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Review

Nutrigenetics, epigenetics and gestational diabetes: consequences in mother and child

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Pages 215-235 | Received 18 Oct 2018, Accepted 08 Feb 2019, Published online: 22 Mar 2019

References

  • Hernández-Aguilera A, Fernández-Arroyo S, Cuyàs E, et al. Epigenetics and nutrition-related epidemics of metabolic diseases: current perspectives and challenges. Food Chem Toxicol. 2016;96:191–204.
  • Katada S, Imhof A, Sassone-Corsi P. Connecting threads: epigenetics and metabolism. Cell. 2012;148:24–28.
  • van Dijk SJ, Tellam RL, Morrison JL, et al. Recent developments on the role of epigenetics in obesity and metabolic disease. Clin Epigenetics. 2015;7:66.
  • Lowe WL jr, Scholtens DM, Victoria S, et al. Genetics of gestational diabetes mellitus and maternal metabolism. Curr Diab Rep. 2016;16:15.
  • Karaderi T, Drong AW, Lindgren CM. Insights into the genetic susceptibility to type 2 diabetes from genome-wide association studies of obesity-related traits. Curr Diab Rep. 2015;15:83.
  • Wang X, Strizich G, Hu Y, et al. Qi Q Genetic markers of type 2 diabetes: progress in genome-wide association studies and clinical application for risk prediction. J Diabetes. 2016;8:24–35.
  • Ding M, Chavarro J, Olsen S, et al. Genetic variants of gestational diabetes mellitus: a study of 112 SNPs among 8722 women in two independent populations. Diabetologia. 2018;61:1758–1768.
  • Gluckman PD, Hanson MA, Beedle AS. Non-genomic transgenerational inheritance of disease risk. Bioessays. 2007;29:145–154.
  • Schwenk RW, Vogel H, Schürmann A. Genetic and epigenetic control of metabolic health. Mol Metab. 2013;2:337–347.
  • Christensen BC, Marsit CJ. Epigenomics in environmental health. Front Genet. 2011;2:84.
  • Boekelheide K, Blumberg B, Chapin RE, et al. Predicting later-life outcomes of early-life exposures. Environ Health Perspect. 2012;120:1353–1361.
  • Tobi EW, Slieker RC, Luijk R, et al.,, . DNA methylation as a mediator of the association between prenatal adversity and risk factors for metabolic disease in adulthood. Sci Adv. 2018;4:eaao4364.
  • Blackmore HL, Ozanne SE. Maternal diet-induced obesity and offspring cardiovascular health. J Dev Orig Health Dis. 2013;4:338–347.
  • Heindel JJ, Balbus J, Birnbaum L, et al. Developmental origins of health and disease: integrating environmental influences. Endocrinology. 2015;156:3416.
  • Nolan CJ, Damm P, Prentki M. Type 2 diabetes across generations: from pathophysiology to prevention and management. Lance. 2011;378:169–181.
  • Ma RC, Tutino GE, Lillycrop KA, et al. Maternal diabetes, gestational diabetes and the role of epigenetics in their long term effects on offspring. Prog Biophys Mol Biol. 2015;118:55–68.
  • Gagné-Ouellet V, Houde AA, Guay SP, et al. Placental lipoprotein lipase DNA methylation alterations are associated with gestational diabetes and body composition at 5 years of age. Epigenetics. 2017;12:616–625.
  • Godfrey KM, Reynolds RM, Prescott SL, et al. Influence of maternal obesity on the long-term health of offspring. Lancet Diabetes Endocrinol. 2017;5:53–64.
  • Agarwal P, Morriseau TS, Kereliuk SM, et al. Maternal obesity, diabetes during pregnancy and epigenetic mechanisms that influence the developmental origins of cardiometabolic disease in the offspring. Crit Rev Clin Lab Sci. 2018;55:71–101.
  • American Diabetes Association (ADA). Standards of medical care in diabetes- 2018”. Diabetes Care. 2018;41(Suppl 1):S13–S27.
