Impact of oxidative stress during pregnancy on fetal epigenetic patterns and early origin of vascular diseases

Nutrition Reviews

Volumn 73, Issue 1, 2015, Pages 12-21

  Ávila, Jose Guillermo Ortega ^a,b   Echeverri, Isabella ^a,c   de Plata, Cecilia Aguilar ^a   Castillo, Andrés ^a  

^a UNIVERSIDAD DEL VALLE   (Colombia)

^b PONTIFICIA UNIVERSIDAD JAVERIANA   (Colombia)

^c UNIVERSIDAD ICESI   (Colombia)

Author keywords

Cardiovascular diseases; Endothelial dysfunction; Epigenetics; Fetal programming; Oxidative stress; Pregnancy

Indexed keywords

ANTIOXIDANT; CYTOSINE; DNA METHYLTRANSFERASE; GENOMIC DNA; GLUCOCORTICOID; HOMOCYSTEINE; METHIONINE; MICRORNA; REACTIVE OXYGEN METABOLITE;

ARTICLE; BLOOD CLOTTING DISORDER; CPG ISLAND; DYSLIPIDEMIA; ENDOTHELIAL DYSFUNCTION; ENVIRONMENTAL FACTOR; EPIGENETICS; GENETIC REGULATION; GLUCOSE INTOLERANCE; HUMAN; HYPERTENSION; ISCHEMIC HEART DISEASE; METHYLATION; OBESITY; OXIDATIVE STRESS; PREGNANCY; PROMOTER REGION; UTERUS; VASCULAR DISEASE; CARDIOVASCULAR DISEASES; FEMALE; FETUS DEVELOPMENT; GENETIC EPIGENESIS; GENETICS; PHYSIOLOGY;

CARDIOVASCULAR DISEASES; EPIGENESIS, GENETIC; FEMALE; FETAL DEVELOPMENT; HUMANS; OXIDATIVE STRESS; PREGNANCY;

EID: 84942244571     PISSN: 00296643     EISSN: 17534887     Source Type: Journal    
DOI: 10.1093/nutrit/nuu001     Document Type: Article

References (138)

