Hypothesis: Genetic and epigenetic risk factors interact to modulate vulnerability and resilience to FASD

Frontiers in Genetics

Volumn 5, Issue AUG, 2014, Pages

  Tunc Ozcan, Elif ^a   Sittig, Laura J ^a   Harper, Kathryn M ^a   Graf, Evan N ^a   Redei, Eva E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Allele specific expression; Prenatal ethanol; Rat; Second generation; Strain differences; Thyroid hormones

Indexed keywords

INSULIN; THYROTROPIN; THYROXINE;

ALCOHOL CONSUMPTION; ALLELE; ARTICLE; BRAIN REGION; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENETICS; FETAL ALCOHOL SYNDROME; GENE EXPRESSION; GENE INTERACTION; GENE LINKAGE DISEQUILIBRIUM; GENETIC RISK; HUMAN; HYPOTHESIS; NONHUMAN; PRENATAL EXPOSURE; PRENATAL GROWTH; PROGENY; SEX; TERATOGENICITY;

EID: 84906279900     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00261     Document Type: Article

References (57)

1. Anthony, B., Vinci-Booher, S., Wetherill, L., Ward, R., Goodlett, C., and Zhou, F. C. (2010). Alcohol-induced facial dysmorphology in C57BL/6 mouse models of fetal alcohol spectrum disorder. Alcohol 44, 659-671. doi: 10.1016/j.alcohol.2010.04.002
2. Balaraman, S., Tingling, J. D., Tsai, P. C., and Miranda, R. C. (2013). Dysregulation of microRNA expression and function contributes to the etiology of fetal alcohol spectrum disorders. Alcohol Res. 35, 18-24.
3. Barker, D. J. (2004). The developmental origins of chronic adult disease. Acta Paediatr. 93, 26-33. doi: 10.1111/j.1651-2227.2004.tb00236.x
4. Barker, D. J., Bull, A. R., Osmond, C., and Simmonds, S. J. (1990). Fetal and placental size and risk of hypertension in adult life. BMJ 301, 259-262.
5. Barker, D. J., Hales, C. N., Fall, C. H., Osmond, C., Phipps, K., and Clark, P. M. (1993). Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62-67.
6. Barker, D. J., Winter, P. D., Osmond, C., Margetts, B., and Simmonds, S. J. (1989). Weight in infancy and death from ischaemic heart disease. Lancet 2, 577-580.
7. Browman, K. E., and Crabbe, J. C. (2000). Quantitative trait loci affecting ethanol sensitivity in BXD recombinant inbred mice. Alcohol Clin. Exp. Res. 24, 17-23. doi: 10.1111/j.1530-0277.2000.tb04547.x
8. Brunton, P. J., and Russell, J. A. (2011). Neuroendocrine control of maternal stress responses and fetal programming by stress in pregnancy. Prog. Neuropsychopharmacol. Biol. Psychiatry 35, 1178-1191. doi: 10.1016/j.pnpbp.2010.12.023
9. Chen, Y., Ozturk, N. C., Ni, L., Goodlett, C., and Zhou, F. C. (2011). Strain differences in developmental vulnerability to alcohol exposure via embryo culture in mice. Alcohol Clin. Exp. Res. 35, 1293-1304. doi: 10.1111/j.1530-0277.2011.01465.x
10. Cudd, T. A., Chen, W. J., and West, J. R. (2002). Fetal and maternal thyroid hormone responses to ethanol exposure during the third trimester equivalent of gestation in sheep. Alcohol Clin. Exp. Res. 26, 53-58. doi: 10.1111/j.1530-0277.2002.tb02431.x
11. Delaval, K., and Feil, R. (2004). Epigenetic regulation of mammalian genomic imprinting. Curr. Opin. Genet. Dev. 14, 188-195. doi: 10.1016/j.gde.2004.01.005
