Impact of oxidative stress in fetal programming

Journal of Pregnancy

Volumn 2012, Issue , 2012, Pages

  Thompson, Loren P ^a   Al Hasan, Yazan ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; REACTIVE OXYGEN METABOLITE;

FEMALE; FETUS DEVELOPMENT; FETUS HYPOXIA; GENETIC EPIGENESIS; GENETICS; HUMAN; MATERNAL NUTRITION; METABOLISM; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; REVIEW;

BIOLOGICAL MARKERS; EPIGENESIS, GENETIC; FEMALE; FETAL DEVELOPMENT; FETAL HYPOXIA; HUMANS; OXIDATIVE STRESS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; REACTIVE OXYGEN SPECIES;

EID: 84866246324     PISSN: 20902727     EISSN: 20902735     Source Type: Journal    
DOI: 10.1155/2012/582748     Document Type: Review

References (109)

1. Burton G. J., Oxygen, the Janus gas; its effects on human placental development and function. Journal of Anatomy 2009 215 1 27 35 2-s2.0-67449127564 10.1111/j.1469-7580.2008.00978.x
2. Symonds M. E., Stephenson T., Gardner D. S., Budge H., Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows. Reproduction, Fertility and Development 2007 19 1 53 63 2-s2.0-33846011358 10.1071/RD06130 (Pubitemid 46044731)
3. Herrera E. A., Kane A. D., Hansell J. A., A role for xanthine oxidase in the control of fetal cardiovascular function in late gestation sheep. Journal of Physiology 2012 590 8 1825 1837
4. Thakor A. S., Richter H. G., Kane A. D., Dunster C., Kelly F. J., Poston L., Giussani D. A., Redox modulation of the fetal cardiovascular defence to hypoxaemia. Journal of Physiology 2010 588 21 4235 4247 2-s2.0-78049460045 10.1113/jphysiol.2010.196402
5. Thakor A. S., Herrera E. A., Serón-Ferré M., Giussani D. A., Melatonin and vitamin C increase umbilical blood flow via nitric oxide-dependent mechanisms. Journal of Pineal Research 2010 49 4 399 406 2-s2.0-78349249373 10.1111/j.1600-079X.2010.00813.x
6. Hanson M. A., Gluckman P. D., Developmental origins of health and disease: new insights. Basic and Clinical Pharmacology and Toxicology 2008 102 2 90 93 2-s2.0-38449116576 10.1111/j.1742-7843.2007.00186.x (Pubitemid 351143434)
7. Nuyt A. M., Alexander B. T., Developmental programming and hypertension. Current Opinion in Nephrology and Hypertension 2009 18 2 144 152 10.1097/MNH.0b013e328326092c
8. Nesterenko T. H., Aly H., Fetal and neonatal programming: evidence and clinical implications. American Journal of Perinatology 2009 26 3 191 198 2-s2.0-61449267584 10.1055/s-0028-1103027
9. Barnes S. K., Ozanne S. E., Pathways linking the early environment to long-term health and lifespan. Progress in Biophysics and Molecular Biology 2011 106 1 323 336 2-s2.0-79958015940 10.1016/j.pbiomolbio.2010.12.005
10. Barker D. J. P., Osmond C., Golding J., Kuh D., Wadsworth M. E. J., Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. British Medical Journal 1989 298 6673 564 567 2-s2.0-0024542325 (Pubitemid 19072097)
11. Barker D. J. P., Osmond C., Simmonds S. J., Wield G. A., The relation of small head circumference and thinness at birth to death from cardiovascular disease in adult life. British Medical Journal 1993 306 6875 422 426 2-s2.0-0027476835 (Pubitemid 23045550)
12. Osmond C., Barker D. J. P., Winter P. D., Fall C. H. D., Simmonds S. J., Early growth and death from cardiovascular disease in women. British Medical Journal 1993 307 6918 1519 1524 2-s2.0-0027484614 (Pubitemid 23357224)
