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Transposable Elements: Targets for Early Nutritional Effects on Epigenetic Gene Regulation
Open accessAbstract
Early nutrition affects adult metabolism in humans and other mammals, potentially via persistent alterations in DNA methylation. With viable yellow agouti (A(vy)) mice, which harbor a transposable element in the agouti gene, we tested the hypothesis that the metastable methylation status of specific transposable element insertion sites renders them epigenetically labile to early methyl donor nutrition. Our results show that dietary methyl supplementation of a/a dams with extra folic acid, vitamin B(12), choline, and betaine alter the phenotype of their A(vy)/a offspring via increased CpG methylation at the A(vy) locus and that the epigenetic metastability which confers this lability is due to the A(vy) transposable element. These findings suggest that dietary supplementation, long presumed to be purely beneficial, may have unintended deleterious influences on the establishment of epigenetic gene regulation in humans.
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“In this case there is a correlation between DNA methylation at the promoter and silencing of the gene [5,6].”
From A genome-wide screen for modifiers of transgene variegation identifies genes with critical roles in development (2008) · cites this paper as [5]
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Immune and Epigenetic Pathways Linking Childhood Adversity and Health Across the Lifespan
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Variable histone modifications at the Avymetastable epiallele
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“These examples include the viable yellow agouti mouse, and themethylation status at the agouti (A) metastable epiallele of offspring from mothers fed methyl donors such as vitamin B12, methionine, choline and folate throughout pregnancy (Waterland and Jirtle 2003).”
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The X as Model for RNA's Niche in Epigenomic RegulationPreprint
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Stromswold, K. (2006) · Cognition · doi:10.1016/j.cognition.2006.04.007 · Cited by 82
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“Methylation and expression are affected by environmental and genetic influences, such as embryo culture conditions (35), DNA methyl transferase 1 overexpression (36), hyperhomocysteinaemia (34) and folate-deficient or -supplemented diets before and during pregnancy, in the postnatal and post-weaning periods and the Ep…”
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Gene by Environment Interaction in Asthma
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“Dietary intake of methyl donors (such as folate, vitamin B12, choline, and betaine) during pregnancy clearly influenced methylation in a mouse model (85).”
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“Conversely, a high 89 number of offspring of mice fed with a control diet had a lower frequency of CpG 90 methylation and a yellow or slightly mottled coat color (Waterland and Jirtle 2003).”
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Preterm Birth—An Emerging Risk Factor for Adult Hypertension?
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DNA Methylation Patterns Reflect Epigenetic Reprogramming in Bovine Embryos
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“In the agouti viable yellow (A/a) mouse model, maternal supplementation of methyl group donors (folic acid, vitamin B12, choline and betaine) during pregnancy led to CpG DNA hypermethylation at the regulatory region of the A gene, which resulted in a change in offspring's coat color from yellow to brown [22,23].”
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“The mechanism involves DNA methylation (148).”
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Early environmental factors, alteration of epigenetic marks and metabolic disease susceptibility
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MethodPhenotypic Plasticity: What Has DNA Methylation Got to Do with It?
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“Whereas most TEs are silenced epigenetically,(33) some have variable methylation patterns that have been shown to be influenced by nutrition in mice.(9) Their methylation states can alter neighbouring gene expression, exemplified by the Agouti mouse model detailed later.”
InfluentialBacterial folate biosynthesis and colorectal cancer risk: more than just a gut feeling
Kok, D. E. G., Steegenga, W. T., Smid, E. J., Zoetendal, E. G., Ulrich, C. M., & Kampman, E. (2018) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1522499 · Cited by 70
“…that intake or status of folate is associated with DNA methylation of critical genes during early development and in adult life (Joubert et al. 2016; Kok et al. 2015; O’Reilly et al. 2016; Pauwels et al. 2017; SteegersTheunissen et al. 2009; van den Donk et al. 2007; Waterland and Jirtle 2003).”
BackgroundGenetics of schizophrenia: A consensus paper of the WFSBP Task Force on Genetics
Giegling, I., Hosák, L., Mößner, R., Serretti, A., Bellivier, F., Claes, S. J., Collier, D. A., Corrales, A., DeLisi, L. E., Gallo, C., et al. (2017) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2016.1268715 · Cited by 76
Mechanisms of Non-Genetic Inheritance and Psychiatric Disorders
Tóth, M. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.127 · Cited by 69
Gomes, M. V., Toffoli, L. V., Arruda, D. W., Soldera, L. M., Pelosi, G. G., das Neves-Souza, R. D., de Freitas, E. R. F. S., Castro, D. T., & Marquez, A. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052570 · Cited by 71
“First evidences in animal models suggested that dietary intake of micronutrients involved in the one-carbon metabolism, namely folate, vitamin B12, vitamin B6, methionine, choline and betaine might be associated to the availability of the methyl donor Sadenosylmethionine (SAM) and consequently change the DNA methylati…”
BackgroundEarly Determinants of Obesity: Genetic, Epigenetic, and In Utero Influences
Rhee, K. E., Phelan, S., & McCaffery, J. M. (2012) · International Journal of Pediatrics · doi:10.1155/2012/463850 · Cited by 78
“Nutritional components that may influence the methylation of epigenetically susceptible loci include folic acid, vitamin B6 and 12, selenium, choline and betaine, methionine, soy genistein, bisphenol A, tocopherols, diallyl disulfide in garlic, and tea polyphenols [28].”