1. Chmurzynska A. Fetal programming: link between early nutrition, DNA methylation, and complex diseases. Nutr Rev. 2010;68:87-98.
2. Waterland RA, Kellermayer R, Laritsky E, et al. Season of conception in rural Gambia affects DNA methylation at putative human metastable epialleles. PLoS Genet. 2010;6:e1001252.
3. Barker DJ. Developmental origins of chronic disease. Public Health. 2012;126:185-189.
4. Barker DJ, Gluckman PD, Godfrey KM, et al. Fetal nutrition and cardiovascular disease in adult life. Lancet. 1993;341:938-941.
5. Godfrey KM, Barker DJ. Fetal programming and adult health. Public Health Nutr. 2001;4:611-624.
6. Loke YJ, Novakovic B, Ollikainen M, et al. The Peri/postnatal Epigenetic Twins Study (PETS). Twin Res Hum Genet. 2013;16:13-20.
7. Gaziano TA. Cardiovascular disease in the developing world and its cost-effective management. Circulation. 2005;112:3547-3553.
8. Reardon S. A world of chronic disease. Science. 2011;333:558-559.
9. Robins JC, Marsit CJ, Padbury JF, et al. Endocrine disruptors, environmental oxygen, epigenetics and pregnancy. Front Biosci. 2011;1:690-700.
10. Hitchler MJ, Domann FE. An epigenetic perspective on the free radical theory of development. Free Radic Biol Med. 2007;43:1023-1036.
11. Ulrey CL, Liu L, Andrews LG, et al. The impact of metabolism on DNA methylation. Hum Mol Genet. 2005;1:R139-R147.
12. Kilcoyne KR, Smith LB, Atanassova N, et al. Fetal programming of adult Leydig cell function by androgenic effects on stem/progenitor cells. PNAS. 2014;111:E1924-E1932.
13. Ogita H, Liao JK. Endothelial function and oxidative stress. Endothelium. 2004;11:123-132.
14. Kinlay S, Ganz P. Relation between endothelial dysfunction and the acute coronary syndrome: implications for therapy. Am J Cardiol. 2000;86:10J-13J.
15. Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation. 2000;101:1899-1906.
16. Kim F, Pham M, Maloney E, et al. Vascular inflammation, insulin resistance, and reduced nitric oxide production precede the onset of peripheral insulin resistance. Arterioscler Thromb Vasc Biol. 2008;28:1982-1988.
17. Rexhaj E, Paoloni-Giacobino A, Rimoldi SF, et al. Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span. J Clin Invest. 2013;123:5052-5060.
18. Gan Y, Shen YH, Wang J, et al. Role of histone deacetylation in cell-specific expression of endothelial nitric-oxide synthase. J Biol Chem. 2005;280:16467-16475.
19. Barre`s R, Osler ME, Yan J, et al. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab. 2009;10:189-198.
20. Yu S, Khor TO, Cheung KL, et al. Nrf2 expression is regulated by epigeneticmechanisms in prostate cancer of TRAMP mice. PLoS One. 2010;5:e8579.
21. Dørup I, Skajaa K, Sørensen KE. Normal pregnancy is associated with enhanced endothelium-dependent flow-mediated vasodilation. Am J Physiol. 1999;276:H821-H825.
22. Williams DJ, Vallance PJ, Neild GH, et al. Nitric oxide-mediated vasodilation in human pregnancy. Am J Physiol. 1997;272:H748-H752.
23. Khan F, Mires G, Macleod M, et al. Relationship between maternal arterial wave reflection, microvascular function and fetal growth in normal pregnancy. Microcirculation. 2010;17:608-614.
24. Elvan-Taspinar A, Franx A, Bots ML, et al. Arterial stiffness and fetal growth in normotensive pregnancy. Am J Hypertens. 2005;18:337-341.
25. Veas CJ, Aguilera VC, Muñoz IJ, et al. Fetal endothelium dysfunction is associated with circulating maternal levels of sE-selectin, sVCAM1, and sFlt-1 during preeclampsia. J Matern Fetal Neonatal Med. 2011;24:1371-1377.
26. Martin H, Gazelius B, Norman M. Impaired acetylcholine-induced vascular relaxation in low birthweight infants: implications for adult hypertension. Pediatr Res. 2000;47:457-462.
27. Norman M, Martin H. Preterm birth attenuates association between low birth weight and endothelial dysfunction. Circulation. 2003;108:996-1001.
