Maternal choline intake alters the epigenetic state of fetal cortisol‐regulating genes in humans

Jiang, Xinyin; Yan, Jian; West, Allyson A.; Perry, Clifton; Malysheva, Olga; Devapatla, Srisatish; Pressman, Eva; Vermeylen, Françoise; Caudill, Marie A.

doi:10.1096/fj.12-207894

Cited by 194 publications

(189 citation statements)

References 37 publications

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“…In zebrafish, oocytes are hypomethylated (75-80% CpG methylation) relative to sperm (91-95%), which is similar to the situation in mice (Jiang et al, 2012;Potok et al, 2013). However, a striking observation in zebrafish is that the sperm methylome is inherited without significant changes until zygotic gene activation (blastula stage, approximately 1000 cells, approximately 3 h post fertilization) as demonstrated using whole-genome bisulfite sequencing of gametes and early developmental embryos (Jiang et al, 2013;Potok et al, 2013).…”

Section: (3) Evidence For Epigenetic Inheritance In Zebrafishmentioning

confidence: 78%

“…In addition to folic acid, the influence of prenatal dietary supplementation of choline, which provides methyl groups as a substrate for DNA methyltransferases (Batra, Sridhar & Devasagayam, 2010), has also attracted interest in terms of the physiological and psychological health of offspring (Zeisel, 2006;Jiang et al, 2012). In particular, high maternal dietary choline intake in humans leads to a lower risk of neural tube defects in infants (Shaw et al, 2004).…”

Section: (C) Parental Nutrition-induced Epigenetic Inheritancementioning

confidence: 99%

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Lamarck rises from his grave: parental environment‐induced epigenetic inheritance in model organisms and humans

2017

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Organisms can change their physiological/behavioural traits to adapt and survive in changed environments. However, whether these acquired traits can be inherited across generations through non-genetic alterations has been a topic of debate for over a century. Emerging evidence indicates that both ancestral and parental experiences, including nutrition, environmental toxins, nurturing behaviour, and social stress, can have powerful effects on the physiological, metabolic and cellular functions in an organism. In certain circumstances, these effects can be transmitted across several generations through epigenetic (i.e. non-DNA sequence-based rather than mutational) modifications. In this review, we summarize recent evidence on epigenetic inheritance from parental environment-induced developmental and physiological alterations in nematodes, fruit flies, zebrafish, rodents, and humans. The epigenetic modifications demonstrated to be both susceptible to modulation by environmental cues and heritable, including DNA methylation, histone modification, and small non-coding RNAs, are also summarized. We particularly focus on evidence that parental environment-induced epigenetic alterations are transmitted through both the maternal and paternal germlines and exert sex-specific effects. The thought-provoking data presented here raise fundamental questions about the mechanisms responsible for these phenomena. In particular, the means that define the specificity of the response to parental experience in the gamete epigenome and that direct the establishment of the specific epigenetic change in the developing embryos, as well as in specific tissues in the descendants, remain obscure and require elucidation. More precise epigenetic assessment at both the genome-wide level and single-cell resolution as well as strategies for breeding at relatively sensitive periods of development and manipulation aimed at specific epigenetic modification are imperative for identifying parental environment-induced epigenetic marks across generations. Considering their diverse epigenetic architectures, the conservation and prevalence of the mechanisms underlying epigenetic inheritance in non-mammals require further investigation in mammals. Interpretation of the consequences arising from epigenetic inheritance on organisms and a better understanding of the underlying mechanisms will provide insight into how gene-environment interactions shape developmental processes and physiological functions, which in turn may have wide-ranging implications for human health, and understanding biological adaptation and evolution.

