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Current Genomics

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ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

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Review Article

Maternal Obesity, Maternal Overnutrition and Fetal Programming: Effects of Epigenetic Mechanisms on the Development of Metabolic Disorders

Author(s): Ezgi Şanlı and Seray Kabaran*

Volume 20, Issue 6, 2019

Page: [419 - 427] Pages: 9

DOI: 10.2174/1389202920666191030092225

Price: $65

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Abstract

Background: Maternal obesity and maternal overnutrition, can lead to epigenetic alterations during pregnancy and these alterations can influence fetal and neonatal phenotype which increase the risk of metabolic disorders in later stages of life.

Objective: The effects of maternal obesity on fetal programming and potential mechanisms of maternal epigenetic regulation of gene expression which have persistent effects on fetal health and development were investigated.

Methods: Review of the literature was carried out in order to discuss the effects of maternal obesity and epigenetic mechanisms in fetal programming of metabolic disorders. All abstracts and full-text articles were examined and the most relevant articles were included in this review.

Results: Maternal obesity and maternal overnutrition during fetal period has important overall effects on long-term health. Maternal metabolic alterations during early stages of fetal development can lead to permanent changes in organ structures, cell numbers and metabolism. Epigenetic modifications (DNA methylation, histone modifications, microRNAs) play an important role in disease susceptibility in the later stages of human life. Maternal nutrition alter expression of hypothalamic genes which can increase fetal and neonatal energy intake. Epigenetic modifications may affect the increasing rate of obesity and other metabolic disorders worldwide since the impact of these changes can be passed through generations.

Conclusion: Weight management before and during pregnancy, together with healthy nutritional intakes may improve the maternal metabolic environment, which can reduce the risks of fetal programming of metabolic diseases. Further evidence from long-term follow-up studies are needed in order to determine the role of maternal obesity on epigenetic mechanisms.

Keywords: Maternal obesity, maternal nutrition, maternal overnutrition, fetal programming, epigenetic mechanisms, fetal metabolic disorders.