13. Barker D. J. P., Bull A. R., Osmond C., Simmonds S. J., Fetal and placental size and risk of hypertension in adult life. British Medical Journal 1990 301 6746 259 262 2-s2.0-0025297450 (Pubitemid 20241224)
14. Eriksson J. G., Forsén T., Tuomilehto J., Jaddoe V. W. V., Osmond C., Barker D. J. P., Effects of size at birth and childhood growth on the insulin resistance syndrome in elderly individuals. Diabetologia 2002 45 3 342 348 2-s2.0-0036210553 10.1007/s00125-001-0757-6 (Pubitemid 34267356)
15. Eriksson J. G., Forsen T. J., Osmond C., Barker D. J. P., Pathways of infant and childhood growth that lead to type 2 diabetes. Diabetes Care 2003 26 11 3006 3010 2-s2.0-0242363747 10.2337/diacare.26.11.3006 (Pubitemid 37339490)
16. Curhan G. C., Willett W. C., Rimm E. B., Spiegelman D., Ascherio A. L., Stampfer M. J., Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation 1996 94 12 3246 3250 2-s2.0-0030481473 (Pubitemid 26427494)
17. Curhan G. C., Chertow G. M., Willett W. C., Spiegelman D., Colditz G. A., Manson J. E., Speizer F. E., Stampfer M. J., Birth weight and adult hypertension and obesity in women. Circulation 1996 94 6 1310 1315 2-s2.0-0029794571 (Pubitemid 26307258)
18. Hales C. N., Barker D. J. P., The thrifty phenotype hypothesis. British Medical Bulletin 2001 60 5 20 2-s2.0-0035704552 10.1093/bmb/60.1.5 (Pubitemid 34123501)
19. Gluckman P. D., Hanson M. A., Spencer H. G., Predictive adaptive responses and human evolution. Trends in Ecology and Evolution 2005 20 10 527 533 2-s2.0-24944487171 10.1016/j.tree.2005.08.001 (Pubitemid 41323708)
20. Hay W. W. Jr., Strategies for feeding the preterm infant. Neonatology 2008 94 4 245 254 2-s2.0-53049107637 10.1159/000151643
21. Barker D. J. P., Osmond C., Forsén T. J., Kajantie E., Eriksson J. G., Trajectories of growth among children who have coronary events as adults. The New England Journal of Medicine 2005 353 17 1802 1809 2-s2.0-27244457374 10.1056/NEJMoa044160 (Pubitemid 41549892)
22. Dennery P. A., Oxidative stress in development: nature or nurture? Free Radical Biology and Medicine 2010 49 7 1147 1151 2-s2.0-77956176210 10.1016/j.freeradbiomed.2010.07.011
23. Hitchler M. J., Domann F. E., An epigenetic perspective on the free radical theory of development. Free Radical Biology and Medicine 2007 43 7 1023 1036 2-s2.0-34548140496 10.1016/j.freeradbiomed.2007.06.027 (Pubitemid 47302657)
24. Schafer F. Q., Buettner G. R., Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radical Biology and Medicine 2001 30 11 1191 1212 2-s2.0-0035371184 10.1016/S0891-5849(01)00480-4 (Pubitemid 32463931)
25. Castagné V., Lefèvre K., Natero R., Becker D. A., Clarke P. G. H., An optimal redox status for the survival of axotomized ganglion cells in the developing retina. Neuroscience 1999 93 1 313 320 2-s2.0-0344915166 10.1016/S0306-4522(99)00138-4 (Pubitemid 29290711)
26. Giussani D. A., Salinas C. E., Villena M., Blanco C. E., The role of oxygen in prenatal growth: studies in the chick embryo. Journal of Physiology 2007 585 3 911 917 2-s2.0-37249023025 10.1113/jphysiol.2007.141572 (Pubitemid 350278724)
27. Myatt L., Review: reactive oxygen and nitrogen species and functional adaptation of the placenta. Placenta 2010 31 S66 S69 2-s2.0-76749110706 10.1016/j.placenta.2009.12.021