  • Hod M, Kapur A, Sacks A, et al. The international Federation of Gynecology and Obstetrics (FIGO). Initiative on gestational diabetes mellitus: a pragmatic guide for diagnosis, management, and care. J Gynecol Obstet. 2015;131(Suppl 3):S173–211.
  • Rayanagoudar G, Hashi AA, Zamora J, et al. Quantification of the type 2 diabetes risk in women with gestational diabetes: a systematic review and meta-analysis of 95,750 women. Diabetologia. 2016;59:1403–1411.
  • Burlina S, Dalfrà MG, Lapolla A. Clinical and biochemical approach to predicting post-pregnancy metabolic decompensation. Diabetes Res Clin Pract. 2018;145:178–183. DOI:10.1016/j.diabres.2018.02.035
  • Metzger BE, the HAPO Study Cooperative Research Group. Hyperglycemia and Adverse Pregnancy Outcome (HAPO) study. Associations with neonatal anthropometrics. Diabetes. 2009;58:453–459.
  • Freinkel N. Banting Lecture 1980: of pregnancy and progeny. Diabetes. 1980;29:1023–1035.
  • Lowe WL Jr, Scholtens DM, Lowe LP, et al. Association of Gestational Diabetes With Maternal Disorders of Glucose Metabolism and Childhood Adiposity. JAMA. 2018;320(10):1005–1016.
  • Zhu Y, Zhang C. Prevalence of gestational diabetes and risk of progression to type 2 diabetes: a global perspective. Curr Diab Rep. 2016;16(1):7. . Review.
  • Plows JF, Stanley JL, Baker PN, et al. The pathophysiology of gestational diabetes mellitus. Int J Mol Sci. 2018;19(11):pii: E3342.
  • Zhang C, Ning Y. Effect of dietary and lifestyle factors on the risk of gestational diabetes: review of epidemiologic evidence. Am J Clin Nutr. 2011;94:1975S–1979S. Epub 2011 May 25.
  • Zhang C, Bao W, Rong Y, et al. Genetic variants and the risk of gestational diabetes mellitus: a systematic review. Hum Reprod Update. 2013;19:376–390.
  • Frayling TM. Genome-wide association studies provide new insights into type 2 diabetes aetiology. Nat Rev Genet. 2007;8:657–662.
  • McCarthy MI. Genomics, type 2 diabetes, and obesity. N Engl J Med. 2010;363:2339–2350.
  • Stover PJ, James WPT, Krook A, et al. Emerging concepts on the role of epigenetics in the relationships between nutrition and health. J Intern Med. 2018;284(1):37–49. . Epub 2018 May 23.
  • Simopoulos AP. Nutrigenetics/nutrigenomics. Annu Rev Public Health. 2010;31:53–68.
  • Phillips CM, Tierney AC, Roche HM. Gene-nutrient interactions in the metabolic syndrome. J Nutrigenet Nutrigenomics. 2008;1:136–151.
  • Roche HM, Phillips C, Gibney MJ. The metabolic syndrome: the crossroads of diet and genetics. Proc Nutr Soc. 2005;64:371–377.
  • Phillips C, Lopez-Miranda J, Perez-Jimenez F, et al. Genetic and nutrient determinants of the metabolic syndrome. Curr Opin Cardiol. 2006;21:185–193.
  • Moleres A, Ochoa MC, Rendo-Urteaga T, et al. Dietary fatty acid distribution modifies obesity risk linked to the rs9939609 polymorphism of the fat mass and obesity-associated gene in a Spanish case-control study of children. Br J Nutr. 2012;107:533–538.
  • Ortega-Azorín C, Sorlí JV, Asensio EM, et al. Associations of the FTO rs9939609 and the MC4R rs17782313 polymorphisms with type 2 diabetes are modulated by diet, being higher when adherence to the Mediterranean diet pattern is low. Cardiovasc Diabetol. 2012;11:137.