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[1]
Ng, M.; Fleming, T.; Robinson, M.; Thomson, B.; Graetz, N.; Margono, C.; Mullany, E.C.; Biryukov, S.; Abbafati, C.; Abera, S.F.; Abraham, J.P.; Abu-Rmeileh, N.M.; Achoki, T.; AlBuhairan, F.S.; Alemu, Z.A.; Alfonso, R.; Ali, M.K.; Ali, R.; Guzman, N.A.; Ammar, W.; Anwari, P.; Banerjee, A.; Barquera, S.; Basu, S.; Bennett, D.A.; Bhutta, Z.; Blore, J.; Cabral, N.; Nonato, I.C.; Chang, J.C.; Chowdhury, R.; Courville, K.J.; Criqui, M.H.; Cundiff, D.K.; Dabhadkar, K.C.; Dandona, L.; Davis, A.; Dayama, A.; Dharmaratne, S.D.; Ding, E.L.; Durrani, A.M.; Esteghamati, A.; Farzadfar, F.; Fay, D.F.; Feigin, V.L.; Flaxman, A.; Forouzanfar, M.H.; Goto, A.; Green, M.A.; Gupta, R.; Hafezi-Nejad, N.; Hankey, G.J.; Harewood, H.C.; Havmoeller, R.; Hay, S.; Hernandez, L.; Husseini, A.; Idrisov, B.T.; Ikeda, N.; Islami, F.; Jahangir, E.; Jassal, S.K.; Jee, S.H.; Jeffreys, M.; Jonas, J.B.; Kabagambe, E.K.; Khalifa, S.E.; Kengne, A.P.; Khader, Y.S.; Khang, Y.H.; Kim, D.; Kimokoti, R.W.; Kinge, J.M.; Kokubo, Y.; Kosen, S.; Kwan, G.; Lai, T.; Leinsalu, M.; Li, Y.; Liang, X.; Liu, S.; Logroscino, G.; Lotufo, P.A.; Lu, Y.; Ma, J.; Mainoo, N.K.; Mensah, G.A.; Merriman, T.R.; Mokdad, A.H.; Moschandreas, J.; Naghavi, M.; Naheed, A.; Nand, D.; Narayan, K.M.; Nelson, E.L.; Neuhouser, M.L.; Nisar, M.I.; Ohkubo, T.; Oti, S.O.; Pedroza, A.; Prabhakaran, D.; Roy, N.; Sampson, U.; Seo, H.; Sepanlou, S.G.; Shibuya, K.; Shiri, R.; Shiue, I.; Singh, G.M.; Singh, J.A.; Skirbekk, V.; Stapelberg, N.J.; Sturua, L.; Sykes, B.L.; Tobias, M.; Tran, B.X.; Trasande, L.; Toyoshima, H.; van de Vijver, S.; Vasankari, T.J.; Veerman, J.L.; Velasquez-Melendez, G.; Vlassov, V.V.; Vollset, S.E.; Vos, T.; Wang, C.; Wang, X.; Weiderpass, E.; Werdecker, A.; Wright, J.L.; Yang, Y.C.; Yatsuya, H.; Yoon, J.; Yoon, S.J.; Zhao, Y.; Zhou, M.; Zhu, S.; Lopez, A.D.; Murray, C.J.; Gakidou, E. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: A systematic analysis for the Global Burden of Disease Study 2013. Lancet, 2014, 384(9945), 766-781.
[http://dx.doi.org/10.1016/S0140-6736(14)60460-8] [PMID: 24880830]
[2]
Gaillard, R.; Durmuş, B.; Hofman, A.; Mackenbach, J.P.; Steegers, E.A.; Jaddoe, V.W. Risk factors and outcomes of maternal obesity and excessive weight gain during pregnancy. Obesity (Silver Spring), 2013, 21(5), 1046-1055.
[http://dx.doi.org/10.1002/oby.20088] [PMID: 23784909]
[3]
Valsamakis, G.; Kyriazi, E.L.; Mouslech, Z.; Siristatidis, C.; Mastorakos, G. Effect of maternal obesity on pregnancy outcomes and long-term metabolic consequences. Hormones (Athens), 2015, 14(3), 345-357.
[http://dx.doi.org/10.14310/horm.2002.1590] [PMID: 26188222]
[4]
Bouret, S.G. Role of early hormonal and nutritional experiences in shaping feeding behavior and hypothalamic development. J. Nutr., 2010, 140(3), 653-657.
[http://dx.doi.org/10.3945/jn.109.112433] [PMID: 20107150]
[5]
Plagemann, A.; Harder, T.; Schellong, K.; Schulz, S.; Stupin, J.H. Early postnatal life as a critical time window for determination of long-term metabolic health. Best Pract. Res. Clin. Endocrinol. Metab., 2012, 26(5), 641-653.
[http://dx.doi.org/10.1016/j.beem.2012.03.008] [PMID: 22980046]
[6]
Gicquel, C.; El-Osta, A.; Le Bouc, Y. Epigenetic regulation and fetal programming. Best Pract. Res. Clin. Endocrinol. Metab., 2008, 22(1), 1-16.
[http://dx.doi.org/10.1016/j.beem.2007.07.009] [PMID: 18279777]
[7]
Waterland, R.A.; Jirtle, R.L. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition, 2004, 20(1), 63-68.
[http://dx.doi.org/10.1016/j.nut.2003.09.011] [PMID: 14698016]
[8]
Nicholas, L.M.; Morrison, J.L.; Rattanatray, L.; Zhang, S.; Ozanne, S.E.; McMillen, I.C. The early origins of obesity and insulin resistance: Timing, programming and mechanisms. Int. J. Obes., 2016, 40(2), 229-238.
[http://dx.doi.org/10.1038/ijo.2015.178] [PMID: 26367335]
[9]