28. Roberts J. M., Lain K. Y., Recent insights into the pathogenesis of pre-eclampsia. Placenta 2002 23 5 359 372 2-s2.0-0036579918 10.1053/plac.2002. 0819 (Pubitemid 41110499)
29. Moore L. G., Human genetic adaptation to high altitude. High Altitude Medicine and Biology 2001 2 2 257 279 2-s2.0-0034913630 10.1089/ 152702901750265341 (Pubitemid 32677861)
30. Giussani D. A., Phillips P. S., Anstee S., Barker D. J. P., Effects of altitude versus economic status on birth weight and body shape at birth. Pediatric Research 2001 49 4 490 494 2-s2.0-0035069341 (Pubitemid 32274961)
31. Niermeyer S., Mollinedo P. A., Huicho L., Child health and living at high altitude. Archives of Disease in Childhood 2009 94 10 806 811 2-s2.0-70349392876 10.1136/adc.2008.141838
32. Julian C. G., Wilson M. J., Moore L. G., Evolutionary adaptation to high altitude: a view from in utero. American Journal of Human Biology 2009 21 5 614 622 2-s2.0-70350714142 10.1002/ajhb.20900
33. Zamudio S., High-altitude hypoxia and preeclampsia. Frontiers in Bioscience 2007 12 8 2967 2977 2-s2.0-34347262653 10.2741/2286
34. Li Y., Gonzalez P., Zhang L., Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: mechanisms and possible interventions. Progress in Neurobiology 2012 98 2 145 165 10.1016/j.pneurobio.2012.05.010
35. Camm E. J., Hansell J. A., Kane A. D., Herrera E. A., Lewis C., Wong S., Morrell N. W., Giussani D. A., Partial contributions of developmental hypoxia and undernutrition to prenatal alterations in somatic growth and cardiovascular structure and function. American Journal of Obstetrics and Gynecology 2010 203 5 495.e24 495.e34 2-s2.0-78149284735 10.1016/j.ajog.2010.06.046
36. Giussani D. A., Camm E. J., Niu Y., Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS ONE 2012 7 2 e31017
37. Morrison J. L., Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clinical and Experimental Pharmacology and Physiology 2008 35 7 730 743 2-s2.0-44249097830 10.1111/j.1440-1681.2008.04975.x (Pubitemid 351725247)
38. Dong Y., Yu Z., Sun Y., Zhou H., Stites J., Newell K., Weiner C. P., Chronic fetal hypoxia produces selective brain injury associated with altered nitric oxide synthases. American Journal of Obstetrics and Gynecology 2011 204 3 254e16 254e28 2-s2.0-79952312039 10.1016/j.ajog.2010.11.032
39. Guo R., Hou W., Dong Y., Yu Z., Stites J., Weiner C. P., Brain injury caused by chronic fetal hypoxemia is mediated by inflammatory cascade activation. Reproductive Sciences 2010 17 6 540 548 2-s2.0-77952380587 10.1177/1933719110364061
40. Gunn A. J., Bennet L., Fetal hypoxia insults and patterns of brain injury: insights from animal models. Clinics in Perinatology 2009 36 3 579 593 2-s2.0-69249249242 10.1016/j.clp.2009.06.007
41. Zhang L., Prenatal hypoxia and cardiac programming. Journal of the Society for Gynecologic Investigation 2005 12 1 2 13 2-s2.0-11144288674 10.1016/j.jsgi.2004.09.004 (Pubitemid 40039057)
42. Thompson L. P., Dong Y., Chronic hypoxia decreases endothelial nitric oxide synthase protein expression in fetal guinea pig hearts. Journal of the Society for Gynecologic Investigation 2005 12 6 388 395 2-s2.0-24144463996 10.1016/j.jsgi.2005.04.011 (Pubitemid 41242376)
