In utero oxidative stress epigenetically programs antioxidant defense capacity and adulthood diseases

Antioxidants and Redox Signaling

Volumn 17, Issue 2, 2012, Pages 237-253

  Strakovsky, Rita S ^a   Pan, Yuan Xiang ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ANTIOXIDANT; HEAVY METAL; HYDROGEN PEROXIDE; INTERLEUKIN 6; INTERLEUKIN 8; LEPTIN; LIPOPOLYSACCHARIDE; MALONALDEHYDE; MONOCYTE CHEMOTACTIC PROTEIN 1; NICOTINE; REACTIVE OXYGEN METABOLITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TUMOR NECROSIS FACTOR ALPHA; XENOBIOTIC AGENT;

ADULTHOOD; ANTIOXIDANT ACTIVITY; BLOOD VOLUME; CELL CYCLE; CELL DIFFERENTIATION; DNA METHYLATION; ENVIRONMENTAL FACTOR; EPIGENETICS; GENE EXPRESSION; HEART OUTPUT; INSULIN DEPENDENT DIABETES MELLITUS; INTRAUTERINE GROWTH RETARDATION; LIPID PEROXIDATION; MATERNAL NUTRITION; MATERNAL OBESITY; MATERNAL SMOKING; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PREECLAMPSIA; PREGNANCY; PREGNANCY DIABETES MELLITUS; PREGNANCY OUTCOME; PRIORITY JOURNAL; PULSE RATE; REVIEW; SYSTEMIC VASCULAR RESISTANCE;

ANIMALS; ANTIOXIDANTS; DISEASE; EPIGENESIS, GENETIC; FEMALE; HUMANS; OXIDATIVE STRESS; UTERUS;

ANIMALIA;

EID: 84862064764     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4372     Document Type: Review

References (140)

1. Aagaard-Tillery KM, Grove K, Bishop J, Ke X, Fu Q, McKnight R, and Lane RH. Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 41: 91-102, 2008.
2. Akyol A, Langley-Evans SC, and McMullen S. Obesity induced by cafeteria feeding and pregnancy outcome in the rat. Br J Nutr 102: 1601-1610, 2009.
3. Al-Gubory KH, Bolifraud P, Germain G, Nicole A, and Ceballos-Picot I. Antioxidant enzymatic defence systems in sheep corpus luteum throughout pregnancy. Reproduction 128: 767-774, 2004. (Pubitemid 40028553)
4. Allen RG and Balin AK. Oxidative influence on development and differentiation: an overview of a free radical theory of development. Free Radic Biol Med 6: 631-661, 1989. (Pubitemid 19147814)
5. Allen RG and Venkatraj VS. Oxidants and antioxidants in development and differentiation. J Nutr 122: 631-635, 1992.
6. Archer SL, Marsboom G, Kim GH, Zhang HJ, Toth PT, Svensson EC, Dyck JR, Gomberg-Maitland M, Thebaud B, Husain AN, Cipriani N, and Rehman J. Epigenetic attenuation of mitochondrial superoxide dismutase 2 in pulmonary arterial hypertension: a basis for excessive cell proliferation and a new therapeutic target. Circulation 121: 2661-2671, 2010.
7. Aris A, Benali S, Ouellet A, Moutquin JM, and Leblanc S. Potential biomarkers of preeclampsia: inverse correlation between hydrogen peroxide and nitric oxide early in maternal circulation and at term in placenta of women with preeclampsia. Placenta 30: 342-347, 2009.
8. Atamer Y, Kocyigit Y, Yokus B, Atamer A, and Erden AC. Lipid peroxidation, antioxidant defense, status of trace metals and leptin levels in preeclampsia. Eur J Obstet Gynecol Reprod Biol 119: 60-66, 2005. (Pubitemid 40289099)
9. Baiza-Gutman LA, Flores-Sanchez MM, Diaz-Flores M, and Hicks JJ. Presence of uterine peroxidase activity in the rat early pregnancy. Int J Biochem Cell Biol 32: 255-262, 2000. (Pubitemid 30001827)
10. Ball ER, Caniglia MK, Wilcox JL, Overton KA, Burr MJ, Wolfe BD, Sanders BJ, Wisniewski AB, and Wrenn CC. Effects of genistein in the maternal diet on reproductive development and spatial learning in male rats. Horm Behav 57: 313-322, 2010.