Kitsiou-Tzeli, S.; Tzetis, M. Maternal epigenetics and fetal and neonatal growth. Curr. Opin. Endocrinol. Diabetes Obes., 2017, 24(1), 43-46.
[PMID: 27898587]
[10]
Desai, M.; Jellyman, J.K.; Ross, M.G. Epigenomics, gestational programming and risk of metabolic syndrome. Int. J. Obes., 2015, 39(4), 633-641.
[http://dx.doi.org/10.1038/ijo.2015.13] [PMID: 25640766]
[11]
Elshenawy, S.; Simmons, R. Maternal obesity and prenatal programming. Mol. Cell. Endocrinol., 2016, 435, 2-6.
[http://dx.doi.org/10.1016/j.mce.2016.07.002] [PMID: 27392495]
[12]
Nicholas, L.M.; Morrison, J.L.; Rattanatray, L.; Zhang, S.; Ozanne, S.E.; McMillen, I.C. The early origins of obesity and insulin resistance: Timing, programming and mechanisms. Int. J. Obes., 2016, 40(2), 229-238.
[http://dx.doi.org/10.1038/ijo.2015.178] [PMID: 26367335]
[13]
Montalvo-Martínez, L.; Maldonado-Ruiz, R.; Cárdenas-Tueme, M.; Reséndez-Pérez, D.; Camacho, A. Maternal overnutrition programs central inflammation and addiction-like behavior in offspring. BioMed Res. Int., 2018, 20188061389
[http://dx.doi.org/10.1155/2018/8061389] [PMID: 30027100]
[14]
Maffeis, C.; Morandi, A. Effect of maternal obesity on foetal growth and metabolic health of the offspring. Obes. Facts, 2017, 10(2), 112-117.
[http://dx.doi.org/10.1159/000456668] [PMID: 28384625]
[15]
Padmanabhan, V.; Cardoso, R.C.; Puttabyatappa, M. Developmental programming, a pathway to disease. Endocrinology, 2016, 157(4), 1328-1340.
[http://dx.doi.org/10.1210/en.2016-1003] [PMID: 26859334]
[16]
Alfaradhi, M.Z.; Ozanne, S.E. Developmental programming in response to maternal overnutrition. Front. Genet., 2011, 2, 27.
[http://dx.doi.org/10.3389/fgene.2011.00027] [PMID: 22303323]
[17]
Fernandez-Twinn, D.S.; Constância, M.; Ozanne, S.E. Intergenerational epigenetic inheritance in models of developmental programming of adult disease. Semin. Cell Dev. Biol., 2015, 43, 85-95.
[http://dx.doi.org/10.1016/j.semcdb.2015.06.006] [PMID: 26135290]
[18]
Fernandez-Twinn, D.S.; Ozanne, S.E. Early life nutrition and metabolic programming. Ann. N. Y. Acad. Sci., 2010, 1212(1), 78-96.
[http://dx.doi.org/10.1111/j.1749-6632.2010.05798.x] [PMID: 21070247]
[19]
Roseboom, T.; de Rooij, S.; Painter, R. The Dutch famine and its long-term consequences for adult health. Early Hum. Dev., 2006, 82(8), 485-491.
[http://dx.doi.org/10.1016/j.earlhumdev.2006.07.001] [PMID: 16876341]
[20]
Barker, D.J.; Osmond, C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet, 1986, 1(8489), 1077-1081.
[http://dx.doi.org/10.1016/S0140-6736(86)91340-1] [PMID: 2871345]
[21]
Barker, D.J. The fetal origins of coronary heart disease. Acta Paediatr. Suppl., 1997, 422(S422), 78-82.
[http://dx.doi.org/10.1111/j.1651-2227.1997.tb18351.x] [PMID: 9298799]
[22]
Barker, D.J. The developmental origins of chronic adult disease. Acta Paediatr. Suppl., 2004, 93(446), 26-33.
[http://dx.doi.org/10.1111/j.1651-2227.2004.tb00236.x] [PMID: 15702667]
[23]
Stephenson, S.; Cunliffe, A. Foetal developmental origins of adult onset non-insulin dependent diabetes mellitus. J. Nutr. Food Sci., 2018, 8(5), 1-11.
[http://dx.doi.org/10.4172/2155-9600.1000733]
[24]
Ravelli, A.C.; van der Meulen, J.H.; Michels, R.P.J.; Osmond, C.; Barker, D.J.; Hales, C.N.; Bleker, O.P. Glucose tolerance in adults after prenatal exposure to famine. Lancet, 1998, 351(9097), 173-177.
[http://dx.doi.org/10.1016/S0140-6736(97)07244-9] [PMID: 9449872]
[25]
Hales, C.N.; Barker, D.J. The thrifty phenotype hypothesis. Br. Med. Bull., 2001, 60(1), 5-20.
[http://dx.doi.org/10.1093/bmb/60.1.5] [PMID: 11809615]
[26]
Wells, J.C. The thrifty phenotype hypothesis: Thrifty offspring or thrifty mother? J. Theor. Biol., 2003, 221(1), 143-161.
[http://dx.doi.org/10.1006/jtbi.2003.3183] [PMID: 12634051]
[27]
Armitage, J.A.; Poston, L.; Taylor, P.D. Developmental origins of obesity and the metabolic syndrome: The role of maternal obesity. Front. Horm. Res., 2008, 36, 73-84.