43. Evans L. C., Liu H., Pinkas G. A., Thompson L. P., Chronic hypoxia increases peroxynitrite, MMP9 expression, and collagen accumulation in fetal guinea pig hearts. Pediatric Research 2012 71 1 25 31 10.1038/pr.2011.10
44. Dong Y., Thompson L. P., Differential expression of endothelial nitric oxide synthase in coronary and cardiac tissue in hypoxic fetal guinea pig hearts. Journal of the Society for Gynecologic Investigation 2006 13 7 483 490 2-s2.0-33749506409 10.1016/j.jsgi.2006.06.005 (Pubitemid 44528298)
45. Hashimoto K., Pinkas G., Evans L., Liu H., Al-Hasan Y., Thompson L. P., Protective effect of N-acetylcysteine on liver damage during chronic intrauterine hypoxia in fetal guinea pig. Reproductive Sciences. In press 10.1177/1933719112440052
46. Rueda-Clausen C. F., Dolinsky V. W., Morton J. S., Proctor S. D., Dyck J. R. B., Davidge S. T., Hypoxia-induced intrauterine growth restriction increases the susceptibility of rats to high-fat diet-induced metabolic syndrome. Diabetes 2011 60 2 507 516 2-s2.0-79551574617 10.2337/db10-1239
47. Camm E. J., Martin-Gronert M. S., Wright N. L., Hansell J. A., Ozanne S. E., Giussani D. A., Prenatal hypoxia independent of undernutrition promotes molecular markers of insulin resistance in adult offspring. FASEB Journal 2011 25 1 420 427 2-s2.0-79251581849 10.1096/fj.10-158188
48. 2 receptors and structures in ovine fetuses following exposure to long-term hypoxia. American Journal of Nephrology 2010 31 2 141 150 2-s2.0-70449644971 10.1159/000259901
49. Rueda-Clausen C. F., Morton J. S., Lopaschuk G. D., Davidge S. T., Long-term effects of intrauterine growth restriction on cardiac metabolism and susceptibility to ischaemia/reperfusion. Cardiovascular Research 2011 90 2 285 294 2-s2.0-79955419125 10.1093/cvr/cvq363
50. Rueda-Clausen C. F., Morton J. S., Davidge S. T., Effects of hypoxia-induced intrauterine growth restriction on cardiopulmonary structure and function during adulthood. Cardiovascular Research 2009 81 4 713 722 2-s2.0-60149093704 10.1093/cvr/cvn341
51. Morton J. S., Rueda-Clausen C. F., Davidge S. T., Flow-mediated vasodilation is impaired in adult rat offspring exposed to prenatal hypoxia. Journal of Applied Physiology 2011 110 4 1073 1082 2-s2.0-79954596945 10.1152/japplphysiol.01174.2010
52. Morton J. S., Rueda-Clausen C. F., Davidge S. T., Mechanisms of endothelium-dependent vasodilation in male and female, young and aged offspring born growth restricted. American Journal of Physiology 2010 298 4 R930 R938 2-s2.0-77949805966 10.1152/ajpregu.00641.2009
53. Hemmings D. G., Williams S. J., Davidge S. T., Increased myogenic tone in 7-month-old adult male but not female offspring from rat dams exposed to hypoxia during pregnancy. American Journal of Physiology 2005 289 2 H674 H682 2-s2.0-23744437999 10.1152/ajpheart.00191.2005 (Pubitemid 41129383)
54. 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? Medical Hypotheses 2006 66 1 38 44 2-s2.0-27744479813 10.1016/j.mehy.2005.08.020 (Pubitemid 41605102)
55. Shao D., Oka S. I., Brady C. D., Haendeler J., Eaton P., Sadoshima J., Redox modification of cell signaling in the cardiovascular system. Journal of Molecular and Cellular Cardiology 2012 52 3 550 558 10.1016/j.yjmcc.2011.09.009
56. Cadenas S., Aragonés J., Landázuri M. O., Mitochondrial reprogramming through cardiac oxygen sensors in ischaemic heart disease. Cardiovascular Research 2010 88 2 219 228 2-s2.0-77956605222 10.1093/cvr/cvq256