11. Barker DJ. The developmental origins of adult disease. J Am Coll Nutr 23: 588S-595S, 2004. (Pubitemid 40096746)
12. Bayol SA, Simbi BH, Fowkes RC, and Stickland NC. A maternal " junk food" diet in pregnancy and lactation pro-motes nonalcoholic Fatty liver disease in rat offspring. Endocrinology 151: 1451-1461, 2010.
13. Bayol SA, Simbi BH, and Stickland NC. A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 567: 951-961, 2005. (Pubitemid 41387836)
14. Bernardi F, Guolo F, Bortolin T, Petronilho F, and Dal-Pizzol F. Oxidative stress and inflammatory markers in normal pregnancy and preeclampsia. J Obstet Gynaecol Res 34: 948-951, 2008.
15. Biri A, Bozkurt N, Turp A, Kavutcu M, Himmetoglu O, and Durak I. Role of oxidative stress in intrauterine growth restriction. Gynecol Obstet Invest 64: 187-192, 2007. (Pubitemid 350099002)
16. Bonnet S, Michelakis ED, Porter CJ, Andrade-Navarro MA, Thebaud B, Haromy A, Harry G, Moudgil R, McMurtry MS, Weir EK, and Archer SL. An abnormal mitochondrialhypoxia inducible factor-1alpha-Kv channel pathway disrupts oxygen sensing and triggers pulmonary arterial hypertension in fawn hooded rats: similarities to human pulmonary arterial hypertension. Circulation 113: 2630-2641, 2006. (Pubitemid 43948012)
17. Bouanane S, Benkalfat NB, Baba Ahmed FZ, Merzouk H, Mokhtari NS, Merzouk SA, Gresti J, Tessier C, and Narce M. Time course of changes in serum oxidant/antioxidant status in overfed obese rats and their offspring. Clin Sci (Lond) 116: 669-680, 2009.
18. Bruce KD, Cagampang FR, Argenton M, Zhang J, Ethirajan PL, Burdge GC, Bateman AC, Clough GF, Poston L, Hanson MA, McConnell JM, and Byrne CD. Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology 50: 1796-1808, 2009.
19. Bruin JE, Petre MA, Lehman MA, Raha S, Gerstein HC, Morrison KM, and Holloway AC. Maternal nicotine exposure increases oxidative stress in the offspring. Free Radic Biol Med 44: 1919-1925, 2008.
20. Bruin JE, Petre MA, Raha S, Morrison KM, Gerstein HC, and Holloway AC. Fetal and neonatal nicotine exposure in Wistar rats causes progressive pancreatic mitochondrial damage and beta cell dysfunction. PLoS One 3: e3371, 2008.
21. Burton GJ. Oxygen, the Janus gas;its effects on human placental development and function. J Anat 215: 27-35, 2009.
22. Caluwaerts S, Lambin S, van Bree R, Peeters H, Vergote I, and Verhaeghe J. Diet-induced obesity in gravid rats engenders early hyperadiposity in the offspring. Metabolism 56: 1431-1438, 2007. (Pubitemid 47404608)
23. Carter AM. Placental oxygen consumption. Part I: in vivo studies-a review. Placenta 21 Suppl A: S31-S37, 2000.
24. Chan GC, Fish JE, Mawji IA, Leung DD, Rachlis AC, and Marsden PA. Epigenetic basis for the transcriptional hyporesponsiveness of the human inducible nitric oxide synthase gene in vascular endothelial cells. J Immunol 175: 3846-3861, 2005. (Pubitemid 41292045)
25. Chan WH. Impact of genistein on maturation of mouse oocytes, fertilization, and fetal development. Reprod Toxicol 28: 52-58, 2009.
26. Chen JH, Tarry-Adkins JL, Matharu K, Yeo GS, and Ozanne SE. Maternal protein restriction affects gene expression profiles in the kidney at weaning with implications for the regulation of renal function and lifespan. Clin Sci (Lond) 119: 373-384, 2010.
27. Cho SH, Choi MH, Kwon OS, Lee WY, and Chung BC. Metabolic significance of bisphenol A-induced oxidative stress in rat urine measured by liquid chromatographymass spectrometry. J Appl Toxicol 29: 110-117, 2009.
28. Cimafranca MA, Davila J, Ekman GC, Andrews RN, Neese SL, Peretz J, Woodling KA, Helferich WG, Sarkar J, Flaws JA, Schantz SL, Doerge DR, and Cooke PS. Acute and chronic effects of oral genistein administration in neonatal mice. Biol Reprod 83: 114-121, 2010.