[http://dx.doi.org/10.1159/000115355] [PMID: 18230895]
[28]
Smith, N.H.; Ozanne, S.E. Intrauterine origins of metabolic disease. Rev. Gynaecol. Perinatal Practice, 2006, 6(3-4), 211-217.
[http://dx.doi.org/10.1016/j.rigapp.2006.03.002]
[29]
Luo, Z.C.; Fraser, W.D.; Julien, P.; Deal, C.L.; Audibert, F.; Smith, G.N.; Xiong, X.; Walker, M. Tracing the origins of “fetal origins” of adult diseases: Programming by oxidative stress? Med. Hypotheses, 2006, 66(1), 38-44.
[http://dx.doi.org/10.1016/j.mehy.2005.08.020] [PMID: 16198060]
[30]
Catalano, P.M.; Shankar, K. Obesity and pregnancy: Mechanisms of short term and long term adverse consequences for mother and child. BMJ, 2017, 356, j1.
[http://dx.doi.org/10.1136/bmj.j1] [PMID: 28179267]
[31]
McDowell, M.; Cain, M.A.; Brumley, J. Excessive gestational weight gain. J. Midwifery Womens Health, 2018, 1-9.
[32]
Goldstein, R.F.; Abell, S.K.; Ranasinha, S.; Misso, M.; Boyle, J.A.; Black, M.H.; Li, N.; Hu, G.; Corrado, F.; Rode, L.; Kim, Y.J.; Haugen, M.; Song, W.O.; Kim, M.H.; Bogaerts, A.; Devlieger, R.; Chung, J.H.; Teede, H.J. Association of gestational weight gain with maternal and infant outcomes: A systematic review and meta-analysis. JAMA, 2017, 317(21), 2207-2225.
[http://dx.doi.org/10.1001/jama.2017.3635] [PMID: 28586887]
[33]
Yu, Z.; Han, S.; Zhu, J.; Sun, X.; Ji, C.; Guo, X. Pre-pregnancy body mass index in relation to infant birth weight and offspring overweight/obesity: A systematic review and meta-analysis. PLoS One, 2013, 8(4)e61627
[http://dx.doi.org/10.1371/journal.pone.0061627] [PMID: 23613888]
[34]
Tie, H.T.; Xia, Y.Y.; Zeng, Y.S.; Zhang, Y.; Dai, C.L.; Guo, J.J.; Zhao, Y. Risk of childhood overweight or obesity associated with excessive weight gain during pregnancy: A meta-analysis. Arch. Gynecol. Obstet., 2014, 289(2), 247-257.
[http://dx.doi.org/10.1007/s00404-013-3053-z] [PMID: 24141389]
[35]
Voerman, E.; Santos, S.; Patro Golab, B.; Amiano, P.; Ballester, F.; Barros, H.; Bergström, A.; Charles, M.A.; Chatzi, L.; Chevrier, C.; Chrousos, G.P.; Corpeleijn, E.; Costet, N.; Crozier, S.; Devereux, G.; Eggesbø, M.; Ekström, S.; Fantini, M.P.; Farchi, S.; Forastiere, F.; Georgiu, V.; Godfrey, K.M.; Gori, D.; Grote, V.; Hanke, W.; Hertz-Picciotto, I.; Heude, B.; Hryhorczuk, D.; Huang, R.C.; Inskip, H.; Iszatt, N.; Karvonen, A.M.; Kenny, L.C.; Koletzko, B.; Küpers, L.K.; Lagström, H.; Lehmann, I.; Magnus, P.; Majewska, R.; Mäkelä, J.; Manios, Y.; McAuliffe, F.M.; McDonald, S.W.; Mehegan, J.; Mommers, M.; Morgen, C.S.; Mori, T.A.; Moschonis, G.; Murray, D.; Chaoimh, C.N.; Nohr, E.A.; Nybo Andersen, A.M.; Oken, E.; Oostvogels, A.J.J.M.; Pac, A.; Papadopoulou, E.; Pekkanen, J.; Pizzi, C.; Polanska, K.; Porta, D.; Richiardi, L.; Rifas-Shiman, S.L.; Ronfani, L.; Santos, A.C.; Standl, M.; Stoltenberg, C.; Thiering, E.; Thijs, C.; Torrent, M.; Tough, S.C.; Trnovec, T.; Turner, S.; van Rossem, L.; von Berg, A.; Vrijheid, M.; Vrijkotte, T.G.M.; West, J.; Wijga, A.; Wright, J.; Zvinchuk, O.; Sørensen, T.I.A.; Lawlor, D.A.; Gaillard, R.; Jaddoe, V.W.V. Maternal body mass index, gestational weight gain, and the risk of overweight and obesity across childhood: An individual participant data meta-analysis. PLoS Med., 2019, 16(2)e1002744
[http://dx.doi.org/10.1371/journal.pmed.1002744] [PMID: 30742624]
[36]
Muhlhausler, B.S.; Ong, Z.Y. The fetal origins of obesity: Early origins of altered food intake. Endocr. Metab. Immune Disord. Drug Targets, 2011, 11(3), 189-197.
[http://dx.doi.org/10.2174/187153011796429835] [PMID: 21831032]
[37]
Tarrade, A.; Panchenko, P.; Junien, C.; Gabory, A. Placental contribution to nutritional programming of health and diseases: Epigenetics and sexual dimorphism. J. Exp. Biol., 2015, 218(Pt 1), 50-58.
[http://dx.doi.org/10.1242/jeb.110320] [PMID: 25568451]
[38]
Muhlhausler, B.S.; Adam, C.L.; Findlay, P.A.; Duffield, J.A.; McMillen, I.C. Increased maternal nutrition alters development of the appetite-regulating network in the brain. FASEB J., 2006, 20(8), 1257-1259.