12. Downing, C., Balderrama-Durbin, C., Broncucia, H., Gilliam, D., and Johnson, T. E. (2009). Ethanol teratogenesis in five inbred strains of mice. Alcohol Clin. Exp. Res. 33, 1238-1245. doi: 10.1111/j.1530-0277.2009.00949.x
13. Downing, C., Balderrama-Durbin, C., Kimball, A., Biers, J., Wright, H., Gilliam, D., et al. (2012). Quantitative trait locus mapping for ethanol teratogenesis in BXD recombinant inbred mice. Alcohol Clin. Exp. Res. 36, 1340-1354. doi: 10.1111/j.1530-0277.2012.01754.x
14. Downing, C., Johnson, T. E., Larson, C., Leakey, T. I., Siegfried, R. N., Rafferty, T. M., et al. (2011). Subtle decreases in DNA methylation and gene expression at the mouse Igf2 locus following prenatal alcohol exposure: effects of a methyl-supplemented diet. Alcohol 45, 65-71. doi: 10.1016/j.alcohol.2010.07.006
15. Eberle, C., and Ament, C. (2012). Diabetic and metabolic programming: mechanisms altering the intrauterine milieu. ISRN Pediatr. 2012:975685. doi: 10.5402/2012/975685
16. Feil, R., and Fraga, M. F. (2011). Epigenetics and the environment: emerging patterns and implications. Nat. Rev. Genet. 13, 97-109. doi: 10.1038/nrg3142
17. 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
18. Gilliam, D. M., and Irtenkauf, K. T. (1990). Maternal genetic effects on ethanol teratogenesis and dominance of relative embryonic resistance to malformations. Alcohol Clin. Exp. Res. 14, 539-545. doi: 10.1111/j.1530-0277.1990.tb01196.x
19. Gilliam, D. M., Mantle, M. A., Barkhausen, D. A., and Tweden, D. R. (1997). Effects of acute prenatal ethanol administration in a reciprocal cross of C57BL/6J and short-sleep mice: maternal effects and nonmaternal factors. Alcohol Clin. Exp. Res. 21, 28-34.
20. Glavas, M. M., Ellis, L., Yu, W. K., and Weinberg, J. (2007). Effects of prenatal ethanol exposure on basal limbic-hypothalamic-pituitary-adrenal regulation: role of corticosterone. Alcohol Clin. Exp. Res. 31, 1598-1610. doi: 10.1111/j.1530-0277.2007.00460.x
21. 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
22. Gregg, C., Zhang, J., Weissbourd, B., Luo, S., Schroth, G. P., Haig, D., et al. (2010). High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 329, 643-648. doi: 10.1126/science.1190830
23. Harper, K. M., Tunc-Ozcan, E., Graf, E. N., and Redei, E. E. (2014). Intergenerational effects of prenatal ethanol on glucose tolerance and insulin response. Physiol. Genomics 46, 159-168. doi: 10.1152/physiolgenomics.00181.2013
24. Haycock, P. C. (2009). Fetal alcohol spectrum disorders: the epigenetic perspective. Biol. Reprod. 81, 607-617. doi: 10.1095/biolreprod.108.074690
25. Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., et al. (2008). Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. U.S.A. 105, 17046-17049. doi: 10.1073/pnas.0806560105
26. Heinz, A., Bauer, M., Kuhn, S., Kruger, F., Graf, K. J., Rommelspacher, H., et al. (1996). Long-term observation of the hypothalamic-pituitary-thyroid (HPT) axis in alcohol-dependent patients. Acta Psychiatr. Scand 93, 470-476. doi: 10.1111/j.1600-0447.1996.tb10679.x
27. Hellemans, K. G., Sliwowska, J. H., Verma, P., and Weinberg, J. (2010). Prenatal alcohol exposure: fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci. Biobehav. Rev. 34, 791-807. doi: 10.1016/j.neubiorev.2009.06.004
28. 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