29. Coughlan MT, Permezel M, Georgiou HM, and Rice GE. Repression of oxidant-induced nuclear factor-kappaB activity mediates placental cytokine responses in gestational diabetes. J Clin Endocrinol Metab 89: 3585-3594, 2004. (Pubitemid 38951938)
30. Coughlan MT, Vervaart PP, Permezel M, Georgiou HM, and Rice GE. Altered placental oxidative stress status in gestational diabetes mellitus. Placenta 25: 78-84, 2004. (Pubitemid 38100769)
31. Crinnion WJ. Maternal levels of xenobiotics that affect fetal development and childhood health. Altern Med Rev 14: 212-222, 2009.
32. Daikoku T, Matsumoto H, Gupta RA, Das SK, Gassmann M, DuBois RN, and Dey SK. Expression of hypoxiainducible factors in the peri-implantation mouse uterus is regulated in a cell-specific and ovarian steroid hormonedependent manner. Evidence for differential function of HIFs during early pregnancy. J Biol Chem 278: 7683-7691, 2003. (Pubitemid 36800778)
33. Davison JM, Mellott TJ, Kovacheva VP, and Blusztajn JK. 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 284: 1982-1989, 2009.
34. Devasagayam TP, Sivabalan R, and Tarachand U. Lipid peroxidation in the rat uterus during deciduoma induced cell differentiation. Biochem Int 21: 27-32, 1990. (Pubitemid 20181138)
35. Dolinoy DC, Weidman JR, Waterland RA, and Jirtle RL. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect 114: 567-572, 2006.
36. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95, 2002. (Pubitemid 34654215)
37. Dunwoodie SL. The role of hypoxia in development of the Mammalian embryo. Dev Cell 17: 755-773, 2009.
38. Fall C. Maternal nutrition: effects on health in the next generation. Indian J Med Res 130: 593-599, 2009.
39. Fetoui H, Garoui M, and Zeghal N. Protein restriction in pregnant-and lactating rats-induced oxidative stress and hypohomocysteinaemia in their offspring. J Anim Physiol Anim Nutr (Berl) 93: 263-270, 2009.
40. Forsberg H, Borg LA, Cagliero E, and Eriksson UJ. Altered levels of scavenging enzymes in embryos subjected to a diabetic environment. Free Radic Res 24: 451-459, 1996. (Pubitemid 26188963)
41. Garrel C, Fowler PA, and Al-Gubory KH. Developmental changes in antioxidant enzymatic defences against oxidative stress in sheep placentomes. J Endocrinol 205: 107-116, 2010.
42. Golub MS, Wu KL, Kaufman FL, Li LH, Moran-Messen F, Zeise L, Alexeeff GV, and Donald JM. Bisphenol A: developmental toxicity from early prenatal exposure. Birth Defects Res B Dev Reprod Toxicol 89: 441-466, 2010.
43. Gong L, Pan YX, and Chen H. Gestational low protein diet in the rat mediates Igf2 gene expression in male offspring via altered hepatic DNA methylation. Epigenetics 5: 619-626, 2010.
44. Halliwell B. Protection against tissue damage in vivo by desferrioxamine: what is its mechanism of action? Free Radic Biol Med 7: 645-651, 1989. (Pubitemid 20027483)
45. Hengstler JG, Foth H, Gebel T, Kramer PJ, Lilienblum W, Schweinfurth H, Volkel W, Wollin KM, and Gundert-Remy U. Critical evaluation of key evidence on the human health hazards of exposure to bisphenol A. Crit Rev Toxicol 41: 263-291, 2011.
46. Hiltunen MO, Turunen MP, Hakkinen TP, Rutanen J, Hedman M, Makinen K, Turunen AM, Aalto-Setala K, and Yla-Herttuala S. DNA hypomethylation and methyltransferase expression in atherosclerotic lesions. Vasc Med 7: 5-11, 2002. (Pubitemid 34654067)
47. Hitchler MJ, Oberley LW, and Domann FE. Epigenetic silencing of SOD2 by histone modifications in human breast cancer cells. Free Radic Biol Med 45: 1573-1580, 2008.
48. Hitchler MJ, Wikainapakul K, Yu L, Powers K, Attatippaholkun W, and Domann FE. Epigenetic regulation of manganese superoxide dismutase expression in human breast cancer cells. Epigenetics 1: 163-171, 2006.