57. Semenza G. L., Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochemical Journal 2007 405 1 1 9 2-s2.0-34347227058 10.1042/BJ20070389 (Pubitemid 46999919)
58. Droge W., Free radicals in the physiological control of cell function. Physiological Reviews 2002 82 47 95 (Pubitemid 34654215)
59. Ziech D., Franco R., Pappa A., Panayiotidis M. I., Reactive Oxygen Species (ROS)Induced genetic and epigenetic alterations in human carcinogenesis. Mutation Research 2011 711 1-2 167 173 2-s2.0-79956196320 10.1016/j.mrfmmm. 2011.02.015
60. Aon M. A., Cortassa S., Akar F. G., O'Rourke B., Mitochondrial criticality: a new concept at the turning point of life or death. Biochimica et Biophysica Acta 2006 1762 2 232 240 2-s2.0-29344465712 10.1016/j.bbadis.2005.06. 008 (Pubitemid 43006029)
61. Cerda S., Weitzman S. A., Influence of oxygen radical injury on DNA methylation. Mutation Research 1997 386 2 141 152 2-s2.0-0031000977 10.1016/S1383-5742(96)00050-6 (Pubitemid 27195019)
62. Singhal A., Lucas A., Early origins of cardiovascular disease: is there a unifying hypothesis? The Lancet 2004 363 9421 1642 1645 2-s2.0-2442479898 10.1016/S0140-6736(04)16210-7 (Pubitemid 38625670)
63. Peuchant E., Brun J. L., Rigalleau V., Dubourg L., Thomas M. J., Daniel J. Y., Leng J. J., Gin H., Oxidative and antioxidative status in pregnant women with either gestational or type 1 diabetes. Clinical Biochemistry 2004 37 4 293 298 2-s2.0-1542316294 10.1016/j.clinbiochem.2003.12.005 (Pubitemid 38314883)
64. Bloc G., Dietrich M., Norkus E. P., Factors associated with oxidative stress in human populations. American Journal of Epidemiology 2002 156 274 285 10.1093/aje/kwf029 (Pubitemid 34810481)
65. Mohn A., Chiavaroli V., Cerruto M., Blasetti A., Giannini C., Bucciarelli T., Chiarelli F., Increased oxidative stress in prepubertal children born small for gestational age. Journal of Clinical Endocrinology and Metabolism 2007 92 4 1372 1378 2-s2.0-34147180719 10.1210/jc.2006-1344 (Pubitemid 46556412)
66. Franco M. C. P., Kawamoto E. M., Gorjão R., Rastelli V. M. F., Curi R., Scavone C., Sawaya A. L., Fortes Z. B., Sesso R., Biomarkers of oxidative stress and antioxidant status in children born small for gestational age: evidence of lipid peroxidation. Pediatric Research 2007 62 2 204 208 2-s2.0-34547625004 10.1203/PDR.0b013e3180986d04 (Pubitemid 47205724)
67. Chiavaroli V., Giannini C., D'Adamo E., De Giorgis T., Chiarelli F., Mohn A., Insulin resistance and oxidative stress in children born small and large for gestational age. Pediatrics 2009 124 2 695 702 2-s2.0-67749135430 10.1542/peds.2008-3056
68. Hracsko Z., Orvos H., Novak Z., Pal A., Varga I. S., Evaluation of oxidative stress markers in neonates with intra-uterine growth retardation. Redox Report 2008 13 1 11 16 2-s2.0-41149130724 10.1179/135100008X259097 (Pubitemid 351524326)
69. Bayhan G., Koçyigit Y., Atamer A., Atamer Y., Akkus Z., Potential atherogenic roles of lipids, lipoprotein(a) and lipid peroxidation in preeclampsia. Gynecological Endocrinology 2005 21 1 1 6 2-s2.0-23244461834 10.1080/09513590500097382 (Pubitemid 41097788)