  • Luan J, Browne PO, Harding AH, et al. Evidence for gene-nutrient interaction at the PPARgamma locus. Diabetes. 2001;50(3):686–689.
  • Fisher E, Boeing H, Fritsche A, et al. Whole-grain consumption and transcription factor-7-like 2 (TCF7L2) rs7903146: gene-diet interaction in modulating type 2 diabetes risk. Br J Nutr. 2009;101:478–481.
  • Hindy G, Sonestedt E, Ericson U, et al. Role of TCF7L2 risk variant and dietary fibre intake on incident type 2 diabetes. Diabetologia. 2012;55:2646–2654.
  • Wirstrom T, Hilding A, Gu HF, et al. Consumption of whole grain reduces risk of deteriorating glucose tolerance, including progression to prediabetes. Am J Clin Nutr. 2013;97:179–187.
  • López-Ortiz MM, Garay-Sevilla ME, Tejero ME, et al. Analysis of the interaction between transcription factor 7-like 2 genetic variants with nopal and wholegrain fibre intake: effects on anthropometric and metabolic characteristics in type 2 diabetes patients. Br J Nutr. 2016;116(6):969–978. . Epub 2016 Aug 2.
  • Lai CQ, Corella D, Demissie S, et al. Dietary intake of n-6 fatty acids modulates effect of apolipoprotein A5 gene on plasma fasting triglycerides, remnant lipoprotein concentrations, and lipoprotein particle size: the Framingham Heart Study. Circulation. 2006;113(17): 2062–2070. Epub 2006 Apr 24.
  • Kang R, Kim M, Chae JS, et al. Consumption of whole grains and legumes modulates the genetic effect of the APOA5-1131C variant on changes in triglyceride and apolipoprotein A-V concentrations in patients with impaired fasting glucose or newly diagnosed type 2 diabetes. Trials. 2014;15:100.
  • Corella D, Lai CQ, Demissie S, et al. APOA5 gene variation modulates the effects of dietary fat intake on body mass index and obesity risk in the Framingham Heart Study. J Mol Med (Berl). 2007;85(2): 119–128. Epub 2007 Jan 9.
  • Franzago M, Fraticelli F, Nicolucci A, et al. Molecular analysis of a genetic variants panel related to nutrients and metabolism: association with susceptibility to gestational diabetes and cardiometabolic risk in affected women. J Diabetes Res. 2017:ID 4612623.DOI:10.1155/2017/4612623. Epub 2017 Jan 4.
  • Franzago M, Fraticelli F, Marchetti D, et al. Nutrigenetic variants and cardio-metabolic risk in women with or without gestational diabetes. Diabetes Res Clin Pract. 2018 8;137:64–71. Epub 2018 Jan 8.
  • Franzago M, Fraticelli F, Di Nicola M, et al. Early subclinical atherosclerosis in gestational diabetes: the predictive role of routine biomarkers and nutrigenetic variants. J Diabetes Res. 2018; 2018:9242579. DOI:10.1155/2018/9242579
  • Berná G, Oliveras-López MJ, Jurado-Ruíz E, et al. Nutrigenetics and nutrigenomics insights into diabetes etiopathogenesis. Nutrients. 2014;6:5338–5369.
  • Del Rosario MC, Ossowski V, Knowler WC, et al. Potential epigenetic dysregulation of genes associated with MODY and type 2 diabetes in humans exposed to a diabetic intrauterine environment: an analysis of genome-wide DNA methylation. Metabolism. 2014;63(5):654–660.
  • Chen P, Piaggi P, Traurig M, et al. Differential methylation of genes in individuals exposed to maternal diabetes in utero. Diabetologia. 2017;60(4):645–655.
  • Houshmand-Oeregaard A, Hjort L, Kelstrup L, et al. DNA methylation and gene expression of TXNIP in adult offspring of women with diabetes in pregnancy. PLoS One. 2017;12(10):e0187038.