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Section: (3) Evidence For Epigenetic Inheritance In Zebrafishmentioning

confidence: 78%

Section: (C) Parental Nutrition-induced Epigenetic Inheritancementioning

confidence: 99%

Lamarck rises from his grave: parental environment‐induced epigenetic inheritance in model organisms and humans

2017

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“…These include, for example, up-regulation of System A transporters, which are responsible for transporting amino acids to the fetus (Coan et al 2010;Burton and Fowden 2012), iron transport proteins (Bradley et al 2004), which absorb iron from maternal blood, and placental corticotropin releasing hormone (CRH), which may stimulate maternal glucose production needed to support the growing brain (Gangestad et al 2012). CRH gene promoter DNA methylation has been correlated with its expression in the placenta (Jiang et al 2012); increased gestational age was associated with decreased DNA methylation at CpG sites associated with the CRH gene as well as other cortisol signaling and steroidogenic genes in the placenta (Hogg et al 2013a). Increased DNA methylation at the promoter region of SLC2A3, the gene encoding the glucose transporter GLUT3, was associated with decreased GLUT3 expression through gestation ).…”

Section: Changes With Gestational Agementioning

confidence: 99%

The Human Placental Methylome

Robinson

Price

2015

Cold Spring Harbor Perspectives in Medicine

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This review provides an overview of the unique features of DNA methylation in the human placenta. We discuss the importance of understanding placental development, structure, and function in the interpretation of DNA methylation data. Examples are given of how DNA methylation is important in regulating placental-specific gene expression, including monoallelic expression and X-chromosome inactivation in the placenta. We also discuss studies of global DNA methylation changes in the context of placental pathology and environmental exposures.

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“…Global DNA methylation and site-specific DNA methylation (LEP, IL10, IGF2, and GNASAS1) was, however, not altered by maternal supplemental choline intake. 16 The long-term effects of these methylation changes, due to maternal supplementation, on offspring health remain unknown. In this study, we aimed to determine the effect of maternal dietary methyl-group donor intake (methionine, folate, choline, and betaine) and supplemental intake (folic acid) before and during each trimester of pregnancy on global DNA methylation and hydroxymethylation and gene specific methylation in cord blood in patients from the MAternal Nutrition and Offspring's Epigenome (MANOE) cohort.…”

Section: Introductionmentioning

confidence: 99%

Dietary and supplemental maternal methyl-group donor intake and cord blood DNA methylation

et al. 2016

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Maternal nutrition is critically involved in the development and health of the fetus. We evaluated maternal methyl-group donor intake through diet (methionine, betaine, choline, folate) and supplementation (folic acid) before and during pregnancy in relation to global DNA methylation and hydroxymethylation and gene specific (IGF2 DMR, DNMT1, LEP, RXRA) cord blood methylation. A total of 115 mother-infant pairs were enrolled in the MAternal Nutrition and Offspring's Epigenome (MANOE) study. The intake of methylgroup donors was assessed using a food-frequency questionnaire. LC-MS/MS and pyrosequencing were used to measure global and gene specific methylation, respectively. Dietary intake of methyl-groups before and during pregnancy was associated with changes in LEP, DNMT1, and RXRA cord blood methylation. Statistically significant higher cord blood LEP methylation was observed when mothers started folic acid supplementation more than 6 months before conception compared with 3-6 months before conception (34.6 § 6.3% vs. 30.1 § 3.6%, P D 0.011, LEP CpG1) or no folic acid used before conception (16.2 § 4.4% vs. 13.9 § 3%, P D 0.036 for LEP CpG3 and 24.5 § 3.5% vs. 22.2 § 3.5%, P D 0.045 for LEP mean CpG). Taking folic acid supplements during the entire pregnancy resulted in statistically significantly higher cord blood RXRA methylation as compared with stopping supplementation in the second trimester (12.3 § 1.9% vs. 11.1 § 2%, P D 0.008 for RXRA mean CpG). To conclude, long-term folic acid use before and during pregnancy was associated with higher LEP and RXRA cord blood methylation, respectively. To date, pregnant women are advised to take a folic acid supplement of 400 mg/day from 4 weeks before until 12 weeks of pregnancy. Our results suggest significant epigenetic modifications when taking a folic acid supplement beyond the current advice.

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Maternal choline intake alters the epigenetic state of fetal cortisol‐regulating genes in humans

Cited by 194 publications

References 37 publications

Lamarck rises from his grave: parental environment‐induced epigenetic inheritance in model organisms and humans

Lamarck rises from his grave: parental environment‐induced epigenetic inheritance in model organisms and humans

The Human Placental Methylome

Dietary and supplemental maternal methyl-group donor intake and cord blood DNA methylation

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