29. Knezovich, J. G., and Ramsay, M. (2012). The effect of preconception paternal alcohol exposure on epigenetic remodeling of the h19 and rasgrf1 imprinting control regions in mouse offspring. Front. Genet. 3:10. doi: 10.3389/fgene.2012.00010
30. 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
31. Laufer, B. I., Mantha, K., Kleiber, M. L., Diehl, E. J., Addison, S. M., and Singh, S. M. (2013). Long-lasting alterations to DNA methylation and ncRNAs could underlie the effects of fetal alcohol exposure in mice. Dis. Model Mech. 6, 977-992. doi: 10.1242/dmm.010975
32. Liang, G., Chen, M., Pan, X. L., Zheng, J., and Wang, H. (2011). Ethanol-induced inhibition of fetal hypothalamic-pituitary-adrenal axis due to prenatal overexposure to maternal glucocorticoid in mice. Exp. Toxicol Pathol. 63, 607-611. doi: 10.1016/j.etp.2010.04.015
33. Liappas, I., Piperi, C., Malitas, P. N., Tzavellas, E. O., Zisaki, A., Liappas, A. I., et al. (2006). Interrelationship of hepatic function, thyroid activity and mood status in alcohol-dependent individuals. In Vivo 20, 293-300.
34. Liu, Y., Aryee, M. J., Padyukov, L., Fallin, M. D., Hesselberg, E., Runarsson, A., et al. (2013). Epigenome-wide association data implicate DNA methylation as an intermediary of genetic risk in rheumatoid arthritis. Nat. Biotechnol. 31, 142-147. doi: 10.1038/nbt.2487
35. Manning, M. A., and Eugene Hoyme, H. (2007). Fetal alcohol spectrum disorders: a practical clinical approach to diagnosis. Neurosci. Biobehav. Rev. 31, 230-238. doi: 10.1016/j.neubiorev.2006.06.016
36. Mazzio, E. A., and Soliman, K. F. (2012). Basic concepts of epigenetics: impact of environmental signals on gene expression. Epigenetics 7, 119-130. doi: 10.4161/epi.7.2.18764
37. Mcgivern, R. F., and Redei, E. (1994). Adrenalectomy reverses stress-induced suppression of luteinizing hormone secretion in long-term ovariectomized rats. Physiol. Behav. 55, 1147-1150. doi: 10.1016/0031-9384(94)90402-2
38. Mead, E., and Sarkar, D. (2014). Fetal alcohol spectrum disorders and their transmission through genetic and epigenetic mechanisms. Front. Genet. 5:154. doi: 10.3389/fgene.2014.00154
39. Nunez, Y. O., Truitt, J. M., Gorini, G., Ponomareva, O. N., Blednov, Y. A., Harris, R. A., et al. (2013). Positively correlated miRNA-mRNA regulatory networks in mouse frontal cortex during early stages of alcohol dependence. BMC Genomics 14:725. doi: 10.1186/1471-2164-14-725
40. Rakyan, V. K., Down, T. A., Balding, D. J., and Beck, S. (2011). Epigenome-wide association studies for common human diseases. Nat. Rev. Genet. 12, 529-541. doi: 10.1038/nrg3000
41. Reik, W., Dean, W., and Walter, J. (2001). Epigenetic reprogramming in mammalian development. Science 293, 1089-1093. doi: 10.1126/science.1063443
42. Revskoy, S., Halasz, I., and Redei, E. (1997). Corticotropin-releasing hormone and proopiomelanocortin gene expression is altered selectively in the male rat fetal thymus by maternal alcohol consumption. Endocrinology 138, 389-396. doi: 10.1210/endo.138.1.4838
43. Rouleau, M., Levichek, Z., and Koren, G. (2003). Are mothers who drink heavily in pregnancy victims of FAS. J. FAS Int. 1, 1-5.