70. Atamer Y., Koçyigit Y., Yokus B., Atamer A., Erden A. C., Lipid peroxidation, antioxidant defense, status of trace metals and leptin levels in preeclampsia. European Journal of Obstetrics Gynecology and Reproductive Biology 2005 119 1 60 66 2-s2.0-14244263052 10.1016/j.ejogrb.2004.06.033 (Pubitemid 40289099)
71. Karowicz-Biliska A., Kowalska-Koprek U., Suzin J., Sieroszewski P., Analysis of 8-isoprostane concentration as a marker of oxidative stress in pregnant women diagnosed with IUGR. Ginekologia Polska 2003 74 10 1137 1142 2-s2.0-1542603172
72. Karowicz-Bilinska A., Kdziora-Kornatowska K., Bartosz G., Indices of oxidative stress in pregnancy with fetal growth restriction. Free Radical Research 2007 41 8 870 873 2-s2.0-34547538537 10.1080/10715760701291647 (Pubitemid 47180673)
73. Biri A., Bozkurt N., Turp A., Kavutcu M., Himmetoglu Ö., Durak I., Role of oxidative stress in intrauterine growth restriction. Gynecologic and Obstetric Investigation 2007 64 4 187 192 2-s2.0-36048970984 10.1159/000106488 (Pubitemid 350099002)
74. Cambonie G., Comte B., Yzydorczyk C., Ntimbane T., Germain N., Lê N. L. O., Pladys P., Gauthier C., Lahaie I., Abran D., Lavoie J. C., Nuyt A. M., Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet. American Journal of Physiology 2007 292 3 R1236 R1245 2-s2.0-33847749929 10.1152/ajpregu.00227.2006 (Pubitemid 46377090)
75. Elmes M. J., Gardner D. S., Langley-Evans S. C., Fetal exposure to a maternal low-protein diet is associated with altered left ventricular pressure response to ischaemia-reperfusion injury. British Journal of Nutrition 2007 98 1 93 100 2-s2.0-34547993682 10.1017/S000711450769182X (Pubitemid 47272151)
76. Roghair R. D., Miller F. J., Scholz T. D., Lamb F. S., Segar J. L., Endothelial superoxide production is altered in sheep programmed by early gestation dexamethasone exposure. Neonatology 2007 93 1 19 27 2-s2.0-37249072735 10.1159/000105521 (Pubitemid 350277289)
77. Von Bergen N. H., Koppenhafer S. L., Spitz D. R., Volk K. A., Patel S. S., Roghair R. D., Lamb F. S., Segar J. L., Scholz T. D., Fetal programming alters reactive oxygen species production in sheep cardiac mitochondria. Clinical Science 2009 116 8 659 668 2-s2.0-66949132569 10.1042/CS20080474
78. Herrera E. A., Verkerk M. M., Derks J. B., Giussani D. A., Antioxidant treatment alters peripheral vascular dysfunction induced by postnatal glucocorticoid therapy in rats. PLoS ONE 2010 5 2 2-s2.0-77949502477 10.1371/journal.pone.0009250 e9250
79. Derks J. B., Oudijk M. A., Torrance H. L., Rademaker C. M. A., Benders M. J., Rosen K. G., Cindrova-Davies T., Thakor A. S., Visser G. H. A., Burton G. J., Van Bel F., Giussani D. A., Allopurinol reduces oxidative stress in the ovine fetal cardiovascular system after repeated episodes of ischemia-reperfusion. Pediatric Research 2010 68 5 374 380 2-s2.0-77958508176 10.1203/PDR.0b013e3181ef7780
80. Li G., Xiao Y., Estrella J. L., Ducsay C. A., Gilbert R. D., Zhang L., Effect of fetal hypoxia on heart susceptibility to ischemia and reperfusion injury in the adult rat. Journal of the Society for Gynecologic Investigation 2003 10 5 265 274 2-s2.0-0037674471 10.1016/S1071-5576(03)00074-1 (Pubitemid 36802327)
81. Oh C., Dong Y., Liu H., Thompson L. P., Intrauterine hypoxia upregulates proinflammatory cytokines and matrix metalloproteinases in fetal guinea pig hearts. American Journal of Obstetrics and Gynecology 2008 199 1 78.e1 78.e6 2-s2.0-45649083624 10.1016/j.ajog.2007.12.004
