Epigenetic Programming and Fetal Metabolic Programming

Effect of In Utero and Early-Life Conditions on Adult Health and Disease

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Persistent epigenetic differences associated with prenatal exposure to famine in humans

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Elective induction versus spontaneous labor after sonographic diagnosis of fetal macrosomia.

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In utero programming of chronic disease

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Obesity in Young Men after Famine Exposure in Utero and Early Infancy

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Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress

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Fetuses of obese mothers develop insulin resistance in utero

Catalano, P. M., Presley, L., Minium, J., & Hauguel-de Mouzon, S. (2009) · Diabetes Care · doi:10.2337/dc08-2077 · Cited by 655

DNA methylation signatures link prenatal famine exposure to growth and metabolism

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The interplay of epigenetic marks during stem cell differentiation and development

Atlasi, Y., & Stunnenberg, H. G. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.57 · Cited by 583

Stress-induced perinatal and transgenerational epigenetic programming of brain development and mental health

Babenko, O., Kovalchuk, I., & Metz, G. A. S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.013 · Cited by 513

Maternal nutrition at conception modulates DNA methylation of human metastable epialleles

Dominguez-Salas, P., Moore, S. E., Baker, M. S., Bergen, A. W., Cox, S. E., Dyer, R. A., Fulford, A. J., Guan, Y., Laritsky, E., Silver, M. J., et al. (2014) · Nature Communications · doi:10.1038/ncomms4746 · Cited by 506

Epigenetic and transgenerational reprogramming of brain development

Bale, T. L. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3818 · Cited by 505

Specification and epigenetic programming of the human germ line

Tang, W. W. C., Kobayashi, T., Irie, N., Dietmann, S., & Surani, M. A. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.88 · Cited by 463

Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome

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Transgenerational inheritance: Models and mechanisms of non–DNA sequence–based inheritance

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Epigenetic germline inheritance of diet-induced obesity and insulin resistance

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Transgenerational Glucose Intolerance With Igf2/H19 Epigenetic Alterations in Mouse Islet Induced by Intrauterine Hyperglycemia

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Maternal BMI at the start of pregnancy and offspring epigenome-wide DNA methylation: findings from the pregnancy and childhood epigenetics (PACE) consortium

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Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state

Crevillén, P., Yang, H., Cui, X., Greeff, C., Trick, M., Qiu, Q., Cao, X., & Dean, C. (2014) · Nature · doi:10.1038/nature13722 · Cited by 280

Metabolic Syndrome Scientific Statement by the American Heart Association and the National Heart, Lung, and Blood Institute

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Leptin Gene Epigenetic Adaptation to Impaired Glucose Metabolism During Pregnancy

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Obesity-induced DNA hypermethylation of the adiponectin gene mediates insulin resistance

Kim, A. Y., Park, Y. J., Pan, X., Shin, K. C., Kwak, S., Bassas, A. F., Sallam, R. M., Park, K. S., Alfadda, A. A., Xu, A., et al. (2015) · Nature Communications · doi:10.1038/ncomms8585 · Cited by 241

Leptin resistance in obesity: An epigenetic landscape

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Embryonic stem cell and induced pluripotent stem cell: an epigenetic perspective

Liang, G., & Zhang, Y. (2012) · Cell Research · doi:10.1038/cr.2012.175 · Cited by 232

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

Masuyama, H., & Hiramatsu, Y. (2012) · Endocrinology · doi:10.1210/en.2011-2161 · Cited by 212

Chromatin “Prepattern” and Histone Modifiers in a Fate Choice for Liver and Pancreas

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Diabetes mellitus—advances and challenges in human β-cell proliferation

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Dissecting neural differentiation regulatory networks through epigenetic footprinting

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The role of diet and exercise in the transgenerational epigenetic landscape of T2DM

Barrès, R., & Zierath, J. R. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.87 · Cited by 198

Epigenetic transgenerational inheritance

Skinner, M. K. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.206 · Cited by 186

Developmental bisphenol A (BPA) exposure leads to sex-specific modification of hepatic gene expression and epigenome at birth that may exacerbate high-fat diet-induced hepatic steatosis

Strakovsky, R. S., Wang, H., Engeseth, N. J., Flaws, J. A., Helferich, W. G., Pan, Y., & Lezmi, S. (2015) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2015.02.021 · Cited by 180

Embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes

Han, L., Ren, C., Li, L., Li, X., Ge, J., Wang, H., Miao, Y., Guo, X., Moley, K. H., Shu, W., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0055-6 · Cited by 178