49. Howie GJ, Sloboda DM, Kamal T, and Vickers MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol 587: 905-915, 2009.
50. Hracsko Z, Orvos H, Novak Z, Pal A, and Varga IS. Evaluation of oxidative stress markers in neonates with intra-uterine growth retardation. Redox Rep 13: 11-16, 2008. (Pubitemid 351524326)
51. Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchen MR, and McConnell J. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 5: e10074, 2010.
52. Jansson T and Powell TL. Role of the placenta in fetal programming: underlying mechanisms and potential interventional approaches. Clin Sci (Lond) 113: 1-13, 2007. (Pubitemid 47066020)
53. Jauniaux E, Gulbis B, and Burton GJ. The human first trimester gestational sac limits rather than facilitates oxygen transfer to the foetus-a review. Placenta 24 Suppl A: S86-S93, 2003. (Pubitemid 37184740)
54. Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, and Burton GJ. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 157: 2111-2122, 2000.
55. Jones HN, Woollett LA, Barbour N, Prasad PD, Powell TL, and Jansson T. High-fat diet before and during pregnancy causes marked up-regulation of placental nutrient transport and fetal overgrowth in C57/BL6 mice. FASEB J 23: 271-278, 2009.
56. Jones ML, Mark PJ, Lewis JL, Mori TA, Keelan JA, and Waddell BJ. Antioxidant defenses in the rat placenta in late gestation: increased labyrinthine expression of superoxide dismutases, glutathione peroxidase 3, and uncoupling protein 2. Biol Reprod 83: 254-260, 2010.
57. Kabuto H, Amakawa M, and Shishibori T. Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice. Life Sci 74: 2931-2940, 2004. (Pubitemid 38402291)
58. Kabuto H, Hasuike S, Minagawa N, and Shishibori T. Effects of bisphenol A on the metabolisms of active oxygen species in mouse tissues. Environ Res 93: 31-35, 2003. (Pubitemid 36809222)
59. Kauma S, Takacs P, Scordalakes C, Walsh S, Green K, and Peng T. Increased endothelial monocyte chemoattractant protein-1 and interleukin-8 in preeclampsia. Obstet Gynecol 100: 706-714, 2002. (Pubitemid 35300027)
60. Kim H, Hwang JY, Ha EH, Park H, Ha M, Lee SH, Hong YC, and Chang N. Fruit and vegetable intake influences the association between exposure to polycyclic aromatic hydrocarbons and a marker of oxidative stress in pregnant women. Eur J Clin Nutr 65: 1118-1125, 2011.
61. Korteweg FJ, Gordijn SJ, Timmer A, Holm JP, Ravise JM, and Erwich JJ. A placental cause of intra-uterine fetal death depends on the perinatal mortality classification system used. Placenta 29: 71-80, 2008.
62. Kouzarides T. Chromatin modifications and their function. Cell 128: 693-705, 2007. (Pubitemid 46273577)
63. Kovacic P and Somanathan R. Integrated approach to immunotoxicity: electron transfer, reactive oxygen species, antioxidants, cell signaling, and receptors. J Recept Signal Transduct Res 28: 323-346, 2008.
64. Kumari AS. Pregnancy outcome in women with morbid obesity. Int J Gynaecol Obstet 73: 101-107, 2001. (Pubitemid 32396397)
65. Lapointe J and Bilodeau JF. Antioxidant defenses are modulated in the cow oviduct during the estrous cycle. Biol Reprod 68: 1157-1164, 2003. (Pubitemid 36361992)
66. Laukkanen MO, Mannermaa S, Hiltunen MO, Aittomaki S, Airenne K, Janne J, and Yla-Herttuala S. Local hypomethylation in atherosclerosis found in rabbit ec-sod gene. Arterioscler Thromb Vasc Biol 19: 2171-2178, 1999. (Pubitemid 29422250)
67. Liang C, Decourcy K, and Prater MR. High-saturated-fat diet induces gestational diabetes and placental vasculopathy in C57BL/6 mice. Metabolism 59: 943-950, 2010.
68. Liang C, Oest ME, Jones JC, and Prater MR. Gestational high saturated fat diet alters C57BL/6 mouse perinatal skeletal formation. Birth Defects Res B Dev Reprod Toxicol 86: 362-369, 2009.