  • Liyanage VR, Jarmasz JS, Murugeshan N, et al. DNA modifications: function and applications in normal and disease States. Biology (Basel). 2014;3:670–723.
  • Dolinoy DC, Weidman JR, Jirtle R. Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod Toxicol. 2007;23:297–307.
  • Auclair G, Weber M. Mechanisms of DNA methylation and demethylation in mammals. Biochimie. 2012;94:2202–2211.
  • Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693–705.
  • Lawrence M, Daujat S, Schneider R. Lateral thinking: how histone modifications regulate gene expression. Trends Genet. 2016;32:42–56.
  • Esguerra JLS, Mollet IG, Salunkhe VA, et al. Regulation of pancreatic beta cell stimulus-secretion coupling by microRNAs. Genes (Basel). 2014;5:1018–1031.
  • Wilczynska A, Bushell M. The complexity of miRNA-mediated repression. Cell Death Differ. 2015;22:22–33.
  • Kaspi H, Pasvolsky R, Hornstein E. Could microRNAs contribute to the maintenance of b cell identity? Trends Endocrinol Metab. 2014;25:285–292.
  • Ibarra A, Vega-Guedes B, Brito-Casillas Y, et al. Diabetes in pregnancy and MicroRNAs: promises and limitations in their clinical application. Noncoding RNA. 2018;4(4):pii: E32.
  • Guarino E, Delli Poggi C, Grieco GE, et al. Circulating MicroRNAs as biomarkers of gestational diabetes mellitus: updates and perspectives. Int J Endocrinol. 2018;2018:6380463.
  • Mochizuki K, Hariya N, Honma K, et al. Relationship between epigenetic regulation, dietary habits, and the developmental origins of health and disease theory. Congenit Anom (Kyoto). 2017;57:184–190.
  • Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992;35:595–601.
  • El Hajj N, Schneider E, Lehnen H, et al. Epigenetics and life-long consequences of an adverse nutritional and diabetic intrauterine environment. Reproduction. 2014;148:R111–R120.
  • Godfrey KM, Sheppard A, Gluckman PD, et al. Epigenetic gene promoter methylation at birth is associated with child’s later adiposity. Diabetes. 2011;60:1528–1534.
  • Davison JM, Mellott TJ, Kovacheva VP, et al. Gestational choline supply regulates methylation of histone H3, expression of histone methyltransferases G9a (Kmt1c) and Suv39h1 (Kmt1a), and DNA methylation of their genes in rat fetal liver and brain. J Biol Chem. 2009;284:1982–1989. Epub 2008 Nov 10.
  • Tosh DN, Fu Q, Callaway CW, et al. Epigenetics of programmed obesity: alteration in IUGR rat hepatic IGF1 mRNA expression and histone structure in rapid vs. delayed postnatal catch-up growth. Am J Physiol Gastrointest Liver Physiol. 2010;299:G1023–9.
  • Strakovsky RS, Zhang X, Zhou D, et al. Gestational high fat diet programs hepatic phosphoenolpyruvate carboxykinase gene expression and histone modification in neonatal offspring rats. J Physiol. 2011;589:2707–2717. Epub 2011 Mar 28.
  • Borengasser SJ, Zhong Y, Kang P, et al. Maternal obesity enhances white adipose tissue differentiation and alters genome-scale DNA methylation in male rat offspring. Endocrinology. 2013;154(11):4113–4125.
  • Zhang Y, Wang H, Zhou D, et al. High-fat diet caused widespread epigenomic differences on hepatic methylome in rat. Physiol Genomics. 2015;47(10):514–523.
  • Wankhade UD, Zhong Y, Kang P, et al. Enhanced offspring predisposition to steatohepatitis with maternal high-fat diet is associated with epigenetic and microbiome alterations. PLoS One. 2017;12(4):e0175675.