28. Martin H, Hu J, Gennser G, et al. Impaired endothelial function and increased carotid stiffness in 9-year-old children with low birthweight. Circulation. 2000;102:2739-2744.
29. Goodfellow J, Bellamy MF, Gorman ST, et al. Endothelial function is impaired in fit young adults of low birth weight. Cardiovasc Res. 1998;40:600-606.
30. Leeson CPM, Kattenhorn M, Morley R, et al. Impact of low birth weight and cardiovascular risk factors on endothelial function in early adult life. Circulation. 2001;103:1264-1268.
31. Ligi I, Simoncini S, Tellier E, et al. A switch toward angiostatic gene expression impairs the angiogenic properties of endothelial progenitor cells in low birth weight preterm infants. Blood. 2011;118:1699-1709.
32. Ozaki T, Hawkins P, Nishina H, et al. Effects of undernutrition in early pregnancy on systemic small artery function in late-gestation fetal sheep. Am J Obstet Gynecol. 2000;183:1301-1307.
33. Nishina H, Green LR, McGarrigle HHG, et al. Effect of nutritional restriction in early pregnancy on isolated femoral artery function in midgestation. fetal sheep. J Physiol. 2003;553:637-647.
34. Williams SJ, Hemmings DG, Mitchell JM, et al. Effects of maternal hypoxia or nutrient restriction during pregnancy on endothelial function in adult male rat offspring. J Physiol. 2005;565:125-135.
35. Andersen MR, Walker LR, Stender S. Reduced endothelial nitric oxide synthase activity and concentration in fetal umbilical veins from maternal cigarette smokers. Am J Obstet Gynecol. 2004;191:346-351.
36. O'Regan D, Kenyon CJ, Seckl JR, et al. Glucocorticoid exposure in late gestation in the rat permanently programs gender-specific differences in adult cardiovascular and metabolic physiology. Am J Physiol Endocrinol Metab. 2004;287:E863-E870.
37. Ozaki T, Nishina H, Hanson MA, et al. Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol. 2001;530:141-152.
38. Brawley L, Itoh S, Torrens C, et al. Dietary protein restriction in pregnancy induces hypertension and vascular defects in rat male offspring. Pediatr Res. 2003;54:1-7.
39. Franco MC, Dantas AP, Akamine EH, et al. Enhanced oxidative stress as a potential mechanism underlying the programming of hypertension in utero. J Cardiovasc Pharmacol. 2002;40:501-509.
40. Franco MC, Akamine EH, Rebouças N, et al. Long-term effects of intrauterine malnutrition on vascular function in female offspring: implications of oxidative stress. Life Sci. 2007;80:709-715.
41. Hung TH, Lo LM, Chiu TH, et al. A longitudinal study of oxidative stress and antioxidant status in women with uncomplicated pregnancies throughout gestation. Reprod Sci. 2010;17:401-409.
42. Belo L, Caslake M, Santos-Silva A, et al. LDL size, total antioxidant status and oxidised LDL in normal human pregnancy: a longitudinal study. Atherosclerosis. 2004;177:391-399.
43. Roes EM, Hendriks JC, Raijmakers MT, et al. A longitudinal study of antioxidant status during uncomplicated and hypertensive pregnancies. Acta Obstet Gynecol Scand. 2006;85:148-155.
44. Toescu V, Nuttall SL, Martin U, et al. Changes in plasma lipids and markers of oxidative stress in normal pregnancy and pregnancies complicated by diabetes. Clin Sci. 2004;106:93-98.
45. Orhan H, Onderoglu L, Yücel A, et al. Circulating biomarkers of oxidative stress in complicated pregnancies. Arch Gynecol Obstet. 2003;267:189-195.
46. Palm M, Axelsson O, Wernroth L, et al. F(2)-isoprostanes, tocopherols and normal pregnancy. Free Radic Res. 2009;43:546-552.
47. Jauniaux E, Watson AL, Hempstock J, et al. Onset of maternal arterial bloodflow and placental oxidative stress; a possible factor in human early pregnancy failure. Am J Pathol. 2000;157:2111-2122.
48. Barden A, Beilin LJ, Ritchie J, et al. Plasma and urinary 8-iso-prostane as an indicator of lipid peroxidation in pre-eclampsia and normal pregnancy. Clin Sci. 1996;91:711-718.