82. Tong W., Zhang L., Fetal hypoxia and programming of matrix metalloproteinases. Drug Discovery Today 2012 17 124 134 10.1016/j.drudis.2011. 09.011
83. Tong W., Xue Q., Li Y., Zhang L., Maternal hypoxia alters matrix metalloproteinase expression patterns and causes cardiac remodeling in fetal and neonatal rats. American Journal of Physiology 2011 301 5 H2113 H21121
84. Xue Q., Zhang L., Prenatal hypoxia causes a sex-dependent increase in heart susceptibility to ischemia and reperfusion injury in adult male offspring: role of protein kinase C ε Journal of Pharmacology and Experimental Therapeutics 2009 330 2 624 632 2-s2.0-67651046198 10.1124/jpet.109.153239
85. Yzydorczyk C., Comte B., Cambonie G., Lavoie J. C., Germain N., Shun Y. T., Wolff J., Deschepper C., Touyz R. M., Lelièvre-Pegorier M., Nuyt A. M., Neonatal oxygen exposure in rats leads to cardiovascular and renal alterations in adulthood. Hypertension 2008 52 5 889 895 2-s2.0-55949097598 10.1161/HYPERTENSIONAHA.108.116251
86. Richter H. G., Camm E. J., Modi B. N., Ascorbate prevents placental oxidative stress and enhances birth weight in hypoxic pregnancy in rats. Journal of Physiology 2012 590 6 1377 1387
87. Potdar N., Singh R., Mistry V., Evans M. D., Farmer P. B., Konje J. C., Cooke M. S., First-trimester increase in oxidative stress and risk of small-for-gestational-age fetus. An International Journal of Obstetrics and Gynaecology 2009 116 5 637 642 2-s2.0-62149127296 10.1111/j.1471-0528.2008. 02096.x
88. Burton G. J., Yung H. W., Cindrova-Davies T., Charnock-Jones D. S., Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta 2009 30 43 48 2-s2.0-60249089720 10.1016/j.placenta.2008. 11.003
89. Casasco A., Calligaro A., Casasco M., Tateo S., Cornaglia A. I., Reguzzoni M., Farina A., Immunohistochemical localization of lipoperoxidation products in normal human placenta. Placenta 1997 18 4 249 253 2-s2.0-0030908837 10.1016/S0143-4004(97)80058-6 (Pubitemid 27214227)
90. Simmons R. A., Suponitsky-Kroyter I., Selak M. A., Progressive accumulation of mitochondrial DNA mutations and decline in mitochondrial function lead to β -cell failure. Journal of Biological Chemistry 2005 280 31 28785 28791 2-s2.0-23344432499 10.1074/jbc.M505695200 (Pubitemid 41105780)
91. Peterside I. E., Selak M. A., Simmons R. A., Impaired oxidative phosphorylation in hepatic mitochondria in growth-retarded rats. American Journal of Physiology 2003 285 6 E1258 E1266 2-s2.0-0344033667 (Pubitemid 37464376)
92. Koek G. H., Liedorp P. R., Bast A., The role of oxidative stress in non-alcoholic steatohepatitis. Clinica Chimica Acta 2011 412 15-16 1297 1305 2-s2.0-79956301571 10.1016/j.cca.2011.04.013
93. Ghulmiyyah L. M., Costantine M. M., Yin H., Tamayo E., Clark S. M., Hankins G. D. V., Saade G. R., Longo M., The role of oxidative stress in the developmental origin of adult hypertension. American Journal of Obstetrics and Gynecology 2011 205 2 155.e7 155.e11 2-s2.0-79960929099 10.1016/j.ajog.2011.03. 015
94. Mathers J. C., McKay J. A., Koletzko B., Epigenetics-potential contribution to fetal programming. Early Nutrition Programming and Health Outcomes in Later Life: Obesity and Beyond 2009 Springer Science +Business Media 119 123