  • Moody L, Chen H, Pan YX. Postnatal diet remodels hepatic DNA methylation in metabolic pathways established by a maternal high-fat diet. Epigenomics. 2017;9(11):1387–1402.
  • Keleher MR, Zaidi R, Shah S, et al. Maternal high-fat diet associated with altered gene expression, DNA methylation, and obesity risk in mouse offspring. PLoS One. 2018;13(2):e0192606.
  • Khan I, Dekou V, Hanson M, et al. Predictive adaptive responses to maternal high-fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation. 2004;110:1097–1102.
  • Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science. 2004;305:1733–1736.
  • Gluckman PD, Hanson MA, Low FM. The role of developmental plasticity and epigenetics in human health. Birth Defects Res C Embryo Today. 2011;93:12–18.
  • Bateson P, Gluckman P, Hanson M. The biology of developmental plasticity and the predictive adaptive response hypothesis. J Physiol. 2014;592:2357–2368.
  • Gluckman PD, Hanson MA, Buklijas T. A conceptual framework for the developmental origins of health and disease. J Dev Orig Health Dis. 2010;1:6–18.
  • Roseboom TJ, van der Meulen JH, Ravelli AC, et al. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol. 2001;185:93–98.
  • Painter RC, Roseboom TJ, Bleker OP. Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol. 2005;20:345–352.
  • Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008;105:17046–17049.
  • Martin-Gronert MS, Ozanne SE. Mechanisms linking suboptimal early nutrition and increased risk of type 2 diabetes and obesity. J Nutr. 2010;140:662–666.
  • Seki Y, Williams L, Vuguin PM, et al. Minireview: epigenetic programming of diabetes and obesity: animal models. Endocrinology. 2012;153:1031–1038. Epub 2012 Jan 17.
  • Quilter CR, Cooper WN, Cliffe KM, et al. Impact on offspring methylation patterns of maternal gestational diabetes mellitus and intrauterine growth restraint suggest common genes and pathways linked to subsequent type 2 diabetes risk. FASEB J. 2014;28:4868–4879.
  • Wendland EM, Torloni MR, Falavigna M, et al. Gestational diabetes and pregnancy outcomes–a systematic review of the World Health Organization (WHO) and the International Association of Diabetes in Pregnancy Study Groups (IADPSG) diagnostic criteria. BMC Pregnancy Childbirth. 2012;12:23.
  • Block T, El-Osta A. Epigenetic programming, early life nutrition and the risk of metabolic disease. Atherosclerosis. 2017;266:31–40.
  • Boney CM, Verma A, Tucker R, et al. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics. 2005;115:e290–e296.
  • Dabelea D, Mayer-Davis EJ, Lamichhane AP, et al. Association of intrauterine exposure to maternal diabetes and obesity with type 2 diabetes in youth: the SEARCH case-control study. Diabetes Care. 2008;31:1422–1426. Epub 2008 Mar 28.
  • Nelissen EC, van Montfoort AP, Dumoulin JC, et al. Epigenetics and the placenta. Hum Reprod Update. 2011;17:397–417.
  • Jiang Y, Yu YC, Ding GL, et al. Intrauterine hyperglycemia induces intergenerational Dlk1-Gtl2 methylation changes in mouse placenta. Oncotarget. 2018;9:22398–22405.
  • Reichetzeder C, Dwi Putra SE, Pfab T, et al. Increased global placental DNA methylation levels are associated with gestational diabetes. Clin Epigenetics. 2016;8: 82. eCollection 2016.
  • Bouchard L, Thibault S, Guay SP, et al. Leptin gene epigenetic adaptation to impaired glucose metabolism during pregnancy. Diabetes Care. 2010;33:2436–2441.
  • Bouchard L, Hivert MF, Guay SP, et al. Placental adiponectin gene DNA methylation levels are associated with mothers’ blood glucose concentration. Diabetes. 2012;61:1272–1280. Epub 2012 Mar 6.