49. Harsem NK, Braekke K, Staff AC. Augmented oxidative stress as well as antioxidant capacity in maternal circulation in preeclampsia. Eur J Obstet Gynecol Reprod Biol. 2005;128:209-215.
50. Wang CN, Chen JY, Sabu S, et al. Elevated amniotic fluid F(2)-isoprostane: a potential predictive marker for preeclampsia. Free Radic Biol Med. 2011;50:1124-1130.
51. Coughlan MT, Vervaart PP, Permezel M, et al. Altered placental oxidative stress status in gestational diabetes mellitus. Placenta. 2004;25:78-84.
52. Biri A, Onan A, Devrim E, et al. Oxidant status in maternal and cord plasma and placental tissue in gestational diabetes. Placenta. 2006;27:327-332.
53. Biri A, Bozkurt N, Turp A, et al. Role of oxidative stress in intrauterine growth restriction. Gynecol Obstet Invest. 2007;64:187-192.
54. Kressig P, Beinder E, Schweer H, et al. Post-delivery oxidative stress in women with preeclampsia or IUGR. J Perinat Med. 2008;36:310-315.
55. Gomes HF, Palei AC, Machado JS, et al Assessment of oxidative status markers and NO bioavailability in hypertensive disorders of pregnancy. J Hum Hypertens. 2013;27:345-348.
56. Rajasingam D, Seed PT, Briley AL, et al. A prospective study of pregnancy outcome and biomarkers of oxidative stress in nulliparous obese women. Am J Obstet Gynecol. 2009;200:395.e1-395.e9.
57. Kim YJ, Hong YC, Lee KH, et al., Oxidative stress in pregnant women and birth weight reduction. Reprod Toxicol. 2005;19:487-492.
58. Min J, Park H, Park B, et al. Paraoxonase gene polymorphism and vitamin levels during pregnancy: relationship with maternal oxidative stress and neonatal birthweights. Reprod Toxicol. 2006;22:418-424.
59. Min J, Park B, Kim YJ, et al. Effect of oxidative stress on birth sizes: consideration of window from mid pregnancy to delivery. Placenta. 2009;30:418-423.
60. Myatt L, Kossenjans W, Sahay R, et al. Oxidative stress causes vascular dysfunction in the placenta. J Matern Fetal Neonatal Med. 2000;9:79-82.
61. Hong J, Park EA, Kim YJ, et al. Association of antioxidant vitamins and oxidative stress levels in pregnancy with infant growth during the first year of life. Public Health Nutr. 2008;11:998-1005.
62. Lee BE, Hong YC, Lee KH, et al. Influence of maternal serum levels of vitamins C and E during the second trimester on birth weight and length. Eur J Clin Nutr. 2004;58:1365-1371.
63. Hracsko Z, Orvos H, Novak Z, et al. Evaluation of oxidative stress markers in neonates with intra-uterine growth retardation. Redox Rep. 2008;13:11-16.
64. Saker M, Soulimane Mokhtari N, Merzouk SA, et al. Oxidant and antioxidant status in mothers and their newborns according to birthweight. Eur J Obstet Gynecol Reprod Biol. 2008;141:95-99.
65. Morton JS, Rueda-Clausen CF, Davidge ST. Flow-mediated vasodilation is impaired in adult rat offspring exposed to prenatal hypoxia. J Appl Physiol. 2011;110:1073-1082.
66. Argüelles S, Machado MJ, Ayala A, et al. Correlation between circulating biomarkers of oxidative stress of maternal and umbilical cord blood at birth. Free Radic Res. 2006;40:565-570.
67. Rodford JL, Torrens C, Siow RC, et al. Endothelial dysfunction and reduced antioxidant protection in an animal model of the developmental origins of cardiovascular disease. J Physiol. 2008;586:4709-4720.
68. Peterside IE, Selak MA, Simmons RA. Impaired oxidative phosphorylation in hepatic mitochondria of growth retarded rats alters glucose metabolism. Am J Physiol Endocrinol Metab; 2003;285:1258-1264.
69. Rodford JL, Torrens C, Siow RC, et al. Endothelial dysfunction and reduced antioxidant protection in an animal model of the developmental origins of cardiovascular disease. J Physiol. 2008;586:4709-4720.
70. Franco Mdo C, Dantas AP, Akamine EH, et al. Enhanced oxidative stress as a potential mechanism underlying the programming of hypertension in utero. Cardiovasc Pharmacol. 2002;40:501-509.