69. Liang P, Song F, Ghosh S, Morien E, Qin M, Mahmood S, Fujiwara K, Igarashi J, Nagase H, and Held WA. Genomewide survey reveals dynamic widespread tissue-specific changes in DNA methylation during development. BMC Genomics 12: 231, 2011.
70. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, and Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135: 1382-1386, 2005. (Pubitemid 40799599)
71. Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, and Burdge GC. Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr 100: 278-282, 2008.
72. Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, and Burdge GC. Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 97: 1064-1073, 2007. (Pubitemid 46925358)
73. Lin Y, Han XF, Fang ZF, Che LQ, Nelson J, Yan TH, and Wu D. Beneficial effects of dietary fibre supplementation of a high-fat diet on fetal development in rats. Br J Nutr 106: 510-518, 2011.
74. Mackenzie GG, Salvador GA, Romero C, Keen CL, and Oteiza PI. A deficit in zinc availability can cause alterations in tubulin thiol redox status in cultured neurons and in the developing fetal rat brain. Free Radic Biol Med 51: 480-489, 2011.
75. Madazli R, Benian A, Aydin S, Uzun H, and Tolun N. The plasma and placental levels of malondialdehyde, glutathione and superoxide dismutase in pre-eclampsia. J Obstet Gynaecol 22: 477-480, 2002. (Pubitemid 35222856)
76. Mahn K, Borras C, Knock GA, Taylor P, Khan IY, Sugden D, Poston L, Ward JP, Sharpe RM, Vina J, Aaronson PI, and Mann GE. Dietary soy isoflavone induced increases in antioxidant and eNOS gene expression lead to improved endothelial function and reduced blood pressure in vivo. FASEB J 19: 1755-1757, 2005. (Pubitemid 41429553)
77. Margueron R and Reinberg D. Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11: 285-296, 2010.
78. Martin-Gallan P, Carrascosa A, Gussinye M, and Dominguez C. Biomarkers of diabetes-associated oxidative stress and antioxidant status in young diabetic patients with or without subclinical complications. Free Radic Biol Med 34: 1563-1574, 2003. (Pubitemid 36638716)
79. Maunakea AK, Chepelev I, and Zhao K. Epigenome mapping in normal and disease States. Circ Res 107: 327-339, 2010.
80. McCurdy CE, Bishop JM, Williams SM, Grayson BE, Smith MS, Friedman JE, and Grove KL. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest 119: 323-335, 2009.
81. Menon R, Fortunato SJ, Yu J, Milne GL, Sanchez S, Drobek CO, Lappas M, and Taylor RN. Cigarette smoke induces oxidative stress and apoptosis in normal term fetal membranes. Placenta 32: 317-322, 2011.
82. Metges CC. Early nutrition and later obesity: animal models provide insights into mechanisms. Adv Exp Med Biol 646: 105-112, 2009.
83. Millar DS, Ow KK, Paul CL, Russell PJ, Molloy PL, and Clark SJ. Detailed methylation analysis of the glutathione S-transferase pi (GSTP1) gene in prostate cancer. Oncogene 18: 1313-1324, 1999. (Pubitemid 29094883)
84. Mise H, Sagawa N, Matsumoto T, Yura S, Nanno H, Itoh H, Mori T, Masuzaki H, Hosoda K, Ogawa Y, and Nakao K. Augmented placental production of leptin in preeclampsia: possible involvement of placental hypoxia. J Clin Endocrinol Metab 83: 3225-3229, 1998. (Pubitemid 28500963)
85. Murr R. Interplay between different epigenetic modifications and mechanisms. Adv Genet 70: 101-141, 2010.
86. Myllynen P, Pasanen M, and Pelkonen O. Human placenta: a human organ for developmental toxicology research and biomonitoring. Placenta 26: 361-371, 2005. (Pubitemid 40567913)
87. Nakayama M, Bennett CJ, Hicks JL, Epstein JI, Platz EA, Nelson WG, and De Marzo AM. Hypermethylation of the human glutathione S-transferase-pi gene (GSTP1) CpG island is present in a subset of proliferative inflammatory atrophy lesions but not in normal or hyperplastic epithelium of the prostate: a detailed study using laser-capture microdissection. Am J Pathol 163: 923-933, 2003. (Pubitemid 37040128)
88. Ojeda ML, Nogales F, Jotty K, Barrero MJ, Murillo ML, and Carreras O. Dietary selenium plus folic acid as an antioxidant therapy for ethanol-exposed pups. Birth Defects Res B Dev Reprod Toxicol 86: 490-495, 2009.