[http://dx.doi.org/10.1096/fj.05-5241fje] [PMID: 16684802]
[39]
Brion, M.J.; Ness, A.R.; Rogers, I.; Emmett, P.; Cribb, V.; Davey Smith, G.; Lawlor, D.A. Maternal macronutrient and energy intakes in pregnancy and offspring intake at 10 y: Exploring parental comparisons and prenatal effects. Am. J. Clin. Nutr., 2010, 91(3), 748-756.
[http://dx.doi.org/10.3945/ajcn.2009.28623] [PMID: 20053880]
[40]
Lawlor, D.A.; Smith, G.D.; O’Callaghan, M.; Alati, R.; Mamun, A.A.; Williams, G.M.; Najman, J.M. Epidemiologic evidence for the fetal overnutrition hypothesis: Findings from the mater-university study of pregnancy and its outcomes. Am. J. Epidemiol., 2007, 165(4), 418-424.
[http://dx.doi.org/10.1093/aje/kwk030] [PMID: 17158475]
[41]
Williams, L.; Seki, Y.; Vuguin, P.M.; Charron, M.J. Animal models of in utero exposure to a high fat diet: A review. Biochimica et Biophysica Acta (BBA)-. Molecular Basis of Disease, 2014, 1842(3), 507-519.
[http://dx.doi.org/10.1016/j.bbadis.2013.07.006]
[42]
Fu, G.; Brkić, J.; Hayder, H.; Peng, C. MicroRNAs in human placental development and pregnancy complications. Int. J. Mol. Sci., 2013, 14(3), 5519-5544.
[http://dx.doi.org/10.3390/ijms14035519] [PMID: 23528856]
[43]
Nugent, B.M.; Bale, T.L. The omniscient placenta: Metabolic and epigenetic regulation of fetal programming. Front. Neuroendocrinol., 2015, 39, 28-37.
[http://dx.doi.org/10.1016/j.yfrne.2015.09.001] [PMID: 26368654]
[44]
Upadhyay, A.; Anjum, B.; Godbole, N.M.; Rajak, S.; Shukla, P.; Tiwari, S.; Sinha, R.A.; Godbole, M.M. Time-restricted feeding reduces high-fat diet associated placental inflammation and limits adverse effects on fetal organ development. Biochem. Biophys. Res. Commun., 2019, 514(2), 415-421.
[http://dx.doi.org/10.1016/j.bbrc.2019.04.154] [PMID: 31053302]
[45]
Heerwagen, M.J.; Miller, M.R.; Barbour, L.A.; Friedman, J.E. Maternal obesity and fetal metabolic programming: A fertile epigenetic soil. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2010, 299(3), R711-R722.
[http://dx.doi.org/10.1152/ajpregu.00310.2010] [PMID: 20631295]
[46]
McCurdy, C.E.; Bishop, J.M.; Williams, S.M.; Grayson, B.E.; Smith, M.S.; Friedman, J.E.; Grove, K.L. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J. Clin. Invest., 2009, 119(2), 323-335.
[http://dx.doi.org/10.1172/JCI32661] [PMID: 19147984]
[47]
Tarrade, A.; Panchenko, P.; Junien, C.; Gabory, A. Placental contribution to nutritional programming of health and diseases: Epigenetics and sexual dimorphism. J. Exp. Biol., 2015, 218(Pt 1), 50-58.
[http://dx.doi.org/10.1242/jeb.110320] [PMID: 25568451]
[48]
Murabayashi, N.; Sugiyama, T.; Zhang, L.; Kamimoto, Y.; Umekawa, T.; Ma, N.; Sagawa, N. Maternal high-fat diets cause insulin resistance through inflammatory changes in fetal adipose tissue. Eur. J. Obstet. Gynecol. Reprod. Biol., 2013, 169(1), 39-44.
[http://dx.doi.org/10.1016/j.ejogrb.2013.02.003] [PMID: 23453296]
[49]
Alfaradhi, M.Z.; Ozanne, S.E. Developmental programming in response to maternal overnutrition. Front. Genet., 2011, 2, 27.
[http://dx.doi.org/10.3389/fgene.2011.00027] [PMID: 22303323]
[50]
Jang, H.; Serra, C. Nutrition, epigenetics, and diseases. Clin. Nutr. Res., 2014, 3(1), 1-8.
[http://dx.doi.org/10.7762/cnr.2014.3.1.1] [PMID: 24527414]
[51]
Chango, A.; Pogribny, I.P. Considering maternal dietary modulators for epigenetic regulation and programming of the fetal epigenome. Nutrients, 2015, 7(4), 2748-2770.
[http://dx.doi.org/10.3390/nu7042748] [PMID: 25875118]
[52]
Cheng, Z.; Zheng, L.; Almeida, F.A. Epigenetic reprogramming in metabolic disorders: Nutritional factors and beyond. J. Nutr. Biochem., 2018, 54, 1-10.
[http://dx.doi.org/10.1016/j.jnutbio.2017.10.004] [PMID: 29154162]
[53]
Freeman, D.J. Effects of maternal obesity on fetal growth and body composition: Implications for programming and future health. Semin. Fetal Neonatal Med., 2010, 15(2), 113-118.