BackgroundThe Effects of Prenatal Use of Folic Acid and Other Dietary Supplements on Early Child Development
Wehby, G. L., & Murray, J. C. (2007) · Maternal and Child Health Journal · doi:10.1007/s10995-007-0230-3 · Cited by 68
“Folic acid is considered key for general human development primarily through its role in methylation as supported in recent research [35, 36].”
Perturbation of epigenetic status by toxicants
Bombail, V. (2004) · Toxicology Letters · doi:10.1016/j.toxlet.2004.01.003 · Cited by 69
“A recent study demonstrated that dietary supplementation with methyl group donors (choline, methionine, betaine, folic acid and vitamin B12) in nulliparous mice for a 2-week period prior to mating resulted in a higher frequency of lean, brown pups (Waterland and Jirtle, 2003).”
BackgroundEarly Nutrition: Impact on Epigenetics
Mathers, J. C. (2007) · Forum of nutrition/Bibliotheca Nutritio et dieta · doi:10.1159/000107066 · Cited by 67
What transposable elements tell us about genome organization and evolution: the case of Drosophila
Biémont, C., & Vieira, C. P. (2005) · Cytogenetic and Genome Research · doi:10.1159/000084935 · Cited by 67
Modelling the developmental origins of health and disease in the early embryo
Sinclair, K. D., & Singh, R. (2006) · Theriogenology · doi:10.1016/j.theriogenology.2006.09.017 · Cited by 67
“Periods during which nutrient deprivation can lead to altered cardiovascular development and hypertension [16–20], obesity and diabetes [31], hypothalamic–pituitary–adrenal activity [88], growth hormone and insulin metabolism [89,90] and reproductive development [91] (LPD, low protein diet).”
BackgroundResultPreconception Zinc Deficiency Disrupts Postimplantation Fetal and Placental Development in Mice1
Tian, X., Anthony, K., Neuberger, T., & Díaz, F. J. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.113.113910 · Cited by 67
“It has been known for some time that a suboptimal supply of nutrients during pregnancy can impair embryo and fetal development and postnatal health by altering epigenetic modifications of the chromatin [1–5].”
BackgroundSutton, E. F., Gilmore, L. A., Dunger, D. B., Heijmans, B. T., Hivert, M., Ling, C., Martínez, J. A., Ozanne, S. E., Simmons, R. A., Szyf, M., et al. (2016) · Obesity · doi:10.1002/oby.21487 · Cited by 72
“Data suggest that the nutritional status of a mother at the time of conception can permanently influence the epigenome of her offspring, consequently impacting lifelong health (40,73).”
BackgroundMattocks, D. A. L., Mentch, S. J., Shneyder, J., Ables, G. P., Sun, D., Richie, J. P., Locasale, J. W., & Nichenametla, S. N. (2016) · Experimental Gerontology · doi:10.1016/j.exger.2016.12.003 · Cited by 68
“Previous studies show that changes in SAM, SAH and DNA methylation occur as soon as 6–8 weeks after dietary intervention (Brown-Borg et al., 2014; Amaral et al., 2011; Waterland and Jirtle, 2003).”
BackgroundMitochondrial health, the epigenome and healthspan
Aon, M. A., Cortassa, S., Juhaszova, M., & Sollott, S. J. (2016) · Clinical Science · doi:10.1042/cs20160002 · Cited by 66
Genetic Pathways of Aging and Their Relevance in the Dog as a Natural Model of Human Aging
Sándor, S., & Kubinyi, E. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00948 · Cited by 68
“…as well (Hunter et al., 2015), including heavy metal toxicity (Morales et al., 2015), certain genotoxic agents (Stribinskis and Ramos, 2006), and even nutrition (Waterland and Jirtle, 2003), they represent another possible intracellular interface between the living environment/ lifestyle and aging.”
BackgroundHomocysteine—a retrospective and prospective appraisal
McCaddon, A., & Miller, J. W. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1179807 · Cited by 66
Maternal methyl supplemented diets and effects on offspring health
O'Neill, R. J. W., Vrana, P. B., & Rosenfeld, C. S. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00289 · Cited by 68
“Waterland and Jirtle, 2003 a/a and Avy /a mice The a/a females were placed on a control (NIH-31) or NIH-31 diet supplemented with methyl donors/cofactors (same as in Wolff et al., 1998) 2 weeks prior to mating to Avy /a males and throughout gestation and lactation.”