Maternal Weight Gain in Pregnancy and Risk of Obesity among Offspring: A Systematic Review

Lau, E. Y., Liu, J., Archer, E., McDonald, S. M., & Liu, J. (2014) · Journal of Obesity · doi:10.1155/2014/524939 · Cited by 176

A maternal high‐fat diet modulates fetal SIRT1 histone and protein deacetylase activity in nonhuman primates

Suter, M., Chen, A., Burdine, M., Choudhury, M., Harris, R. A., Lane, R. H., Friedman, J. E., Grove, K. L., Tackett, A. J., & Aagaard, K. M. (2012) · The FASEB Journal · doi:10.1096/fj.12-212878 · Cited by 175

Dietary intervention rescues maternal obesity induced behavior deficits and neuroinflammation in offspring

Kang, S. S., Kurti, A., Fair, D. A., & Fryer, J. D. (2014) · Journal of Neuroinflammation · doi:10.1186/s12974-014-0156-9 · Cited by 167

DNA methylation directs functional maturation of pancreatic β cells

Dhawan, S., Tschen, S.-I., Zeng, C., Guo, T., Hebrok, M., Matveyenko, A. V., & Bhushan, A. (2015) · Journal of Clinical Investigation · doi:10.1172/jci79956 · Cited by 164

Birthweight is associated with DNA promoter methylation of the glucocorticoid receptor in human placenta

Filiberto, A. C., Maccani, M. A., Koestler, D. C., Wilhelm-Benartzi, C. S., Avissar-Whiting, M., Banister, C. E., Gagne, L. A., & Marsit, C. J. (2011) · Epigenetics · doi:10.4161/epi.6.5.15236 · Cited by 162

Longitudinal analysis of DNA methylation associated with birth weight and gestational age

Simpkin, A. J., Suderman, M. J., Gaunt, T. R., Lyttleton, O., McArdle, W. L., Ring, S. M., Tilling, K. M., Smith, G. D., & Relton, C. L. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv119 · Cited by 160

Epigenetic Changes in the Hypothalamic Proopiomelanocortin and Glucocorticoid Receptor Genes in the Ovine Fetus after Periconceptional Undernutrition

Stevens, A., Begum, G., Cook, A., Connor, K. L., Rumball, C. W. H., Oliver, M. H., Challis, J. R. G., Bloomfield, F. H., & White, A. E. (2010) · Endocrinology · doi:10.1210/en.2010-0094 · Cited by 157

Birthweight, Maternal Weight Trajectories and Global DNA Methylation of LINE-1 Repetitive Elements

Michels, K. B., Harris, H. R., & Barault, L. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025254 · Cited by 157

Maternal Obesity Induces Epigenetic Modifications to Facilitate Zfp423 Expression and Enhance Adipogenic Differentiation in Fetal Mice

Yang, Q.-Y., Liang, J.-F., Rogers, C. J., Zhao, J.-X., Zhu, M.-J., & Du, M. (2013) · Diabetes · doi:10.2337/db13-0433 · Cited by 152

Association between maternal adherence to healthy lifestyle practices and risk of obesity in offspring: results from two prospective cohort studies of mother-child pairs in the United States

Dhana, K., Haines, J., Liu, G., Zhang, C., Wang, X., Field, A. E., Chavarro, J. E., & Sun, Q. (2018) · BMJ · doi:10.1136/bmj.k2486 · Cited by 151

Maternal high-fat diet consumption modulates hepatic lipid metabolism and microRNA-122 (miR-122) and microRNA-370 (miR-370) expression in offspring

Benatti, R. O., Melo, A. M., Borges, F. O., Ignácio-Souza, L. M., Simino, L. A. D. P., Milanski, M., Velloso, L. A., Torsoni, M. A., & Torsoni, A. S. (2014) · British Journal Of Nutrition · doi:10.1017/s0007114514000579 · Cited by 149

Ancestral perinatal obesogen exposure results in a transgenerational thrifty phenotype in mice

Chamorro-García, R., Díaz-Castillo, C., Shoucri, B. M., Kaech, H., Leavitt, R., Shioda, T., & Blumberg, B. (2017) · Nature Communications · doi:10.1038/s41467-017-01944-z · Cited by 149

Increased global placental DNA methylation levels are associated with gestational diabetes

Reichetzeder, C., Dwi Putra, S. E., Pfab, T., Slowinski, T., Neuber, C., Kleuser, B., & Hocher, B. (2016) · Clinical Epigenetics · doi:10.1186/s13148-016-0247-9 · Cited by 144