[http://dx.doi.org/10.1016/j.siny.2009.09.001] [PMID: 19853544]
[54]
Sen, S.; Carpenter, A.H.; Hochstadt, J.; Huddleston, J.Y.; Kustanovich, V.; Reynolds, A.A.; Roberts, S. Nutrition, weight gain and eating behavior in pregnancy: A review of experimental evidence for long-term effects on the risk of obesity in offspring. Physiol. Behav., 2012, 107(1), 138-145.
[http://dx.doi.org/10.1016/j.physbeh.2012.04.014] [PMID: 22546810]
[55]
McMillen, I.C.; Robinson, J.S. Developmental origins of the metabolic syndrome: Prediction, plasticity, and programming. Physiol. Rev., 2005, 85(2), 571-633.
[http://dx.doi.org/10.1152/physrev.00053.2003] [PMID: 15788706]
[56]
Muhlhausler, B.S.; Duffield, J.A.; McMillen, I.C. Increased maternal nutrition stimulates peroxisome proliferator activated receptor-γ, adiponectin, and leptin messenger ribonucleic acid expression in adipose tissue before birth. Endocrinology, 2007, 148(2), 878-885.
[http://dx.doi.org/10.1210/en.2006-1115] [PMID: 17068138]
[57]
MacLennan, N.K.; James, S.J.; Melnyk, S.; Piroozi, A.; Jernigan, S.; Hsu, J.L.; Janke, S.M.; Pham, T.D.; Lane, R.H. Uteroplacental insufficiency alters DNA methylation, one-carbon metabolism, and histone acetylation in IUGR rats. Physiol. Genomics, 2004, 18(1), 43-50.
[http://dx.doi.org/10.1152/physiolgenomics.00042.2004] [PMID: 15084713]
[58]
Panchenko, P.E.; Voisin, S.; Jouin, M.; Jouneau, L.; Prézelin, A.; Lecoutre, S.; Breton, C.; Jammes, H.; Junien, C.; Gabory, A. Expression of epigenetic machinery genes is sensitive to maternal obesity and weight loss in relation to fetal growth in mice. Clin. Epigenetics, 2016, 8(1), 22.
[http://dx.doi.org/10.1186/s13148-016-0188-3] [PMID: 26925174]
[59]
Borengasser, S.J.; Zhong, Y.; Kang, P.; Lindsey, F.; Ronis, M.J.; Badger, T.M.; Gomez-Acevedo, H.; Shankar, K. Maternal obesity enhances white adipose tissue differentiation and alters genome-scale DNA methylation in male rat offspring. Endocrinology, 2013, 154(11), 4113-4125.
[http://dx.doi.org/10.1210/en.2012-2255] [PMID: 23959936]
[60]
Vucetic, Z.; Kimmel, J.; Totoki, K.; Hollenbeck, E.; Reyes, T.M. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology, 2010, 151(10), 4756-4764.
[http://dx.doi.org/10.1210/en.2010-0505] [PMID: 20685869]
[61]
Godfrey, K.M.; Sheppard, A.; Gluckman, P.D.; Lillycrop, K.A.; Burdge, G.C.; McLean, C.; Rodford, J.; Slater-Jefferies, J.L.; Garratt, E.; Crozier, S.R.; Emerald, B.S.; Gale, C.R.; Inskip, H.M.; Cooper, C.; Hanson, M.A. Epigenetic gene promoter methylation at birth is associated with child’s later adiposity. Diabetes, 2011, 60(5), 1528-1534.
[http://dx.doi.org/10.2337/db10-0979] [PMID: 21471513]
[62]
Gali Ramamoorthy, T.; Allen, T.J.; Davies, A.; Harno, E.; Sefton, C.; Murgatroyd, C.; White, A. Maternal overnutrition programs epigenetic changes in the regulatory regions of hypothalamic Pomc in the offspring of rats. Int. J. Obes., 2018, 42(8), 1431-1444.
[http://dx.doi.org/10.1038/s41366-018-0094-1] [PMID: 29777232]
[63]
Chen, H.; Simar, D.; Lambert, K.; Mercier, J.; Morris, M.J. Maternal and postnatal overnutrition differentially impact appetite regulators and fuel metabolism. Endocrinology, 2008, 149(11), 5348-5356.
[http://dx.doi.org/10.1210/en.2008-0582] [PMID: 18635655]
[64]
Plagemann, A.; Harder, T.; Brunn, M.; Harder, A.; Roepke, K.; Wittrock-Staar, M.; Ziska, T.; Schellong, K.; Rodekamp, E.; Melchior, K.; Dudenhausen, J.W. Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: An epigenetic model of obesity and the metabolic syndrome. J. Physiol., 2009, 587(Pt 20), 4963-4976.
[http://dx.doi.org/10.1113/jphysiol.2009.176156] [PMID: 19723777]
[65]
Gluckman, P.D.; Hanson, M.A. Developmental and epigenetic pathways to obesity: An evolutionary-developmental perspective. Int. J. Obes., 2008, 32(Suppl. 7), S62-S71.
[http://dx.doi.org/10.1038/ijo.2008.240] [PMID: 19136993]