  • Houde AA, Guay SP, Desgagné V, et al. Adaptations of placental and cord blood ABCA1 DNA methylation profile to maternal metabolic status. Epigenetics. 2013;8(12):1289–1302. . Epub 2013 Oct 10.
  • Houde AA, St-Pierre J, Hivert MF, et al. Placental lipoprotein lipase DNA methylation levels are associated with gestational diabetes mellitus and maternal and cord blood lipid profiles. J Dev Orig Health Dis. 2014;5:132–141.
  • Houde AA, Ruchat SM, Allard C, et al. LRP1B, BRD2 and CACNA1D: new candidate genes in fetal metabolic programming of newborns exposed to maternal hyperglycemia. Epigenomics. 2015;7:1111–1122. Epub 2015 Nov 20.
  • Ruchat SM, Houde AA, Voisin G, et al. Gestational diabetes mellitus epigenetically affects genes predominantly involved in metabolic diseases. Epigenetics. 2013;8:935–943.
  • Desgagne V, Hivert MF, St-Pierre J, et al. Epigenetic dysregulation of the IGF system in placenta of newborns exposed to maternal impaired glucose tolerance. Epigenomics. 2014;6:193–207.
  • Petropoulos S, Guillemin C, Ergaz Z, et al. Gestational diabetes alters offspring DNA methylation profiles in human and rat: identification of key pathways involved in endocrine system disorders, insulin signaling, diabetes signaling, and ILK signaling. Endocrinology. 2015;156:2222–2238.
  • El Hajj N, Pliushch G, Schneider E, et al. Metabolic programming of MEST DNA methylation by intrauterine exposure to gestational diabetes mellitus. Diabetes. 2013;62:1320–1328. Epub 2012 Dec 3.
  • García-Cardona MC, Huang F, García-Vivas JM, et al. DNA methylation of leptin and adiponectin promoters in children is reduced by the combined presence of obesity and insulin resistance. Int J Obes (Lond). 2014;38:1457–1465.
  • Côté S, Gagné-Ouellet V, Guay SP, et al. PPARGC1α gene DNA methylation variations in human placenta mediate the link between maternal hyperglycemia and leptin levels in newborns. Clin Epigenetics. 2016;8:72. eCollection 2016.
  • Houshmand-Oeregaard A, Hansen NS, Hjort L, et al. Differential adipokine DNA methylation and gene expression in subcutaneous adipose tissue from adult offspring of women with diabetes in pregnancy. Clin Epigenetics. 2017;9:37. eCollection 2017.
  • Ott R, Stupin JH, Melchior K, et al. Plagemann A Alterations of adiponectin gene expression and DNA methylation in adipose tissues and blood cells are associated with gestational diabetes and neonatal outcome. Clin Epigenetics. 2018;10(1):131.
  • Ott R, Melchior K, Stupin JH, et al. Plagemann A insulin receptor expression and altered DNA methylation in fat tissues and blood of women with GDM and offspring. J Clin Endocrinol Metab. 2019;104(1):137–149.
  • Sebastiani G, Guarino E, Grieco GE, et al. Circulating microRNA (miRNA) expression profiling in plasma of patients with gestational diabetes mellitus reveals upregulation of miRNA miR-330-3p. Front Endocrinol (Lausanne). 2017;8:345. eCollection 2017.
  • Zhao C, Dong J, Jiang T, et al. Early second-trimester serum miRNA profiling predicts gestational diabetes mellitus. PLoS One. 2011;6(8):e23925. . Epub 2011 Aug 24.
  • Tagoma A, Alnek K, Kirss A, et al. MicroRNA profiling of second trimester maternal plasma shows upregulation of miR-195-5p in patients with gestational diabetes. Gene. 2018;672:137–142. Epub 2018 Jun 4.
  • Zhu Y, Tian F, Li H, et al. Profiling maternal plasma microRNA expression in early pregnancy to predict gestational diabetes mellitus. Int J Gynaecol Obstet. 2015;130:49–53.
