Nutrition During Pregnancy Impacts Offspring's Epigenetic Status-Evidence from Human and Animal Studies

Aisling A Geraghty, Karen L Lindsay, Goiuri Alberdi, Fionnuala M McAuliffe, Eileen R Gibney, Aisling A Geraghty, Karen L Lindsay, Goiuri Alberdi, Fionnuala M McAuliffe, Eileen R Gibney

Abstract

Pregnancy is a vital time of growth and development during which maternal nutrition significantly influences the future health of both mother and baby. During pregnancy, the fetus experiences a critical period of plasticity. Epigenetics, specifically DNA methylation, plays an important role here. As nutrition is influential for DNA methylation, this review aims to determine if maternal nutrition during pregnancy can modify the offspring's epigenome at birth. Research focuses on micronutrients and methyl donors such as folate and B vitamins. Evidence suggests that maternal nutrition does not largely influence global methylation patterns, particularly in nutrient-replete populations; however, an important impact on gene-specific methylation is observed. A link is shown between maternal nutrition and the methylome of the offspring; however, there remains a paucity of research. With the potential to use DNA methylation patterns at birth to predict health of the child in later life, it is vital that further research be carried out.

Keywords: epigenetics; nutrition; offspring; pregnancy; programing.

References

    1. Waterland R, Kellermayer R, Laritsky E, et al. Season of conception in rural gambia affects DNA methylation at putative human metastable epialleles. PLoS Genet. 2010;6(12):1–10.
    1. Grieger J, Clifton V. A review of the impact of dietary intakes in human pregnancy on infant birthweight. Nutrients. 2014;7(1):153–178.
    1. Walsh J, McAuliffe F. Impact of maternal nutrition on pregnancy outcome—does it matter what pregnant women eat? Best Pract Res Clin Obstet Gynaecol. 2015;29(1):63–78.
    1. Gresham E, Byles J, Bisquera A, Hure A. Effects of dietary interventions on neonatal and infant outcomes: a systematic review and meta-analysis. Am J Clin Nutr. 2014;100(5):1298–1321.
    1. Dubois L, Ohm Kyvik K, Girard M, et al. Genetic and environmental contributions to weight, height, and BMI from birth to 19 years of age: an international study of over 12,000 twin pairs. PLoS One. 2012;7(2):e30153.
    1. Godfrey K, Barker D. Fetal programming and adult health. Public Health Nutr. 2001;4(2B):611–624.
    1. Barker D. Fetal origins of coronary heart disease. BMJ. 1995;311(6998):171–174.
    1. Ekamper P, van Poppel F, Stein A, Bijwaard G, Lumey L. Prenatal famine exposure and adult mortality from cancer, cardiovascular disease, and other causes through age 63 years. Am J Epidemiol. 2015;181(4):271–279.
    1. Painter RC, de Rooij SR, Bossuyt PM, et al. Early onset of coronary artery disease after prenatal exposure to the Dutch famine. Am J Clin Nutr. 2006;84(2):322–327.
    1. Painter R, Osmond C, Gluckman P, Hanson M, Phillips D, Roseboom T. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG. 2008;115(10):1243–1249.
    1. Bernal A, Jirtle R. Epigenomic disruption: the effects of early developmental exposures. Birth Defects Res A Clin Mol Teratol. 2011;6203(919):1–14.
    1. Waddington C. The epigenotype. 1942. Int J Epidemiol. 2012;41(1):10–13.
    1. McKay J, Mathers J. Diet induced epigenetic changes and their implications for health. Acta Physiol. 2011;202(2):103–118.
    1. Schaevitz L, Berger-sweeney J. Gene-environment interactions and epigenetic pathways in autism: the importance of one-carbon metabolism. ILAR J. 2012;53(3–4):322–340.
    1. Pike B, Greiner T, Wang X, et al. DNA methylation profiles in diffuse large B-cell lymphoma and their relationship to gene expression status. Leukemia. 2009;22(5):1035–1043.
    1. Crider K, Yang T, Berry R, Bailey L. Folate and DNA methylation: a review of molecular mechanisms and the evidence for folate’s role. Adv Nutr. 2012;3(14):21–38.
    1. Nakao M. Epigenetics: interaction of DNA methylation and chromatin. Gene. 2001;278:25–31.
    1. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6–21.
    1. Lehnen H, Zechner U, Haaf T. Epigenetics of gestational diabetes mellitus and offspring health: the time for action is in early stages of life. Mol Hum Reprod. 2013;19(7):415–422.
    1. Marsit C. Influence of environmental exposure on human epigenetic regulation. J Exp Biol. 2015;3:71–79.
    1. Heijmans B, Tobi E, Stein A, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008;105(44):17046–17049.
    1. Tobi E, Slagboom P, van Dongen J, et al. Prenatal famine and genetic variation are independently and additively associated with DNA methylation at regulatory loci within IGF2/H19. PLoS One. 2012;7(5):e37933.
    1. Finer S, Mathews C, Lowe R, et al. Maternal gestational diabetes is associated with genome-wide DNA methylation variation in placenta and cord blood of exposed offspring. Hum Mol Genet. 2015;44:1–31.
    1. Sharp G, Lawlor D, Richmond R, et al. Maternal pre-pregnancy BMI and gestational weight gain, offspring DNA methylation and later offspring adiposity: findings from the Avon Longitudinal Study of Parents and Children. Int J Epidemiol. 2015;44(4):1288–1304.
    1. Morales E, Groom A, Lawlor D, Relton C. DNA methylation signatures in cord blood associated with maternal gestational weight gain: results from the ALSPAC cohort. BMC Res Notes. 2014;7(1):278.