BackgroundMethodIn vitro and in vivo testing methods of epigenomic endpoints for evaluating endocrine disruptors
Greally, J. M. (2013) · ALTEX · doi:10.14573/altex.2013.4.445 · Cited by 66
Zaina, S. (2010) · International Journal of Molecular Medicine · doi:10.3892/ijmm_00000515 · Cited by 65
Provençal, N., Suderman, M. J., Caramaschi, D., Wang, D., Hallett, M. T., Vitaro, F., Tremblay, R. E., & Szyf, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071691 · Cited by 66
Genome-wide DNA methylation variability in adolescent monozygotic twins followed since birth
Lévesque, M. L., Casey, K. F., Szyf, M., Ismaylova, E., Ly, V., Verner, M., Suderman, M. J., Brendgen, M. R., Vitaro, F., Dionne, G., et al. (2014) · Epigenetics · doi:10.4161/15592294.2014.970060 · Cited by 67
Epigenetics as the mediator of fetal programming of adult onset disease: what is the evidence?
Saffery, R., & Novakovic, B. (2014) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.12431 · Cited by 67
Epigenomic profiling indicates a role for DNA methylation in early postnatal liver development
Waterland, R. A., Kellermayer, R., Rached, M.-T., Tatevian, N., Gomes, M. V., Zhang, J., Zhang, L., Chakravarty, A., Zhu, W., Laritsky, E., et al. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp241 · Cited by 67
Veiga‐Lopez, A., Pennathur, S., Kannan, K., Patisaul, H. B., Dolinoy, D. C., Zeng, L., & Padmanabhan, V. (2015) · Endocrinology · doi:10.1210/en.2014-1863 · Cited by 68
Genetic and Epigenomic Footprints of Folate
Salbaum, J. M., & Kappen, C. (2012) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-398397-8.00006-x · Cited by 65
“As a remnant of a viral sequence with a long terminal repeat (LTR) element that can activate transcription, it can override the normal regulatory machinery at the gene (Waterland and Jirtle, 2003).”
BackgroundOey, H., Isbel, L., Hickey, P. F., Ebaid, B., & Whitelaw, E. (2015) · Epigenetics & Chromatin · doi:10.1186/s13072-015-0047-z · Cited by 63
“iiDMRs reported here are poorly annotated with respect to their ability to influence transcription of adjacent genes but are located well within an interval potentially able to drive gene expression, as exemplified by the IAP at Avy, which lies approximately 100 kb from the agouti coding sequence [18].”
BackgroundTransgenerational endocrine pancreatic adaptation in mice from maternal protein restriction in utero
Frantz, E. D. C., Águila, M. B., Mulder, A. D. R. P., & Mandarim‐de‐Lacerda, C. A. (2011) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2011.01.003 · Cited by 65
“Although the exact mechanism that underpins this phenomenon is poorly understood, DNA methylation, various alterations of histone proteins and the control of mRNA expression by non-coding RNAs are all potential candidates (Waterland, 2009; Waterland and Jirtle, 2003).”
Metadata
- Authors
- Waterland, R. A., & Jirtle, R. L.
- Affiliations
- Duke Medical Center (US)
- Corresponding author
- Jirtle, Randy L.
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 2003-08-01
- Volume
- 23
- Issue
- 15
- Pages
- 5293-5300
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC165709
- OpenAlex
- W2100489386
- Cited by
- 2,019
- References
- 35
- Citations by year
- 2026: 30 · 2025: 47 · 2024: 54 · 2023: 37 · 2022: 82 · 2021: 68 · 2020: 38 · 2019: 75 · 2018: 76 · 2017: 88 · 2016: 93 · 2015: 110 · 2014: 143 · 2013: 130 · 2012: 144
- FWCI
- 22.68
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular and Cellular Biology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Cancer Institute (R01CA025951, CA25951)
- National Institute of Environmental Health Sciences (ES08823, R01ES008823)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Nursing › Nutrition and Dietetics › Folate and B Vitamins Research
- Keywords
- transposable elements, DNA methylation, epigenetic inheritance, early life nutrition, methyl donor supplementation, folic acid, vitamin B12, choline, betaine, agouti gene, CpG methylation, maternal diet, offspring phenotype
- MeSH terms
- Alleles, Animals, Betaine, Choline, DNA Transposable Elements, Exons, Folic Acid, Gene Expression Regulation, Mice, Inbred C3H, Mice, Inbred C57BL, Models, Genetic, Molecular Sequence Data, Nutritional Physiological Phenomena, Phenotype, Sulfites, Vitamin B 12, Polymerase Chain Reaction, Sequence Analysis, DNA, CpG Islands, DNA Methylation, Dietary Supplements, Mice
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