  • Shi Z, Zhao C, Guo X, et al. Differential expression of microRNAs in omental adipose tissue from gestational diabetes mellitus subjects reveals miR-222 as a regulator of ERα expression in estrogen-induced insulin resistance. Endocrinology. 2014;155:1982–1990. Epub 2014 Mar 6.
  • Cao JL, Zhang L, Li J, et al. Up-regulation of miR-98 and unraveling regulatory mechanisms in gestational diabetes mellitus. Sci Rep. 2016;6:32268.
  • Houshmand-Oeregaard A, Schrölkamp M, Kelstrup L, et al. Increased expression of microRNA-15a and microRNA-15b in skeletal muscle from adult offspring of women with diabetes in pregnancy. Hum Mol Genet. 2018;27(10):1763–1771.
  • Ge ZJ, Luo SM, Lin F, et al. DNA methylation in oocytes and liver of female mice and their offspring: effects of high-fat-diet-induced obesity. Environ Health Perspect. 2014a;122:159–164. Epub 2013 Dec 6.
  • Wang Q, Tang SB, Song XB, et al. High-glucose concentrations change DNA methylation levels in human IVM oocytes. Hum Reprod. 2018;25. DOI:10.1093/humrep/dey006
  • Alegría-Torres JA, Baccarelli A, Bollati V. Epigenetics and lifestyle. Epigenomics. 2011;3:267–277.
  • Palma-Gudiel H, Cirera F, Crispi F, et al. The impact of prenatal insults on the human placental epigenome: A systematic review. Neurotoxicol Teratol. 2018;66:80–93.
  • Shah NR, Bracken MB. A systematic review and meta-analysis of prospective studies on the association between maternal cigarette smoking and preterm delivery. Am J Obstet Gynecol. 2000;182:465–472.
  • Breton C, Byun HM, Wenten M, et al. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am J Respir Crit Care Med. 2009;18:462–467. Epub 2009 Jun 4.
  • Fa S, Larsen TV, Bilde K, et al. Assessment of global DNA methylation in the first trimester fetal tissues exposed to maternal cigarette smoking. Clin Epigenetics. 2016;8:128. eCollection 2016.
  • Maccani JZJ, Koestler DC, Houseman EA, et al. Placental DNA methylation alterations associated with maternal tobacco smoking at the RUNX3 gene are also associated with gestational age. Epigenomics. 2013;5:619–630.
  • Maccani MA, Avissar-Whiting M, Banister CE, et al. Maternal cigarette smoking during pregnancy is associated with downregulation of miR-16, miR-21, and miR-146a in the placenta. Epigenetics. 2010 1;5:583–589. Epub 2010 Oct 1.
  • Zhou FC, Balaraman Y, Teng M, et al. Alcohol alters DNA methylation patterns and inhibits neural stem cell differentiation. Alcohol Clin Exp Res. 2011;35:735–746. Epub 2011 Jan 11.
  • Sharp GC, Arathimos R, Reese SE, et al.,, . Maternal alcohol consumption and offspring DNA methylation: findings from six general population-based birth cohorts. Epigenomics. 2018;10:27–42. . Epub 2017 Nov 27.
  • Laker RC, Lillard TS, Okutsu M, et al. Exercise prevents maternal high-fat diet-induced hypermethylation of the Pgc- 1alpha gene and age-dependent metabolic dysfunction in the offspring. Diabetes. 2014;63:1605–1611.
  • Chan JC, Nugent BM, Bale TL. Parental advisory: maternal and paternal stress can impact offspring neurodevelopment. Biol Psychiatry. 2018;83(10):886–894. . Epub 2017 Oct 13.
  • Kertes DA, Kamin HS, Hughes DA, et al. Prenatal maternal stress predicts methylation of genes regulating the hypothalamicpituitary- adrenocortical system in mothers and newborns in the Democratic Republic of Congo. Child Dev. 2016;87:61–72.