71. Desai M, Gayle D, Babu J, et al. Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition. Am J Physiol Regul Integr Comp Physiol. 2005;288:R91-R96.
72. Xiao D, Hu XQ, Huang X, et al. Chronic hypoxia during gestation enhances uterine arterial myogenic tone via heightened oxidative stress. PLoS One. 2013;8:e73731.
73. Dhar-Mascareño M, Cárcamo JM, Golde DW. Hypoxia-reoxygenation-induced mitochondrial damage and apoptosis in human endothelial cells are inhibited by vitamin C. Free Radic Biol Med. 2005;38:1311-1322.
74. Gupta P, Narang M, Banerjee BD, et al. Oxidative stress in term small for gestational age neonates born to undernourished mothers: a case control study. BMC Pediatr. 2004;4:14.
75. Tarry-Adkins JL, Martin-Gronert MS, Fernandez-Twinn DS, et al. Poor maternal nutrition followed by accelerated postnatal growth leads to alterations in DNA damage and repair, oxidative and nitrosative stress, and oxidative defense capacity in rat heart. FASEB J. 2013;27:379-390.
76. Liang C, Oest ME, Prater MR. Intrauterine exposure to high saturated fat diet elevates risk of adult-onset chronic diseases in C57BL/6 mice. Birth Defects Res B Dev Reprod Toxicol. 2009;86:377-384.
77. Racasan S, Braam B, van der Giezen DM, et al. Perinatal L-arginine and antioxidant supplements reduce adult blood pressure in spontaneously hypertensive rats. Hypertension. 2004;44:83-88.
78. Franco Mdo C, Akamine EH, Aparecida de Oliveira M, et al. Vitamins C and E improve endothelial dysfunction in intrauterine-undernourished rats by decreasing vascular superoxide anion concentration. J Cardiovasc Pharmacol. 2003;42:211-217.
79. Cambonie G, Comte B, Yzydorczyk C, et al. Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet. Am J Physiol Regul Integr Comp Physiol. 2007;292:R1236-R1245.
80. Giussani DA, Camm EJ, Niu Y, et al. Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS One. 2012;7:e31017.
81. Kane AD, Herrera EA, Camm EJ, et al. Vitamin C prevents intrauterine programming of in vivo cardiovascular dysfunction in the rat. Circ J. 2013;77:2604-2611.
82. Rueda-Clausen CF, Morton JS, Davidge ST. The early origins of cardiovascular health and disease: who, when, and how. Semin Reprod Med. 2011;29:197-210.
83. Roseboom TJ, van der Meulen JHP, Osmond C, et al. Coronary heart disease after prenatal exposure to the Dutch famine. Heart. 2000;84:595-598.
84. Roseboom TJ, van der Meulen JHP, Osmond C, et al. Plasma lipid profiles in adults after prenatal exposure to the Dutch famine. Am J Clin Nutr. 2000;72:1101-1106.
85. Wang PX, Wang JJ, Lei YX, et al. Impact of fetal and infant exposure to the Chinese Great Famine on the risk of hypertension in adulthood. PLoS One. 2012;7:e49720.
86. Jaddoe VW, de Jonge LL, Hofman A, et al. First trimester fetal growth restriction and cardiovascular risk factors in school age children: population based cohort study. BMJ. 2014;348:g14.
87. Roseboom TJ, van der Meulen JH, van Montfrans GA, et al. Maternal nutrition during gestation and blood pressure in later life. J Hypertens. 2001;19:29-34.
88. Painter RC, de Rooij SR, Bossuyt PM, et al. Maternal nutrition during gestation and carotid arterial compliance in the adult offspring: the Dutch famine birth cohort. J Hypertens. 2007;25:533-540.
89. Touwslager RN, Gerver WJ, Tan FE, et al. Influence of growth during infancy on endothelium-dependent vasodilatation at the age of 6 months. Hypertension. 2012;60:1294-1300.
90. Idris NS, Uiterwaal CS, van der Schouw YT, et al. Famine in childhood and postmenopausal coronary artery calcification: a cohort study. BMJ. 2013;3:e003818.
91. van Abeelen AF, Elias SG, Bossuyt PM, et al. Cardiovascular consequences of famine in the young. Eur Heart J. 2012;33:538-545.