89. Olsson MG, Centlow M, Rutardottir S, Stenfors I, Larsson J, Hosseini-Maaf B, Olsson ML, Hansson SR, and Akerstrom B. Increased levels of cell-free hemoglobin, oxidation markers, and the antioxidative heme scavenger alpha(1)-microglobulin in preeclampsia. Free Radic Biol Med 48: 284-291, 2010.
90. Ornoy A. Embryonic oxidative stress as a mechanism of teratogenesis with special emphasis on diabetic embryopathy. Reprod Toxicol 24: 31-41, 2007. (Pubitemid 47042350)
91. Ouyang YQ, Li SJ, Zhang Q, Cai HB, and Chen HP. Interactions between inflammatory and oxidative stress in preeclampsia. Hypertens Pregnancy 28: 56-62, 2009.
92. Perera FP, Rauh V, Whyatt RM, Tsai WY, Tang D, Diaz D, Hoepner L, Barr D, Tu YH, Camann D, and Kinney P. Effect of prenatal exposure to airborne polycyclic aromatic hydrocarbons on neurodevelopment in the first 3 years of life among inner-city children. Environ Health Perspect 114: 1287-1292, 2006. (Pubitemid 44184692)
93. Perrotta I, Brunelli E, Sciangula A, Zuccala V, Donato G, Tripepi S, Martinelli GL, and Cassese M. Inducible and endothelial nitric oxide synthase expression in human atherogenesis: an immunohistochemical and ultrastructural study. Cardiovasc Pathol 18: 361-368, 2009.
94. Picciano MF. Pregnancy and lactation: physiological adjustments, nutritional requirements and the role of dietary supplements. J Nutr 133: 1997S-2002S, 2003. (Pubitemid 36666549)
95. Pillai P, Patel R, Pandya C, and Gupta S. Sex-specific effects of gestational and lactational coexposure to lead and cadmium on hepatic phase I and phase II xenobiotic/steroidmetabolizing enzymes and antioxidant status. J Biochem Mol Toxicol 23: 419-431, 2009.
96. Polanska K, Hanke W, Sobala W, Brzeznicki S, and Ligocka D. Exposure to polycyclic aromatic hydrocarbons and newborn biometric indicators. Int J Occup Med Environ Health 23: 339-346, 2010.
97. Rodford JL, Torrens C, Siow RC, Mann GE, Hanson MA, and Clough GF. Endothelial dysfunction and reduced antioxidant protection in an animal model of the developmental origins of cardiovascular disease. J Physiol 586: 4709-4720, 2008.
98. Ross AE, Marchionni L, Phillips TM, Miller RM, Hurley PJ, Simons BW, Salmasi AH, Schaeffer AJ, Gearhart JP, and Schaeffer EM. Molecular effects of genistein on male urethral development. J Urol 185: 1894-1898, 2011.
99. Sagol S, Ozkinay E, and Ozsener S. Impaired antioxidant activity in women with pre-eclampsia. Int J Gynaecol Obstet 64: 121-127, 1999. (Pubitemid 29096268)
100. Saker M, Soulimane Mokhtari N, Merzouk SA, Merzouk H, Belarbi B, and Narce M. Oxidant and antioxidant status in mothers and their newborns according to birthweight. Eur J Obstet Gynecol Reprod Biol 141: 95-99, 2008.
101. Salmasi G, Grady R, Jones J, and McDonald SD. Environmental tobacco smoke exposure and perinatal outcomes: a systematic review and meta-analyses. Acta Obstet Gynecol Scand 89: 423-441, 2010.
102. Sebire NJ, Jolly M, Harris JP, Wadsworth J, Joffe M, Beard RW, Regan L, and Robinson S. Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. Int J Obes Relat Metab Disord 25: 1175-1182, 2001. (Pubitemid 32721540)
103. Sen S and Simmons RA. Maternal antioxidant supplementation prevents adiposity in the offspring of Western diet-fed rats. Diabetes 59: 3058-3065, 2010.
104. Sharif J, Nakamura M, Ito T, Kimura Y, Nagamune T, Mitsuya K, and Okamura K. Food restriction in pregnant mice can induce changes in histone modifications and suppress gene expression in fetus. Nucleic Acids Symp Ser (Oxf): 125-126, 2007.