  • Kertes DA, Bhatt SS, Kamin HS, et al. BNDF methylation in mothers and newborns is associated with maternal exposure to war trauma. Clin Clin Epigenet. 2017;9:68.
  • Monk C, Feng T, Lee S, et al. Distress during pregnancy: epigenetic regulation of placenta glucocorticoid-related genes and fetal neurobehavior. Am J Psychiatry. 2016;173:705–713.
  • Palma-Gudiel H, Córdova-Palomera A, Eixarch E, et al. Maternal psychosocial stress during pregnancy alters the epigenetic signature of the glucocorticoid receptor gene promoter in their offspring: a meta-analysis. Epigenetics. 2015;10(10):893–902.
  • Miller C, Krishna S, Zhoumeng L, et al. Early sex differences in hepatic metabolic signaling in offspring of obese female mice. FASEB. 2014;28(Supplement 1033.11).
  • Mischke M, Pruis MGM, Boekschoten MV, et al. Maternal western-style high fat diet induces sex-specific physiological and molecular changes in two-week-old mouse offspring. PLoS ONE. 2013;8:e78623.
  • Bellisario V, Berry A, Capoccia S, et al. Gender-dependent resiliency to stressful and metabolic challenges following prenatal exposure to high-fat diet in the p66Shc −/− mouse. Front. Behav. Neurosci. 2014; 8: 285. PLoS ONE. 2013;8:e78623.
  • Gabory A, Ferry L, Fajardy I, et al. Maternal diets trigger sex-specific divergent trajectories of gene expression and epigenetic systems in mouse placenta. PLoS One. 2012;7(11):e47986.
  • Jaskolka D, Retnakaran R, Zinman B, et al. Sex of the baby and risk of gestational diabetes mellitus in the mother: a systematic review and meta-analysis. Diabetologia. 2015 Nov;58(11):2469–2475. .
  • Retnakaran R, Kramer CK, Ye C, et al. Fetal sex and maternal risk of gestational diabetes mellitus: the impact of having a boy. Diabetes Care. 2015 May;38(5):844–851. .
  • Retnakaran R, Shah BR. Sex of the baby and future maternal risk of Type 2 diabetes in women who had gestational diabetes. Diabet Med. 2016;33(7):956–960.
  • O’Neill K, Alexander J, Azuma R, et al. Gestational diabetes alters the metabolomic profile in 2nd trimester amniotic fluid in a sex-specific manner. Int J Mol Sci. 2018;19(9):pii: E2696.
  • Stuppia L, Franzago M, Ballerini P, et al. Epigenetics and male reproduction: the consequences of paternal lifestyle on fertility, embryo development, and children lifetime health. Clin Epigenetics. 2015;11(7):120. . eCollection 2015.
  • Champroux A, Cocquet J, Henry-Berger J, et al. A decade of exploring the mammalian sperm epigenome: paternal epigenetic and transgenerational inheritance. Front Cell Dev Biol. 2018;6:50. eCollection 2018.
  • Soubry A, Hoyo C, Jirtle RL, et al. A paternal environmental legacy: evidence for epigenetic inheritance through the male germ line. Bioessays. 2014;36:359–371. Epub 2014 Jan 16.
  • Soubry A. POHaD: why we should study future fathers. Environ Epigenet. 2018;4:dvy007. eCollection 2018 Apr.
  • Yajnik CS. Transmission of obesity-adiposity and related disorders from the mother to the baby. Ann Nutr Metab. 2014;64:8–17. Epub 2014 Jul 23.
  • Cortez RV, Taddei CR, Sparvoli LG, et al. Microbiome and its relation to gestational diabetes. Endocrine. 2018. DOI:10.1007/s12020-018-1813-z
  • Wang J, Zheng J, Shi W, et al. Dysbiosis of maternal and neonatal microbiota associated with gestational diabetes mellitus. Gut. 2018;67(9):1614–1625.