Male Germline Transmits Fetal Alcohol Epigenetic Marks for Multiple Generations: a Review

Overview

Journal Addict Biol

Specialty Psychiatry

Date 2015 Jan 13

PMID 25581210

Citations 20

Authors

Dipak K Sarkar

Affiliations

Soon will be listed here.

Abstract

Alcohol exposure during fetal and early postnatal development can lead to an increased incidence of later life adult-onset diseases. Examples include central nervous system dysfunction, depression, anxiety, hyperactivity, and an inability to deal with stressful situations, increased infection and cancer. Direct effects of alcohol leading to developmental abnormalities often involve epigenetic modifications of genes that regulate cellular functions. Epigenetic marks carried over from the parents are known to undergo molecular programming events that happen early in embryonic development by a wave of DNA demethylation, which leaves the embryo with a fresh genomic composition. The proopiomelanocortin (Pomc) gene controls neuroendocrine-immune functions and is imprinted by fetal alcohol exposure. Recently, this gene has been shown to be hypermethylated through three generations. Additionally, the alcohol epigenetic marks on the Pomc gene are maintained in the male but not in the female germline during this transgenerational transmission. These data suggest that the male-specific chromosome might be involved in transmitting alcohol epigenetic marks through multiple generations.

Citing Articles

The Impact of Oxidative Stress on the Epigenetics of Fetal Alcohol Spectrum Disorders.

Terracina S, Tarani L, Ceccanti M, Vitali M, Francati S, Lucarelli M Antioxidants (Basel). 2024; 13(4).

PMID: 38671857 PMC: 11047541. DOI: 10.3390/antiox13040410.

Alcohol-Associated Tissue Injury: Current Views on Pathophysiological Mechanisms.

Simon L, Souza-Smith F, Molina P Annu Rev Physiol. 2022; 84:87-112.

PMID: 35143331 PMC: 11268381. DOI: 10.1146/annurev-physiol-060821-014008.

Transgenerational Abnormalities Induced by Paternal Preconceptual Alcohol Drinking: Findings from Humans and Animal Models.

Terracina S, Ferraguti G, Tarani L, Messina M, Lucarelli M, Vitali M Curr Neuropharmacol. 2021; 20(6):1158-1173.

PMID: 34720083 PMC: 9886817. DOI: 10.2174/1570159X19666211101111430.

Toxic and Teratogenic Effects of Prenatal Alcohol Exposure on Fetal Development, Adolescence, and Adulthood.

Chung D, Pinson M, Bhenderu L, Lai M, Patel R, Miranda R Int J Mol Sci. 2021; 22(16).

PMID: 34445488 PMC: 8395909. DOI: 10.3390/ijms22168785.

Sex-Determining Region Y Controls the Effects of Fetal Alcohol Exposure on Proopiomelanocortin Gene Expression.

Gangisetty O, Mead E, Sarkar D Front Neurosci. 2021; 15:608102.

PMID: 33796006 PMC: 8008069. DOI: 10.3389/fnins.2021.608102.

References

Guerrero-Bosagna C, Settles M, Lucker B, Skinner M . Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One. 2010; 5(9). PMC: 2948035. DOI: 10.1371/journal.pone.0013100. View

Bird A, Taggart M, Frommer M, MILLER O, MacLeod D . A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA. Cell. 1985; 40(1):91-9. DOI: 10.1016/0092-8674(85)90312-5. View

Aalto A, Pasquinelli A . Small non-coding RNAs mount a silent revolution in gene expression. Curr Opin Cell Biol. 2012; 24(3):333-40. PMC: 3372702. DOI: 10.1016/j.ceb.2012.03.006. View

Buiting K, Gross S, Lich C, Gillessen-Kaesbach G, El-Maarri O, Horsthemke B . Epimutations in Prader-Willi and Angelman syndromes: a molecular study of 136 patients with an imprinting defect. Am J Hum Genet. 2003; 72(3):571-7. PMC: 1180233. DOI: 10.1086/367926. View