95. Rees W. D., Susan H. H., Brown D. S., Antipatis C., Palmer R. M., Maternal protein deficiency causes hypermethylation of DNA in the livers of rat fetuses. Journal of Nutrition 2000 130 7 1821 1826 2-s2.0-0343526326 (Pubitemid 30451074)
96. Lillycrop K. A., Phillips E. S., Torrens C., Hanson M. A., Jackson A. A., Burdge G. C., Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR α promoter of the offspring. British Journal of Nutrition 2008 100 2 278 282 2-s2.0-50049108528 10.1017/S0007114507894438
97. Finkel T., Signal transduction by reactive oxygen species. Journal of Cell Biology 2011 194 1 7 15 2-s2.0-79960286223 10.1083/jcb.201102095
98. Gheorghe C. P., Goyal R., Mittal A., Longo L. D., Gene expression in the placenta: maternal stress and epigenetic responses. International Journal of Developmental Biology 2010 54 2-3 507 523 2-s2.0-77950366422 10.1387/ijdb.082770cg
99. Patterson A. J., Chen M., Xue Q., Xiao D., Zhang L., Chronic prenatal hypoxia induces epigenetic programming of PKC ε gene repression in rat hearts. Circulation Research 2010 107 3 365 373 2-s2.0-77956642629 10.1161/CIRCRESAHA.110.221259
100. Patterson A. J., Xiao D., Xiong F., Dixon B., Zhang L., Hypoxia-derived oxidative stress mediates epigenetic repression of PKC ε gene in foetal rat hearts. Cardiovascular Research 2012 93 2 302 310 10.1093/cvr/cvr322
101. Pinney S. E., Simmons R. A., Metabolic programming, epigenetics, and gestational diabetes mellitus. Current Diabetes Reports 2012 12 67 74 10.1007/s11892-011-0248-1
102. Bogdarina I., Haase A., Langley-Evans S., Clark A. J. L., Glucocorticoid effects on the programming of AT1b angiotensin receptor gene methylation and expression in the rat. PLoS ONE 2010 5 2 2-s2.0-77949500501 10.1371/journal. pone.0009237 e9237
103. Rexhaj E., Bloch J., Jayet P. Y., Rimoldi S. F., Dessen P., Mathieu C., Tolsa J., Nicod P., Scherrer U., Sartori C., Fetal programming of pulmonary vascular dysfunction in mice: role of epigenetic mechanisms. American Journal of Physiology 2011 301 1 H247 H252 2-s2.0-79959908836 10.1152/ajpheart.01309.2010
104. Lenzen S., Drinkgern J., Tiedge M., Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radical Biology and Medicine 1996 20 3 463 466 2-s2.0-0029984682 10.1016/0891-5849(96)02051-5 (Pubitemid 26077870)
105. Tiedge M., Lortz S., Drinkgern J., Lenzen S., Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 1997 46 11 1733 1742 2-s2.0-0030689041 (Pubitemid 27456404)
106. Park J. H., Stoffers D. A., Nicholls R. D., Simmons R. A., Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. Journal of Clinical Investigation 2008 118 6 2316 2324 2-s2.0-45549097738 10.1172/JCI33655 (Pubitemid 351872348)
107. Seckl J. R., Prenatal glucocorticoids and long-term programming. European Journal of Endocrinology, Supplement 2004 151 3 U49 U62 2-s2.0-10344226154 (Pubitemid 39627056)
108. Thomassin H., Flavin M., Espinás M. L., Grange T., Glucocorticoid-induced DNA demethylation and gene memory during development. EMBO Journal 2001 20 8 1974 1983 2-s2.0-0035901508 10.1093/emboj/20.8.1974 (Pubitemid 32397399)
109. Bose R., Moors M., Tofighi R., Cascante A., Hermanson O., Ceccatelli S., Glucocorticoids induce long-lasting effects in neural stem cells resulting in senescence-related alterations. Cell Death and Disease 2010 1 11, article e92 2-s2.0-79958729836 10.1038/cddis.2010.60