Arsenic exposure in early pregnancy alters genome-wide DNA methylation in cord blood, particularly in boys

Bröberg, K., Ahmed, S., Engström, K. S., Hossain, M. B., Mlakar, S. J., Bottai, M., Grandér, M., Raqib, R., & Vahter, M. (2014) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174414000221 · Cited by 143

Gestational high fat diet programs hepatic phosphoenolpyruvate carboxykinase gene expression and histone modification in neonatal offspring rats

Strakovsky, R. S., Zhang, X., Zhou, D., & Pan, Y. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.203950 · Cited by 141

Maternal high-fat diet induces insulin resistance and deterioration of pancreatic β-cell function in adult offspring with sex differences in mice

Yokomizo, H., Inoguchi, T., Sonoda, N., Sakaki, Y., Maeda, Y., Inoue, T., Hirata, E., Takei, R., Ikeda, N., Fujii, M., et al. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00688.2013 · Cited by 141

Epigenetics of programmed obesity: alteration in IUGR rat hepatic IGF1 mRNA expression and histone structure in rapid vs. delayed postnatal catch-up growth

Tosh, D. N., Fu, Q., Callaway, C. W., McKnight, R. A., McMillen, I. C., Ross, M. G., Lane, R. H., & Desai, M. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00052.2010 · Cited by 136

Epigenetic programming of obesity and diabetes by in utero exposure to gestational diabetes mellitus

Ruchat, S.-M., Hivert, M., & Bouchard, L. (2013) · Nutrition Reviews · doi:10.1111/nure.12057 · Cited by 135

DNA methylation in blood from neonatal screening cards and the association with BMI and insulin sensitivity in early childhood

van Dijk, S. J., Peters, T. J., Buckley, M. J., Zhou, J., Jones, P. A., Gibson, R. A., Makrides, M., Mühlhäusler, B. S., & Molloy, P. L. (2017) · International Journal of Obesity · doi:10.1038/ijo.2017.228 · Cited by 135

Dnmt3a is an epigenetic mediator of adipose insulin resistance

You, D., Nilsson, E., Tenen, D. E., Lyubetskaya, A., Lo, J. C., Jiang, R., Deng, J., Dawes, B. A., Vaag, A. A., Ling, C., et al. (2017) · eLife · doi:10.7554/elife.30766 · Cited by 126

Gene-specific DNA methylation in newborns in response to folic acid supplementation during the second and third trimesters of pregnancy: epigenetic analysis from a randomized controlled trial

Caffrey, A., Irwin, R. E., McNulty, H., Strain, J. J., Lees‐Murdock, D. J., McNulty, B. A., Ward, M., Walsh, C. P., & Pentieva, K. D. (2018) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqx069 · Cited by 126

The inheritance of acquired epigenetic variations.

Jablonka, E., & Lamb, M. (2015) · International Journal of Epidemiology · doi:10.1093/ije/dyv020 · Cited by 123

Epigenetic changes in fetal hypothalamic energy regulating pathways are associated with maternal undernutrition and twinning

Begum, G., Stevens, A., Smith, E. B., Connor, K. L., Challis, J. R. G., Bloomfield, F. H., & White, A. E. (2012) · The FASEB Journal · doi:10.1096/fj.11-198762 · Cited by 121

Deletion of leptin signaling in vagal afferent neurons results in hyperphagia and obesity

de Lartigue, G., Ronveaux, C. C., & Raybould, H. E. (2014) · Molecular Metabolism · doi:10.1016/j.molmet.2014.06.003 · Cited by 120

Epigenetic signatures of gestational diabetes mellitus on cord blood methylation

Haertle, L., Hajj, N. E., Dittrich, M. T., Müller, T., Nanda, I., Lehnen, H., & Haaf, T. (2017) · Clinical Epigenetics · doi:10.1186/s13148-017-0329-3 · Cited by 119

Differential effects of maternal obesity and weight loss in the periconceptional period on the epigenetic regulation of hepatic insulin‐signaling pathways in the offspring

Nicholas, L. M., Rattanatray, L., MacLaughlin, S. M., Ozanne, S. E., Kleemann, D. O., Walker, S. K., Morrison, J. L., Zhang, S., Mühlhäusler, B. S., Martin‐Gronert, M. S., et al. (2013) · The FASEB Journal · doi:10.1096/fj.13-227918 · Cited by 115