Halsted C, Villanueva J, Devlin A, Niemela O, Parkkila S, Garrow T . Folate deficiency disturbs hepatic methionine metabolism and promotes liver injury in the ethanol-fed micropig. Proc Natl Acad Sci U S A. 2002; 99(15):10072-7. PMC: 126626. DOI: 10.1073/pnas.112336399. View

Abel E . Paternal contribution to fetal alcohol syndrome. Addict Biol. 2004; 9(2):127-33. DOI: 10.1080/13556210410001716980. View

Bird A . Molecular biology. Methylation talk between histones and DNA. Science. 2001; 294(5549):2113-5. DOI: 10.1126/science.1066726. View

Grossniklaus U, Kelly W, Kelly B, Ferguson-Smith A, Pembrey M, Lindquist S . Transgenerational epigenetic inheritance: how important is it?. Nat Rev Genet. 2013; 14(3):228-35. PMC: 4066847. DOI: 10.1038/nrg3435. View

Hellemans K, Sliwowska J, Verma P, Weinberg J . Prenatal alcohol exposure: fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci Biobehav Rev. 2009; 34(6):791-807. PMC: 5518679. DOI: 10.1016/j.neubiorev.2009.06.004. View

10.

Weaver I . Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: let's call the whole thing off. Epigenetics. 2007; 2(1):22-8. DOI: 10.4161/epi.2.1.3881. View

11.

Skinner M . What is an epigenetic transgenerational phenotype? F3 or F2. Reprod Toxicol. 2007; 25(1):2-6. PMC: 2249610. DOI: 10.1016/j.reprotox.2007.09.001. View

12.

Guo W, Crossey E, Zhang L, Zucca S, George O, Valenzuela C . Alcohol exposure decreases CREB binding protein expression and histone acetylation in the developing cerebellum. PLoS One. 2011; 6(5):e19351. PMC: 3104983. DOI: 10.1371/journal.pone.0019351. View

13.

Sarkar D, Kuhn P, Marano J, Chen C, Boyadjieva N . Alcohol exposure during the developmental period induces beta-endorphin neuronal death and causes alteration in the opioid control of stress axis function. Endocrinology. 2007; 148(6):2828-34. DOI: 10.1210/en.2006-1606. View

14.

Guibert S, Weber M . Functions of DNA methylation and hydroxymethylation in mammalian development. Curr Top Dev Biol. 2013; 104:47-83. DOI: 10.1016/B978-0-12-416027-9.00002-4. View

15.

Nishino K, Hattori N, Sato S, Arai Y, Tanaka S, Nagy A . Non-CpG methylation occurs in the regulatory region of the Sry gene. J Reprod Dev. 2011; 57(5):586-93. DOI: 10.1262/jrd.11-033a. View

16.

Pandey S, Ugale R, Zhang H, Tang L, Prakash A . Brain chromatin remodeling: a novel mechanism of alcoholism. J Neurosci. 2008; 28(14):3729-37. PMC: 6671100. DOI: 10.1523/JNEUROSCI.5731-07.2008. View

17.

Rachdaoui N, Sarkar D . Transgenerational epigenetics and brain disorders. Int Rev Neurobiol. 2014; 115:51-73. DOI: 10.1016/B978-0-12-801311-3.00002-0. View

18.

Bekdash R, Zhang C, Sarkar D . Gestational choline supplementation normalized fetal alcohol-induced alterations in histone modifications, DNA methylation, and proopiomelanocortin (POMC) gene expression in β-endorphin-producing POMC neurons of the hypothalamus. Alcohol Clin Exp Res. 2013; 37(7):1133-42. PMC: 3659188. DOI: 10.1111/acer.12082. View

19.

Shi L, Wu J . Epigenetic regulation in mammalian preimplantation embryo development. Reprod Biol Endocrinol. 2009; 7:59. PMC: 2702308. DOI: 10.1186/1477-7827-7-59. View

20.

Rakyan V, Whitelaw E . Transgenerational epigenetic inheritance. Curr Biol. 2003; 13(1):R6. DOI: 10.1016/s0960-9822(02)01377-5. View