[66]
Sasson, I.E.; Vitins, A.P.; Mainigi, M.A.; Moley, K.H.; Simmons, R.A. Pre-gestational vs gestational exposure to maternal obesity differentially programs the offspring in mice. Diabetologia, 2015, 58(3), 615-624.
[http://dx.doi.org/10.1007/s00125-014-3466-7] [PMID: 25608625]
[67]
Lecoutre, S.; Oger, F.; Pourpe, C.; Butruille, L.; Marousez, L.; Dickes-Coopman, A.; Laborie, C.; Guinez, C.; Lesage, J.; Vieau, D.; Junien, C.; Eberlé, D.; Gabory, A.; Eeckhoute, J.; Breton, C. Maternal obesity programs increased leptin gene expression in rat male offspring via epigenetic modifications in a depot-specific manner. Mol. Metab., 2017, 6(8), 922-930.
[http://dx.doi.org/10.1016/j.molmet.2017.05.010] [PMID: 28752055]
[68]
Shankar, K.; Harrell, A.; Liu, X.; Gilchrist, J.M.; Ronis, M.J.; Badger, T.M. Maternal obesity at conception programs obesity in the offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2008, 294(2), R528-R538.
[http://dx.doi.org/10.1152/ajpregu.00316.2007] [PMID: 18032473]
[69]
Seki, Y.; Suzuki, M.; Guo, X.; Glenn, A.S.; Vuguin, P.M.; Fiallo, A.; Du, Q.; Ko, Y.A.; Yu, Y.; Susztak, K.; Zheng, D.; Greally, J.M.; Katz, E.B.; Charron, M.J. In utero exposure to a high-fat diet programs hepatic hypermethylation and gene dysregulation and development of metabolic syndrome in male mice. Endocrinology, 2017, 158(9), 2860-2872.
[http://dx.doi.org/10.1210/en.2017-00334] [PMID: 28911167]
[70]
Unal, R.; Yao-Borengasser, A.; Varma, V.; Rasouli, N.; Labbate, C.; Kern, P.A.; Ranganathan, G. Matrix metalloproteinase-9 is increased in obese subjects and decreases in response to pioglitazone. J. Clin. Endocrinol. Metab., 2010, 95(6), 2993-3001.
[http://dx.doi.org/10.1210/jc.2009-2623] [PMID: 20392866]
[71]
Cheng, X.; Blumenthal, R.M. Coordinated chromatin control: Structural and functional linkage of DNA and histone methylation. Biochemistry, 2010, 49(14), 2999-3008.
[http://dx.doi.org/10.1021/bi100213t] [PMID: 20210320]
[72]
Kouzarides, T. Chromatin modifications and their function. Cell, 2007, 128(4), 693-705.
[http://dx.doi.org/10.1016/j.cell.2007.02.005] [PMID: 17320507]
[73]
Dolinoy, D.C.; Das, R.; Weidman, J.R.; Jirtle, R.L. Metastable epialleles, imprinting, and the fetal origins of adult diseases. Pediatr. Res., 2007, 61(5 Pt 2), 30R-37R.
[http://dx.doi.org/10.1203/pdr.0b013e31804575f7] [PMID: 17413847]
[74]
Geiman, T.M.; Robertson, K.D. Chromatin remodeling, histone modifications, and DNA methylation-how does it all fit together? J. Cell. Biochem., 2002, 87(2), 117-125.
[http://dx.doi.org/10.1002/jcb.10286] [PMID: 12244565]
[75]
Gabory, A.; Attig, L.; Junien, C. Developmental programming and epigenetics. Am. J. Clin. Nutr., 2011, 94(Suppl. 6), 1943S-1952S.
[http://dx.doi.org/10.3945/ajcn.110.000927] [PMID: 22049164]
[76]
Butler, J.S.; Koutelou, E.; Schibler, A.C.; Dent, S.Y. Histone-modifying enzymes: Regulators of developmental decisions and drivers of human disease. Epigenomics, 2012, 4(2), 163-177.
[http://dx.doi.org/10.2217/epi.12.3] [PMID: 22449188]
[77]
Funato, H.; Oda, S.; Yokofujita, J.; Igarashi, H.; Kuroda, M. Fasting and high-fat diet alter histone deacetylase expression in the medial hypothalamus. PLoS One, 2011, 6(4)e18950
[http://dx.doi.org/10.1371/journal.pone.0018950] [PMID: 21526203]
[78]
Gonçalves, L.K.; da Silva, I.R.V.; Cechinel, L.R.; Frusciante, M.R.; de Mello, A.S.; Elsner, V.R.; Funchal, C.; Dani, C. Maternal consumption of high-fat diet and grape juice modulates global histone H4 acetylation levels in offspring hippocampus: A preliminary study. Neurosci. Lett., 2017, 661, 29-32.
[http://dx.doi.org/10.1016/j.neulet.2017.09.042] [PMID: 28951285]
[79]
Strakovsky, R.S.; Zhang, X.; Zhou, D.; Pan, Y.X. The regulation of hepatic Pon1 by a maternal high-fat diet is gender specific and may occur through promoter histone modifications in neonatal rats. J. Nutr. Biochem., 2014, 25(2), 170-176.