Maternal obesity and gestational diabetes are associated with placental leptin DNA methylation

Lesseur, C., Armstrong, D. A., Paquette, A. G., Li, Z., Padbury, J. F., & Marsit, C. J. (2014) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2014.06.037 · Cited by 115

Impact of Maternal Obesity on Perinatal and Childhood Outcomes

Santangeli, L., Sattar, N. A., & Huda, S. S. (2014) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2014.10.009 · Cited by 114

Maternal diet–induced microRNAs and mTOR underlie β cell dysfunction in offspring

Alejandro, E. U., Gregg, B. E., Wallen, T. E., Kumusoglu, D., Meister, D. L., Chen, A., Merrins, M. J., Satin, L. S., Liu, M. R., Arvan, P., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci74237 · Cited by 114

The effects of paternal high-fat diet exposure on offspring metabolism with epigenetic changes in the mouse adiponectin and leptin gene promoters

Masuyama, H., Mitsui, T., Eguchi, T., Tamada, S., & Hiramatsu, Y. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00095.2016 · Cited by 114

Maternal high-fat diets cause insulin resistance through inflammatory changes in fetal adipose tissue

Murabayashi, N., Sugiyama, T., Zhang, L., Kamimoto, Y., Umekawa, T., Ma, N., & Sagawa, N. (2013) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2013.02.003 · Cited by 114

Downregulation of IRS-1 in adipose tissue of offspring of obese mice is programmed cell-autonomously through post-transcriptional mechanisms

Fernandez-Twinn, D. S., Alfaradhi, M. Z., Martin-Gronert, M. S., Duque-Guimaraes, D. E., Piekarz, A., Ferland-McCollough, D., Bushell, M., & Ozanne, S. E. (2014) · Molecular Metabolism · doi:10.1016/j.molmet.2014.01.007 · Cited by 114

Gestational Diabetes and Maternal Obesity Are Associated with Epigenome-Wide Methylation Changes in Children

Hjort, L., Martino, D., Grunnet, L. G., Naeem, H., Maksimovic, J., Olsson, A. H., Zhang, C., Ling, C., Olsen, S. F., Saffery, R., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.122572 · Cited by 114

Maternal obesity influences expression and DNA methylation of the adiponectin and leptin systems in human third-trimester placenta

Nogues, P., Santos, E. D., Jammes, H., Berveiller, P., Arnould, L., Vialard, F., & Dieudonné, M. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0612-6 · Cited by 114

Phthalate exposure in utero causes epigenetic changes and impairs insulin signalling

Parsanathan, R., & Balasubramanian, K. (2014) · Journal of Endocrinology · doi:10.1530/joe-14-0111 · Cited by 108

High-fructose diet in pregnancy leads to fetal programming of hypertension, insulin resistance, and obesity in adult offspring

Saad, A. F., Dickerson, J., Kechichian, T. B., Yin, H., Gamble, P., Salazar, A. E., Patrikeev, I., Motamedi, M., Saade, G. R., & Costantine, M. M. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.03.038 · Cited by 106

The histone demethylase Phf2 acts as a molecular checkpoint to prevent NAFLD progression during obesity

Bricambert, J., Alves‐Guerra, M., Estèves, P., Prip‐Buus, C., Bertrand‐Michel, J., Guillou, H., Chang, C. J., Wal, M. N. V., Canonne‐Hergaux, F., Mathurin, P., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04361-y · Cited by 106

DNA methylation of leptin and adiponectin promoters in children is reduced by the combined presence of obesity and insulin resistance

García-Cardona, M. C., Huang, F., García-Vivas, J. M., López‐Camarillo, C., Navarro, B. E. D. R., Navarro-Olivos, E., Hong‐Chong, E., Bolaños‐Jiménez, F., & Marchat, L. A. (2014) · International Journal of Obesity · doi:10.1038/ijo.2014.30 · Cited by 106

The Effects of High-Fat Diet Exposure in Utero on the Obesogenic and Diabetogenic Traits through Epigenetic Changes in Adiponectin and Leptin Gene Expression for Multiple Generations in Female Mice

Masuyama, H., Mitsui, T., Nobumoto, E., & Hiramatsu, Y. (2015) · Endocrinology · doi:10.1210/en.2014-2020 · Cited by 104

In utero exposure to a maternal high-fat diet alters the epigenetic histone code in a murine model

Suter, M., Ma, J., Vuguin, P. M., Hartil, K., Fiallo, A., Harris, R. A., Charron, M. J., & Aagaard, K. M. (2014) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2014.01.045 · Cited by 103

