (2012). Regulation of cancer progression by Β-endorphin neuron. Cancer Res. 72, 836-840. doi: 10.1158/0008-5472.CAN-11-3292
89. Saxonov, S., Berg, P., and Brutlag, D. L. (2006). A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc. Natl. Acad. Sci. U.S.A. 103, 1412-1417. doi: 10.1073/pnas.0510310103
90. Schier, A. F. (2007). The maternal-zygotic transition: death and birth of RNAs. Science 316, 406-407. doi: 10.1126/science.1140693
91. Schneider, M. L., Moore, C. F., Kraemer, G. W., Roberts, A. D., and DeJesus, O. T. (2002). The impact of prenatal stress, fetal alcohol exposure, or both on development: perspectives from a primate model. Psychoneuroendocrinology 27, 285-298. doi: 10.1016/S0306-4530(01)00050-6
92. Schneider, M. L., Moore, C. F., Larson, J. A., Barr, C. S., DeJesus, O. T., and Roberts, A. D. (2009). Timing of moderate level prenatal alcohol exposure influences gene expression of sensory processing behavior in rhesus monkeys. Front. Integr. Neurosci. 3:30. doi: 10.3389/neuro.07.030.2009
93. Sharma, R. P., Grayson, D. R., and Gavin, D. P. (2008). Histone deacetylase 1 expression is increased in the prefrontal cortex of schizophrenia subjects: analysis of the National Databank microarray collection. Schizophr. Res. 98, 111-117. doi: 10.1016/j.schres.2007.09.020
94. Sharma, H. K., Tripathi, B. M., and Pelto, P. J. (2010). The evolution of alcohol use in India. AIDS Behav. 14(Suppl. 1), S8-S17.
95. Shi, L., and Wu, J. (2009). Epigenetic regulation in mammalian preimplantation embryo development. Reprod. Biol. Endocrinol. 7, 59. doi: 10.1186/1477-7827-7-59
96. Singh, P. K., and Campbell, M. J. (2013). The interactions of microRNA and epigenetic modifications in prostate cancer. Cancers (Basel) 5, 998-1019. doi: 10.3390/cancers5030998
97. Stockard, C. (1913). The effect on the offspring of intoxicating the male parent and the transmission of the defects to subsequent generations. Am. Nat. 47, 641-682. doi: 10.1086/279379
98. Streissguth, A. P., and Dehaene, P. (1993). Fetal alcohol syndrome in twins of alcoholic mothers: concordance of diagnosis and IQ. Am. J. Med. Genet. 47, 857-861. doi: 10.1002/ajmg.1320470612
99. Sun, G., Yan, J., Noltner, K., Feng, J., Li, H., Sarkis, D. A., et al. (2009). SNPs in human miRNA genes affect biogenesis and function. RNA 15, 1640-1651. doi: 10.1261/rna.1560209
100. Tapocik, J. D., Solomon, M., Flanigan, M., Meinhardt, M., Barbier, E., Schank, J. R., et al. (2013). Coordinated dysregulation of mRNAs and microRNAs in the rat medial prefrontal cortex following a history of alcohol dependence. Pharmacogenomics J. 13, 286-296. doi: 10.1038/tpj.2012.17
101. Thomas, J. D., Biane, J. S., O'Bryan, K. A., O'Neill, T. M., and Dominguez, H. D. (2007). Choline supplementation following third-trimester equivalent alcohol exposure attenuates behavioral alterations in rats. Behav. Neurosci. 121, 120-130. doi: 10.1037/0735-7044.121.1.120
102. Thomas, J. D., Idrus, N. M., Monk, B. R., and Dominquez, H. D. (2010). Prenatal choline supplementation mitigates behavioral alterations associated with prenatal alcohol exposure in rats. Birth Defect. Res. A Clin. Mol. Teratol. 88, 827-837. doi: 10.1002/bdra.20713
103. Thomas, J. D., and Tran, T. D. (2012). Choline supplementation mitigates trace, but not delay, eyeblink conditioning deficits in rats exposed to alcohol during development. Hippocampus 22, 619-630. doi: 10.1002/hipo.20925
104. Thornburg, K. L., Shannon, J., Thuillier, P., and Turker, M. S. (2010). In utero life and epigenetic predisposition for disease. Adv. Genet. 71, 57-78. doi: 10.1016/B978-0-12-380864-6.00003-1
105. Ungerer, M., Knezovich, J., and Ramsay, M. (2013). In utero alcohol exposure, epigenetic changes, and their consequences. Alcohol Res. 35, 37-46.
106. Veazey, K. J., Carnahan, M. N., Muller, D., Miranda, R. C., and Golding, M. C. (2013). Alcohol-induced epigenetic alterations to developmentally crucial genes regulating neural stemness and differentiation. Alcohol. Clin. Exp. Res. 37, 1111-1122. doi: 10.1111/acer.12080
107. Wang, L. L., Zhang, Z., Li, Q., Yang, R., Pei, X., Xu, Y., et al. (2009). Ethanol exposure induces differential microRNA and target gene expression and teratogenic effects which can be suppressed by folic acid supplementation. Hum. Reprod. 24, 562-579. doi: 10.1093/humrep/den439
108. Warren, K. R., and Li, T. K. (2005). Genetic polymorphisms: impact on the risk of fetal alcohol spectrum disorders. Birth Defects Res. A Clin. Mol. Teratol. 73, 195-203. doi: 10.1002/bdra.20125
109. Wozniak, J. R., Fuglestad, A. J., Eckerle, J. K., Kroupina, M. G., Miller, N. C., Boys, C. J., et al. (2013). Choline supplementation in children with fetal alcohol spectrum disorders has high feasibility and tolerability. Nutr. Res. 33, 897-904. doi: 10.1016/j.nutres.2013.08.005
110. Wynne, O., and Sarkar, D. K. (2013). "Stress and neuroendocrine-immune interaction: a therapeutic role for Β-endorphin," in The Wiley-Blackwell Handbook of Psychoneuroimmunology , eds A. W. Kusnecov and H. Anisman (Chichester: John Wiley & Sons Ltd), 198-211. doi: 10.1002/9781118314814.ch10
111. Zeisel, S. H. (2004). Nutritional importance of choline for brain development. J. Am. Coll. Nutr. 23, 621S-626S. doi: 10.1080/07315724.2004.10719433
112. Zeisel, S. H. (2006). Choline: critical role during fetal development and dietary requirements in adults. Annu. Rev. Nutr. 26, 229-250. doi: 10.1146/annurev.nutr.26.061505.111156
113. Zhong, L., Zhu, J., Lv, T., Chen, G., Sun, H., Yang, X., et al. (2010). Ethanol and its metabolites induce histone lysine 9 acetylation and an alteration of the expression of heart development-related genes in cardiac progenitor cells. Cardiovasc. Toxicol. 10, 268-274. doi: 10.1007/s12012-010-9081-z