[http://dx.doi.org/10.1016/j.jnutbio.2013.09.016] [PMID: 24445041]
[80]
Aagaard-Tillery, K.M.; Grove, K.; Bishop, J.; Ke, X.; Fu, Q.; McKnight, R.; Lane, R.H. Developmental origins of disease and determinants of chromatin structure: Maternal diet modifies the primate fetal epigenome. J. Mol. Endocrinol., 2008, 41(2), 91-102.
[http://dx.doi.org/10.1677/JME-08-0025] [PMID: 18515302]
[81]
Suter, M.A.; Chen, A.; Burdine, M.S.; Choudhury, M.; Harris, R.A.; Lane, R.H.; Friedman, J.E.; Grove, K.L.; Tackett, A.J.; Aagaard, K.M. A maternal high-fat diet modulates fetal SIRT1 histone and protein deacetylase activity in nonhuman primates. FASEB J., 2012, 26(12), 5106-5114.
[http://dx.doi.org/10.1096/fj.12-212878] [PMID: 22982377]
[82]
Borengasser, S.J.; Kang, P.; Faske, J.; Gomez-Acevedo, H.; Blackburn, M.L.; Badger, T.M.; Shankar, K. High fat diet and in utero exposure to maternal obesity disrupts circadian rhythm and leads to metabolic programming of liver in rat offspring. PLoS One, 2014, 9(1)e84209
[http://dx.doi.org/10.1371/journal.pone.0084209] [PMID: 24416203]
[83]
Aagaard-Tillery, K.M.; Grove, K.; Bishop, J.; Ke, X.; Fu, Q.; McKnight, R.; Lane, R.H. Developmental origins of disease and determinants of chromatin structure: Maternal diet modifies the primate fetal epigenome. J. Mol. Endocrinol., 2008, 41(2), 91-102.
[http://dx.doi.org/10.1677/JME-08-0025] [PMID: 18515302]
[84]
Vucetic, Z.; Kimmel, J.; Totoki, K.; Hollenbeck, E.; Reyes, T.M. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology, 2010, 151(10), 4756-4764.
[http://dx.doi.org/10.1210/en.2010-0505] [PMID: 20685869]
[85]
Zamore, P.D.; Haley, B. Ribo-gnome: The big world of small RNAs. Science, 2005, 309(5740), 1519-1524.
[http://dx.doi.org/10.1126/science.1111444] [PMID: 16141061]
[86]
Neri, C.; Edlow, A.G. Effects of maternal obesity on fetal programming: Molecular approaches. Cold Spring Harb. Perspect. Med., 2015, 6(2)a026591
[http://dx.doi.org/10.1101/cshperspect.a026591] [PMID: 26337113]
[87]
Nakahara, K.; Carthew, R.W. Expanding roles for miRNAs and siRNAs in cell regulation. Curr. Opin. Cell Biol., 2004, 16(2), 127-133.
[http://dx.doi.org/10.1016/j.ceb.2004.02.006] [PMID: 15196554]
[88]
Lee, H.S. Impact of maternal diet on the epigenome during in utero life and the developmental programming of diseases in childhood and adulthood. Nutrients, 2015, 7(11), 9492-9507.
[http://dx.doi.org/10.3390/nu7115467] [PMID: 26593940]
[89]
Benatti, R.O.; Melo, A.M.; Borges, F.O.; Ignacio-Souza, L.M.; Simino, L.A.P.; Milanski, M.; Velloso, L.A.; Torsoni, M.A.; Torsoni, A.S. Maternal high-fat diet consumption modulates hepatic lipid metabolism and microRNA-122 (miR-122) and microRNA-370 (miR-370) expression in offspring. Br. J. Nutr., 2014, 111(12), 2112-2122.
[http://dx.doi.org/10.1017/S0007114514000579] [PMID: 24666709]
[90]
Zhang, J.; Zhang, F.; Didelot, X.; Bruce, K.D.; Cagampang, F.R.; Vatish, M.; Hanson, M.; Lehnert, H.; Ceriello, A.; Byrne, C.D. Maternal high fat diet during pregnancy and lactation alters hepatic expression of insulin like growth factor-2 and key microRNAs in the adult offspring. BMC Genomics, 2009, 10(1), 478.
[http://dx.doi.org/10.1186/1471-2164-10-478] [PMID: 19835573]
[91]
Enquobahrie, D.A.; Wander, P.L.; Tadesse, M.G.; Qiu, C.; Holzman, C.; Williams, M.A. Maternal pre-pregnancy body mass index and circulating microRNAs in pregnancy. Obes. Res. Clin. Pract., 2017, 11(4), 464-474.
[http://dx.doi.org/10.1016/j.orcp.2016.10.287] [PMID: 27789200]
[92]
Méndez-Mancilla, A.; Lima-Rogel, V.; Toro-Ortíz, J.C.; Escalante-Padrón, F.; Monsiváis-Urenda, A.E.; Noyola, D.E.; Salgado-Bustamante, M. Differential expression profiles of circulating microRNAs in newborns associated to maternal pregestational overweight and obesity. Pediatr. Obes., 2018, 13(3), 168-174.
[http://dx.doi.org/10.1111/ijpo.12247] [PMID: 29045034]

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