Extracellular RNAs Are Associated With Insulin Resistance and Metabolic Phenotypes

Shah, R. V., Murthy, V. L., Pacold, M. E., Danielson, K., Tanrıverdi, K., Larson, M. G., Hanspers, K., Pico, A. R., Mick, E. O., Reis, J. P., et al. (2017) · Diabetes Care · doi:10.2337/dc16-1354 · Cited by 103

Augmentation of histone deacetylase 3 (HDAC3) epigenetic signature at the interface of proinflammation and insulin resistance in patients with type 2 diabetes

Chandrakumar, S., Paramasivam, P., Balakumar, M., Lenin, R. R., Prabhu, D., Anjana, R. M., Mohan, V., & Balasubramanyam, M. (2016) · Clinical Epigenetics · doi:10.1186/s13148-016-0293-3 · Cited by 96

DNA methylation patterns in newborns exposed to tobacco in utero

Ivorra, C., Fraga, M. F., Bayón, G. F., Fernández, A. F., García-Vicent, C., Chaves, F. J., Redón, J., & Lurbe, E. (2015) · Journal of Translational Medicine · doi:10.1186/s12967-015-0384-5 · Cited by 93

Genome-wide DNA methylation pattern in visceral adipose tissue differentiates insulin-resistant from insulin-sensitive obese subjects

Crujeiras, A. B., Díaz‐Lagares, Á., Moreno‐Navarrete, J. M., Sandoval, J., Hervás, D., Gómez, A., Ricart, W., Casanueva, F. F., Esteller, M., & Fernández‐Real, J. M. (2016) · Translational research · doi:10.1016/j.trsl.2016.07.002 · Cited by 93

Decreased ovarian reserve, dysregulation of mitochondrial biogenesis, and increased lipid peroxidation in female mouse offspring exposed to an obesogenic maternal diet

Aiken, C., Tarry‐Adkins, J. L., Penfold, N., Dearden, L., & Ozanne, S. E. (2015) · The FASEB Journal · doi:10.1096/fj.15-280800 · Cited by 92

Metabolic Programming, Epigenetics, and Gestational Diabetes Mellitus

Pinney, S. E., & Simmons, R. A. (2011) · Current Diabetes Reports · doi:10.1007/s11892-011-0248-1 · Cited by 90

Developmental Programming by Maternal Insulin Resistance: Hyperinsulinemia, Glucose Intolerance, and Dysregulated Lipid Metabolism in Male Offspring of Insulin-Resistant Mice

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Exposure to the Chinese Famine in Childhood Increases Type 2 Diabetes Risk in Adults

Wang, J., Li, Y., Han, X., Liu, B., Hu, H., Wang, F., Li, X., YANG, K. Y., Yuan, J., Yao, P., et al. (2016) · Journal of Nutrition · doi:10.3945/jn.116.234575 · Cited by 89

Placental and Cord Blood Methylation of Genes Involved in Energy Homeostasis: Association With Fetal Growth and Neonatal Body Composition

Díaz, M., García-Beltrán, C., Sebastiani, G., de Zegher, F., López‐Bermejo, A., & Ibáñez, L. (2016) · Diabetes · doi:10.2337/db16-0776 · Cited by 89

Alteration in Expression and Methylation of IGF2/H19 in Placenta and Umbilical Cord Blood Are Associated with Macrosomia Exposed to Intrauterine Hyperglycemia

Su, R., Wang, C., Feng, H., Lin, L., Liu, X., Wei, Y., & Yang, H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148399 · Cited by 88

The epigenetic signature of systemic insulin resistance in obese women

Arner, P., Sahlqvist, A., Sinha, I., Xu, H. Y., Yao, X., Waterworth, D. M., Rajpal, D. K., Loomis, A. K., Freudenberg, J., Johnson, T., et al. (2016) · Diabetologia · doi:10.1007/s00125-016-4074-5 · Cited by 86

Differential methylation of genes in individuals exposed to maternal diabetes in utero

Chen, P., Piaggi, P., Traurig, M. T., Bogardus, C., Knowler, W. C., Baier, L. J., & Hanson, R. L. (2017) · Diabetologia · doi:10.1007/s00125-016-4203-1 · Cited by 86

Dynamics of genomic H3K27me3 domains and role of EZH2 during pancreatic endocrine specification

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Expression of epigenetic machinery genes is sensitive to maternal obesity and weight loss in relation to fetal growth in mice

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