    1. Guénard F, Deshaies Y, Cianflone K, Kral J, Marceau P, Vohl M. Differential methylation in glucoregulatory genes of offspring born before vs. after maternal gastrointestinal bypass surgery. Proc Natl Acad Sci U S A. 2013;110(28):11439–11444.
    1. Crider K, Quinlivan E, Berry R, et al. Genomic DNA methylation changes in response to folic acid supplementation in a population-based intervention study among women of reproductive age. PLoS One. 2011;6(12):e28144.
    1. Rampersaud G, Kauwell G, Hutson AD, Cerda J, Bailey L. Genomic DNA methylation decreases in response to moderate folate depletion in elderly women. Am J Clin Nutr. 2000;72:998–1003.
    1. Anderson O, Sant K, Dolinoy D. Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism, and DNA methylation. J Nutr Biochem. 2012;23(8):853–859.
    1. Godfrey K, Sheppard A, Gluckman P, et al. Epigenetic gene promoter methylation at birth is associated with child’s later adiposity. Diabetes. 2011;60:1528–1534.
    1. Sinclair K, Allegrucci C, Singh R, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci U S A. 2007;104:19351–19356.
    1. Hollingsworth J, Maruoka S, Boon K, et al. In utero supplementation with methyl donors enhances allergic airway disease in mice. J Clin Invest. 2008;118(10):3462–3469.
    1. Wolff G, Kodell R, Moore S, Cooney C. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 1998;12(11):949–957.
    1. Cooney C, Dave A, Wolff G. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr. 2002;132(8 suppl):2393S–2400S.
    1. Kovacheva V, Mellott T, Davison J, et al. Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression. J Biol Chem. 2007;282(43):31777–31788.
    1. Okano M, Bell D, Haber D, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 1999;99:247–257.
    1. Maloney C, Hay S, Young L, Sinclair K, Rees W. A methyl-deficient diet fed to rat dams during the peri-conception period programs glucose homeostasis in adult male but not female offspring. J Nutr. 2011;141(1):95–100.
    1. Lillycrop K, Phillips E, Jackson A, Hanson M, Burdge G. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005;135(6):1382–1386.
    1. Gong L, Pan Y, Chen H. Gestational low protein diet in the rat mediates Igf2 gene expression in male offspring via altered hepatic DNA methylation. Epigenetics. 2010;5(7):619–626.
    1. Masuyama H, Hiramatsu Y. Effects of a high-fat diet exposure in utero on the metabolic syndrome-like phenomenon in mouse offspring through epigenetic changes in adipocytokine gene expression. Endocrinology. 2012;153(6):2823–2830.
    1. Dunn G, Bale T. Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology. 2009;150(11):4999–5009.
    1. Burdge G, Slater-Jefferies J, Torrens C, Phillips E. Dietary protein restriction of pregnant rats in the F 0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr. 2008;97(3):435–439.
    1. Fryer A, Nafee T, Ismail K, Carroll W, Emes R, Farrell W. LINE-1 DNA methylation is inversely correlated with cord plasma homocysteine in man: a preliminary study. Epigenetics. 2009;4(6):394–398.
    1. Amarasekera M, Martino D, Ashley S, et al. Genome-wide DNA methylation profiling identifies a folate-sensitive region of differential methylation upstream of ZFP57-imprinting regulator in humans. FASEB J. 2014;28(9):4068–4076.
    1. Boeke C, Baccarelli A, Kleinman K, et al. Gestational intake of methyl donors and global LINE-1 DNA methylation in maternal and cord blood: prospective results from a folate-replete population. Epigenetics. 2012;7(3):253–260.
    1. Fryer A, Emes R, Ismail K, et al. Quantitative, high-resolution epigenetic profiling of CpG loci identifies associations with cord blood plasma homocysteine and birth weight in humans. Epigenetics. 2011;6(1):86–94.
    1. McKay J, Groom A, Potter C, et al. Genetic and non-genetic influences during pregnancy on infant global and site specific DNA methylation: role for folate gene variants and vitamin B 12. PLoS One. 2012;7(3):e33290.
    1. Azzi S, Sas T, Koudou Y, et al. Degree of methylation of ZAC1 (PLAGL1) is associated with prenatal and post-natal growth in healthy infants of the EDEN mother child cohort. Epigenetics. 2014;9(3):338–345.
    1. Hoyo C, Murtha A, Schildkraut J, et al. Methylation variation at IGF2 differentially methylated regions and maternal folic acid use before and during pregnancy. Epigenetics. 2011;6(7):928–936.
    1. Steegers-Theunissen R, Obermann-Borst S, Kremer D, et al. Periconceptional maternal folic acid use of 400 μg per day is related to increased methylation of the IGF2 gene in the very young child. PLoS One. 2009;4(11):1–5.
    1. Alvarez R, Checa M, Brun S, et al. Both retinoic-acid-receptor- and retinoid-X-receptor-dependent signalling pathways mediate the induction of the brownadipose-tissue-uncoupling-protein-1 gene by retinoids. Biochem J. 2000;345:91–97.
    1. Zhang F, Cardarelli R, Carroll J, et al. Significant differences in global genomic DNA methylation by gender and race/ethnicity in peripheral blood. Epigenetics. 2011;6(5):623–629.
    1. Khulan B, Cooper W, Skinner B, et al. Periconceptional maternal micronutrient supplementation is associated with widespread gender related changes in the epigenome: a study of a unique resource in the Gambia. Hum Mol Genet. 2012;21(9):2086–2101.
    1. Relton C, Groom A, Pourcain B, et al. DNA methylation patterns in cord blood DNA and body size in childhood. PLoS One. 2012;1821;7(3):e3.

Source: PubMed

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