105. Sikkema JM, van Rijn BB, Franx A, Bruinse HW, de Roos R, Stroes ES, and van Faassen EE. Placental superoxide is increased in pre-eclampsia. Placenta 22: 304-308, 2001. (Pubitemid 32537052)
106. Siow RC and Mann GE. Dietary isoflavones and vascular protection: activation of cellular antioxidant defenses by SERMs or hormesis? Mol Aspects Med 31: 468-477, 2010.
107. Sohal RS, Allen RG, and Nations C. Oxidative stress and cellular differentiation. Ann N Y Acad Sci 551: 59-73;discussion 74, 1988.
108. Steegers EA, von Dadelszen P, Duvekot JJ, and Pijnenborg R. Pre-eclampsia. Lancet 376: 631-644, 2010.
109. Strakovsky RS, Zhang X, Zhou D, and Pan YX. Gestational high fat diet programs hepatic phosphoenolpyruvate carboxykinase (Pck) expression and histone modification in neonatal offspring rats. J Physiol 589 (Pt 11): 2707-2717, 2011.
110. Straussman R, Nejman D, Roberts D, Steinfeld I, Blum B, Benvenisty N, Simon I, Yakhini Z, and Cedar H. Developmental programming of CpG island methylation profiles in the human genome.Nat Struct Mol Biol 16: 564-571, 2009.
111. Suganuma H, Arai Y, Kitamura Y, Hayashi M, Okumura A, and Shimizu T. Maternal docosahexaenoic acid-enriched diet prevents neonatal brain injury. Neuropathology 30: 597-605, 2010.
112. Sugino N, Takiguchi S, Kashida S, Karube A, Nakamura Y, and Kato H. Superoxide dismutase expression in the human corpus luteum during the menstrual cycle and in early pregnancy. Mol Hum Reprod 6: 19-25, 2000. (Pubitemid 30043584)
113. Suter M, Bocock P, Showalter L, Hu M, Shope C, McKnight R, Grove K, Lane R, and Aagaard-Tillery K. Epigenomics: maternal high-fat diet exposure in utero disrupts peripheral circadian gene expression in nonhuman primates. FASEB J 25: 714-726, 2011.
114. Takagi Y, Nikaido T, Toki T, Kita N, Kanai M, Ashida T, Ohira S, and Konishi I. Levels of oxidative stress and redoxrelated molecules in the placenta in preeclampsia and fetal growth restriction. Virchows Arch 444: 49-55, 2004. (Pubitemid 38200090)
115. Takehara Y, Yoshioka T, and Sasaki J. Changes in the levels of lipoperoxide and antioxidant factors in human placenta during gestation. Acta Med Okayama 44: 103-111, 1990. (Pubitemid 20328847)
116. Takiguchi S, Sugino N, Kashida S, Yamagata Y, Nakamura Y, and Kato H. Rescue of the corpus luteum and an increase in luteal superoxide dismutase expression induced by placental luteotropins in the rat: action of testosterone without conversion to estrogen. Biol Reprod 62: 398-403, 2000. (Pubitemid 30067342)
117. Tarry-Adkins JL, Chen JH, Jones RH, Smith NH, and Ozanne SE. Poor maternal nutrition leads to alterations in oxidative stress, antioxidant defense capacity, and markers of fibrosis in rat islets: potential underlying mechanisms for development of the diabetic phenotype in later life. FASEB J 24: 2762-2771, 2010.
118. Tarry-Adkins JL, Martin-Gronert MS, Chen JH, Cripps RL, and Ozanne SE. Maternal diet influences DNA damage, aortic telomere length, oxidative stress, and antioxidant defense capacity in rats. FASEB J 22: 2037-2044, 2008. (Pubitemid 351811479)
119. Thaler R, Karlic H, Rust P, and Haslberger AG. Epigenetic regulation of human buccal mucosa mitochondrial superoxide dismutase gene expression by diet. Br J Nutr 101: 743-749, 2009.
120. Theys N, Clippe A, Bouckenooghe T, Reusens B, and Remacle C. Early low protein diet aggravates unbalance between antioxidant enzymes leading to islet dysfunction. PLoS One 4: e6110, 2009.
121. Tomat AL, Inserra F, Veiras L, Vallone MC, Balaszczuk AM, Costa MA, and Arranz C. Moderate zinc restriction during fetal and postnatal growth of rats: effects on adult arterial blood pressure and kidney. Am J Physiol Regul Integr Comp Physiol 295: R543-R549, 2008.