92. Morgan HD, Santos F, Green K, et al. Epigenetic reprogramming in mammals. Hum Mol Genet. 2005;14:R47-R58.
93. Fuks F, Hurd PJ, Wolf D, et al. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem. 2003;278:4035-4040.
94. Kirchner H, Osler ME, Krook A, et al. Epigenetic flexibility in metabolic regulation:disease cause and prevention? Trends Cell Biol. 2013;23:203-209.
95. Zee BM, Levin RS, Dimaggio PA, et al. Global turnover of histone post-translational modifications and variants in human cells. Epigenetics Chromatin. 2010;3:22.
96. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature. 2007;447:425-432.
97. Cerda S, Weitzman SA. Influence of oxygen radical injury on DNA methylation. Mutat Res. 1997;386:141-152.
98. Valinluck V, Tsai HH, Rogstad DK, et al. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res. 2004;32:4100-4108.
99. Ghosh R, Mitchell DL. Effect of oxidative DNA damage in promoter elements on transcription factor binding. Nucleic Acids Res. 1999;27:3213-3218.
100. Maltseva DV, Baykov AA, Jeltsch A, et al. Impact of 7,8-dihydro-8-oxoguanine on methylation of the CpG site by Dnmt3a. Biochemistry. 2009;48:1361-1368
101. Turk PW, Laayoun A, Smith SS, et al. DNA adduct 8-hydroxyl-20-deoxyguanosine (8-hydroxyguanine) affects function of human DNAmethyltransferase. Carcinogenesis. 1995;16: 1253-1255.
102. Kasai H. Analysis of a form of oxidative DNA damage, 8-hydroxy-2'-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutat Res. 1997;387:147-163.
103. Akatsuka S, Aung TT, Dutta KK, et al. Contrasting genome-wide distribution of 8- hydroxyguanine and acrolein-modified adenine during oxidative stress-induced renal carcinogenesis. Am J Pathol. 2006;169:1328-1342.
104. Campos AC, Molognoni F, Melo FH, et al. Oxidative stress modulates DNA methylation during melanocyte anchorage blockade associated with malignant transformation. Neoplasia. 2007;9:1111-1121.
105. Lim SO, Gu JM, Kim MS, et al. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology. 2008;135:2128-2140.
106. Min JY, Lim SO, Jung G. Downregulation of catalase by reactive oxygen species via hypermethylation of CpG island II on the catalase promoter. FEBS Lett. 2010;584:2427-2432.
107. Hong J, Resnick M, Behar J, et al. Acid-induced p16 hypermethylation contributes to development of esophageal adenocarcinoma via activation of NADPH oxidase NOX5-S. Am J Physiol Gastrointest Liver Physiol. 2010;299:G697-G706
108. Ulrey CL, Liu L, Andrews LG, et al. The impact of metabolism on DNA methylation. Hum Mol Genet. 2005;1:R139-R147.
109. Loenen WA. S-Adenosylmethionine: jack of all trades and master of everything? Biochem Soc Trans. 2006;34:330-333.
110. Mosharov E, Cranford MR, Banerjee R. The quantitatively important relationship between homocysteine metabolism and glutathione synthesis by the transsulfuration pathway and its regulation by redox changes. Biochemistry. 2000;39:13005-13011.
111. Day RM, Suzuki YJ, Fanburg BL. Regulation of glutathione by oxidative stress in bovine pulmonary artery endothelial cells. Antioxid Redox Signal. 2003;5:699-704.
112. Lertratanangkoon K, Orkiszewski RS, Scimeca JM. Methyl-donor deficiency due to chemically induced glutathione depletion. Cancer Res. 1996;56:995-1005.
113. Lertratanangkoon K, Wu CJ, Savaraj N, et al. Alterations of DNA methylation by glutathione depletion. Cancer Lett. 1997;120:149-156.
114. Niedzwiecki MM, Hall MN, Liu X, et al. Blood glutathione redox status and global methylation of peripheral blood mononuclear cell DNA in Bangladeshi adults. Epigenetics. 2013;8:730-738.
115. Garciá-Giménez JL, Olaso G, Hake SB, et al. Histone h3 glutathionylation in proliferating mammalian cells destabilizes nucleosomal structure. Antioxid Redox Signal. 2013;19:1305-1320.
116. Fryer AA, Emes RD, Ismail KM, et al. Quantitative, high-resolution epigenetic profiling of CpG loci identifies associations with cord blood plasma homocysteine and birth weight in humans. Epigenetics. 2011;6:86-94.