44. Seisenberger, S., Peat, J. R., Hore, T. A., Santos, F., Dean, W., and Reik, W. (2013). Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368:20110330. doi: 10.1098/rstb.2011.0330
45. Shukla, P. K., Sittig, L. J., Ullmann, T. M., and Redei, E. E. (2011). Candidate placental biomarkers for intrauterine alcohol exposure. Alcohol Clin. Exp. Res. 35, 559-565. doi: 10.1111/j.1530-0277.2010.01373.x
46. Sittig, L. J. (2012). Developmental Programming of Brain Regional Thyroid Status by the Deiodinase-III: Parent-of-Origin Genetic and Epigenetic Influences. Chicago, IL: Northwestern University.
47. Sittig, L. J., Herzing, L. B., Shukla, P. K., and Redei, E. E. (2011a). Parent-of-origin allelic contributions to deiodinase-3 expression elicit localized hyperthyroid milieu in the hippocampus. Mol. Psychiatry 16, 786-787. doi: 10.1038/mp.2011.19
48. Sittig, L. J., and Redei, E. E. (2010). Paternal genetic contribution influences fetal vulnerability to maternal alcohol consumption in a rat model of fetal alcohol spectrum disorder. PLoS ONE 5:e10058. doi: 10.1371/journal.pone.0010058
49. Sittig, L. J., and Redei, E. E. (2012). Novel polymorphisms within the Dlk1-Dio3 imprinted locus in rat: a putative genetic basis for strain-specific allelic gene expression. Front. Genet. 3:296. doi: 10.3389/fgene.2012.00296
50. Sittig, L. J., Shukla, P. K., Herzing, L. B., and Redei, E. E. (2011b). Strain-specific vulnerability to alcohol exposure in utero via hippocampal parent-of-origin expression of deiodinase-III. FASEB J. 25, 2313-2324. doi: 10.1096/fj.10-179234
51. Skinner, M. K., Haque, C. G., Nilsson, E., Bhandari, R., and Mccarrey, J. R. (2013). Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line. PLoS ONE 8:e66318. doi: 10.1371/journal.pone.0066318
52. Slone, J. L., and Redei, E. E. (2002). Maternal alcohol and adrenalectomy: asynchrony of stress response and forced swim behavior. Neurotoxicol. Teratol 24, 173-178. doi: 10.1016/S0892-0362(01)00186-6
53. Stouder, C., Somm, E., and Paoloni-Giacobino, A. (2011). Prenatal exposure to ethanol: a specific effect on the H19 gene in sperm. Reprod. Toxicol 31, 507-512. doi: 10.1016/j.reprotox.2011.02.009
54. Tunc-Ozcan, E., Ullmann, T. M., Shukla, P. K., and Redei, E. E. (2013). Low-dose thyroxine attenuates autism-associated adverse effects of fetal alcohol in male offspring's social behavior and hippocampal gene expression. Alcohol Clin. Exp. Res. 37, 1986-1995. doi: 10.1111/acer.12183
55. Wilcoxon, J. S., Kuo, A. G., Disterhoft, J. F., and Redei, E. E. (2005). Behavioral deficits associated with fetal alcohol exposure are reversed by prenatal thyroid hormone treatment: a role for maternal thyroid hormone deficiency in FAE. Mol. Psychiatry 10, 961-971. doi: 10.1038/sj.mp.4001694
56. Wilcoxon, J. S., and Redei, E. E. (2004). Prenatal programming of adult thyroid function by alcohol and thyroidhormones. Am. J. Physiol. Endocrinol. Metab. 287, E318-E326. doi: 10.1152/ajpendo.00022.2004
57. Wilcoxon, J. S., Schwartz, J., Aird, F., and Redei, E. E. (2003). Sexually dimorphic effects of maternal alcohol intake and adrenalectomy on left ventricular hypertrophy in rat offspring. Am. J. Physiol. Endocrinol. Metab. 285, E31-E39. doi: 10.1152/ajpendo.00552.2002