122. Tosh DN, Fu Q, Callaway CW, McKnight RA, McMillen IC, Ross MG, Lane RH, and Desai M. Epigenetics of programmed obesity: alteration in IUGR rat hepatic IGF1 mRNA expression and histone structure in rapid versus delayed postnatal catch-up growth. Am J Physiol Gastrointest Liver Physiol 299: G1023-G1029, 2010.
123. Trocino RA, Akazawa S, Ishibashi M, Matsumoto K, Matsuo H, Yamamoto H, Goto S, Urata Y, Kondo T, and Nagataki S. Significance of glutathione depletion and oxidative stress in early embryogenesis in glucose-induced rat embryo culture. Diabetes 44: 992-998, 1995.
124. Tsukimori K, Yoshitomi T, Morokuma S, Fukushima K, and Wake N. Serum uric acid levels correlate with plasma hydrogen peroxide and protein carbonyl levels in preeclampsia. Am J Hypertens 21: 1343-1346, 2008.
125. Valko M, Izakovic M, Mazur M, Rhodes CJ, and Telser J. Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 266: 37-56, 2004. (Pubitemid 39562306)
126. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, and Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39: 44-84, 2007. (Pubitemid 44566469)
127. Vanaja DK, Ehrich M, Van den Boom D, Cheville JC, Karnes RJ, Tindall DJ, Cantor CR, and Young CY. Hypermethylation of genes for diagnosis and risk stratification of prostate cancer. Cancer Invest 27: 549-560, 2009.
128. Votavova H, Dostalova Merkerova M, Fejglova K, Vasikova A, Krejcik Z, Pastorkova A, Tabashidze N, Topinka J, Veleminsky M, Jr., Sram RJ, and Brdicka R. Transcriptome alterations in maternal and fetal cells induced by tobacco smoke. Placenta 32: 763-770, 2011.
129. Vucetic Z, Kimmel J, Totoki K, Hollenbeck E, and Reyes TM. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151: 4756-4764, 2010.
130. Warren AY, Matharoo-Ball B, Shaw RW, and Khan RN. Hydrogen peroxide and superoxide anion modulate pregnant human myometrial contractility. Reproduction 130: 539-544, 2005. (Pubitemid 41472479)
131. Waterland RA, Travisano M, Tahiliani KG, Rached MT, and Mirza S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond) 32: 1373-1379, 2008.
132. Wolff GL, Kodell RL, Moore SR, and Cooney CA. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 12: 949-957, 1998. (Pubitemid 28359576)
133. Xiao D, Huang X, Yang S, and Zhang L. Antenatal nicotine induces heightened oxidative stress and vascular dysfunction in rat offspring. Br J Pharmacol 164: 1400-1409, 2011.
134. Zabihi S and Loeken MR. Understanding diabetic teratogenesis: where are we now and where are we going? Birth Defects Res A Clin Mol Teratol 88: 779-790, 2010.
135. Zhang X, Strakovsky RS, Zhou D, Zhang Y, and Pan YX. A maternal high-fat diet represses the expression of antioxidant defense genes and induces the cellular senescence pathway in the liver of male offspring rats. J Nutr 141: 1254-1259, 2011.
136. Zhao L, Chen YH, Wang H, Ji YL, Ning H, Wang SF, Zhang C, Lu JW, Duan ZH, and Xu DX. Reactive oxygen species contribute to lipopolysaccharide-induced teratogenesis in mice. Toxicol Sci 103: 149-157, 2008. (Pubitemid 351524486)
137. Zheng S and Pan YX. Histone modifications, not DNA methylation, cause transcriptional repression of p16 (CDKN2A) in the mammary glands of offspring of proteinrestricted rats. J Nutr Biochem 22: 567-573, 2011.
138. Zheng S, Rollet M, and Pan YX. Maternal protein restriction during pregnancy induces CCAAT/enhancer-binding protein (C/EBPbeta) expression through the regulation of histone modification at its promoter region in female offspring rat skeletal muscle. Epigenetics 6: 161-170, 2011.
139. Ziech D, Franco R, Pappa A, and Panayiotidis MI. Reactive Oxygen Species (ROS)-Induced genetic and epigenetic alterations in human carcinogenesis. Mutat Res 711: 167-173, 2011.
140. Zusterzeel PL, Rutten H, Roelofs HM, Peters WH, and Steegers EA. Protein carbonyls in decidua and placenta of pre-eclamptic women as markers for oxidative stress. Placenta 22: 213-219, 2001. (Pubitemid 32537039)