117. Avila MA, Corrales FJ, Ruiz F, et al. Specific interaction of methionine adenosyltransferase with free radicals. Biofactors. 1998;8:27-32.
118. Corrales FJ, Perez-Mato I, Sanchez Del Pino MM, et al. Regulation of mammalian liver methionine adenosyltransferase. J Nutr. 2002;132:2377S-2381S.
119. Katoh Y, Ikura T, Hoshikawa Y, et al. Methionine adenosyltransferase II serves as a transcriptional corepressor of Maf oncoprotein. Mol Cell. 2011;41:554-566.
120. Jiménez-Chillarón JC, Dyáz R, Martyńez D, et al. The role of nutrition on epigenetic modifications and their implications on health. Biochimie. 2012;94:2242-2263.
121. Vertuani S, Angusti A, Manfredini S. The antioxidants and pro-antioxidants network:an overview. Curr Pharm Des. 2004;10:1677-1694.
122. Lillycrop KA, Rodford J, Garratt ES, et al. Maternal protein restriction with or without folic acid supplementation during pregnancy alters the hepatic transcriptome in adult male rats. Br J Nutr. 2010;103:1711-1719.
123. Morris TJ, Vickers M, Gluckman P, et al. Transcriptional profiling of rats subjected to gestational undernourishment: implications for the developmental variations in metabolic traits. PLoS One. 2009;29:e7271.
124. Li Y, Zhang X, Sun Y, et al. Folate deficiency during early-mid pregnancy affects the skeletal muscle transcriptome of piglets from a reciprocal cross. PLoS One. 2013;8:e82616.
125. Tian YJ, Luo N, Chen NN, et al. Maternal nicotinamide supplementation causes global DNA hypomethylation, uracil hypo-incorporation and gene expression changes in fetal rats. Br J Nutr. 2014;10:1-8.
126. Chawla RK, Watson WH, Jones DP. Effect of hypoxia on hepatic DNA methylation and tRNAmethyltransferase in rat: similarities to effects of methyl-deficient diets. J Cell Biochem. 1996;61:72-80.
127. Shahrzad S, Bertrand K, Minhas K, et al. Induction of DNA hypomethylation by tumor hypoxia. Epigenetics. 2007;2:119-125.
128. Ke X, Lei Q, James SJ, et al. Uteroplacental insufficiency affects epigenetic determinants of chromatin structure in brains of neonatal and juvenile IUGR rats. Physiol Genomics. 2006; 25:16-28.
129. Park JH, Stoffers DA, Nicholls RD, et al. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest. 2008;118:2316-2324.
130. Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci. 2008;105:17046-17049.
131. Stein AD, Zybert PA, Van de Bor M, et al. Intrauterine famine exposure and body proportions at birth: the Dutch Hunger Winter. Int J Epidemiol. 2004;33:831-836.
132. Tobi EW, Lumey LH, Talens RP, et al. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet. 2009;18:4046-4053.
133. Krause BJ, Costello PM, Muñoz-Urrutia E, et al. Role of DNA methyltransferase 1 on the altered eNOS expression in human umbilical endothelium from intrauterine growth restricted fetuses. Epigenetics. 2013;8:944-952.
134. Pandey D, Sikka G, Bergman Y, et al. Transcriptional regulation of endothelial arginase 2 by histone deacetylase 2. Arterioscler Thromb Vasc Biol. 2014;34:1556-1566.
135. Patterson AJ, Xiao D, Xiong F, et al. Hypoxia-derived oxidative stress mediates epigenetic repression of PKCe gene in foetal rat hearts. Cardiovasc Res. 2012;93:302-310.
136. Vassallo PF, Simoncini S, Ligi I, et al. Accelerated senescence of cord blood endothelial progenitor cells in premature neonates is driven by SIRT1 decreased expression. Blood. 2014;123:2116-2126.
137. Dasgupta C, Chen M, Zhang H, et al. Chronic hypoxia during gestation causes epigenetic repression of the estrogen receptor-a gene in ovine uterine arteries via heightened promoter methylation. Hypertension. 2012;60:697-704.
138. Lau C, Rogers JM, Desai M, et al. Fetal programming of adult disease: implications for prenatal care. Obstet Gynecol. 2011;117:978-985.