Embryonic oxidative stress as a mechanism of teratogenesis with special emphasis on diabetic embryopathy

Reproductive Toxicology

Volumn 24, Issue 1, 2007, Pages 31-41

  Ornoy, Asher ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Alcohol; Antioxidants; Cigarette smoking; Cocaine; Diabetes; Hypoxia; Ionizing radiation; Oxidative stress

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; CAROTENOID; FOLIC ACID; REACTIVE OXYGEN METABOLITE; TERATOGENIC AGENT;

ALCOHOL ABUSE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CIGARETTE SMOKING; COCAINE DEPENDENCE; CONGENITAL MALFORMATION; CONTROLLED STUDY; DIABETIC EMBRYOPATHY; EMBRYO; EMBRYO DEATH; EMBRYOPATHY; ENZYME ACTIVITY; HYPOXIA; IONIZING RADIATION; NONHUMAN; OXIDATIVE STRESS; PREECLAMPSIA; RAT; REPRODUCTION; REVIEW; RISK FACTOR; TERATOGENESIS; YOLK SAC;

ABNORMALITIES, DRUG-INDUCED; ANIMALS; ANOXIA; ANTIOXIDANTS; COCAINE; DIABETES MELLITUS; EMBRYO; ETHANOL; FEMALE; FETAL DISEASES; FETUS; HUMANS; OXIDATIVE STRESS; PLACENTA; PREGNANCY; PREGNANCY IN DIABETICS; RADIATION, IONIZING; RATS; REACTIVE OXYGEN SPECIES; SMOKING; TERATOGENS;

ANIMALIA; RATTUS;

EID: 34447268977     PISSN: 08906238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.reprotox.2007.04.004     Document Type: Review

References (90)

1. Halliwell B. How to characterize a biological antioxidant. Free Radic Res Commun 9 (1990) 1-32
2. Halliwell B., Gutteridge J.M.C., and Cross C. Free radicals, antioxidants and human diseases: where are we now?. Lab Clin Med 119 (1992) 598-613
3. Halliwell B., and Gutteridge J.M.C. Free radicals in biology and medicine (1995), Clarendon Press, Oxford
4. Kohen R., and Nyska A. Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reaction and methods for their quantitation. Toxicol Pathol 30 (2002) 620-650
5. Papaccio G., Pisanti F.A., and Frascatore S. Acetyl homocysteine thiolactone induced increase: superoxide dismutase counteracts the effect of sub diabetogenic doses of streptozocin. Diabetes 35 (1986) 470-474
6. Zimmerman E.F., Potturi R.B., Resnick E., and Fisher J.E. Role of oxygen free radicals in cocaine-induced vascular disruption in mice. Teratology 49 (1994) 192-201
7. Fantel A.G., Barber C.V., and Mackles B. Ischemia reperfusion: a new hypothesis for the developmental toxicity of cocaine. Teratology 46 (1992) 285-292
8. Eriksson U.J., and Borg L.A.H. Diabetes and embryonic malformations. Role of substrate-induced free oxygen radical production for dysmorphogenesis in cultured rat embryos. Diabetes 42 (1993) 411-419
9. Eriksson U.J., Cederberg J., and Wentzel P. Congenital malformations in offspring of diabetic mothers-animal and human studies. Rev Endocr Metab Disord 4 (2003) 79-93
10. Ornoy A., Zaken V., and Kohen R. Role of reactive oxygen species (ROS) in the diabetes-induced anomalies in rat embryos in vitro: reduction in antioxidant enzymes and LMWA may be the causative factor for increased anomalies. Teratology 60 (1999) 376-386
11. Hass M., Iqbal J., Clearch L.B., Brank L., and Massaro D. Rat lung, Cu, Zn superoxide dismutase, isolation and sequence of full-length cDNA and studies of enzyme induction. J Clin Invest 83 (1989) 1241-1245
12. Sharma M.K., and Buetner G.R. Interaction of vitamin C and vitamin E during free radical stress in plasma. Free Radic Biol Med 14 (1993) 649-653
13. Karowicz-Bilinska A., Suzin J., and Sieroszewski P. Evaluation of oxidative stress indices during treatment in pregnant women with intrauterine growth retardation. Med Sci Monit 3 (2002) CR 211-6
14. Allen R.G. Oxygen-reactive species and antioxidant response during development. The metabolic paradox of cellular differentiation. Soc Exp Biol Med 196 (1991) 117-129
15. El Hage S., and Singh S.M. Temporal expression of genes encoding free radical-metabolizing enzymes is associated with higher mRNA levels during in vitro development in mice. Dev Genet 11 (1990) 149-159
16. Wentzel, Thunbrg L., and Eriksson U.J. Teratogenic effect of diabetic serum is prevented by suplementation of superoxide dismutase and N-acetylcysteine in rat embryo culture. Diabetologia 40 (1994) 7-14
17. Ornoy A., Kimyagarov D., Yaffe P., Raz I., and Cohen R. Role of reactive oxygen species in diabetes-induced embryo toxicity: studies on pre-implantation mouse embryos cultured in serum from diabetic pregnant woman. Isr J Med Sci 32 (1996) 1066-1073
18. Khan J.Y., and Black S.M. Developmental changes in murine brain antioxidant enzymes. Pediatr Res 54 (2003) 77-82
19. Jauniaux E., Hempstock J., Greenwold N., and Burton G.J. Trophoblastic oxidative stress in relation to temporal and regional differences in maternal placental blood flow in normal and abnormal early pregnancies. Am J Pathol 162 (2003) 115-125
20. Pankewycz O.G., Guan J.X., and Benedict J.F. Cytokines as mediators of autoimmune diabetes and diabetic complications. Endocr Rev 16 (1995) 164-176
21. Zaken V., Kohen R., and Ornoy A. The development of antioxidant defense mechanism in young rat embryos in vivo and in vitro. Early Pregnancy Biol Med 4 (2000) 110-123
22. Avgil M. Cohen diabetic rat: a unique experimental rat model combining genetic and environmental causative factors for the research of fetal growth restriction. Emphasis on the oxidant antioxidant status. MSc thesis, Hebrew University, August 2005.
23. Zangen S.W., Yaffe P., Kohen R., and Ornoy A. The role of reactive oxygen species in diabetes-induced anomalies in embryos of Cohen diabetic rats. Int J Exp Diabetes Res 3 (2002) 247-255
24. Jennings P.E., Jones A.F., Florkowski C.M., Lunec J., and Barnett A.H. Increased diene conjugates in diabetic subjects with microangiopathy. Diabet Med 4 (1987) 452-456
25. Cederberg J., and Eriksson U.J. Antioxidative treatment of pregnant diabetic rats diminishes embryonic dysmorphogenesis. Birth Defects Res A Clin Mol Teratol 73 (2005) 498-505
26. Sivan C.M., and Eriksson U.J. Vitamin C supplementation of the maternal diet reduces the rate of malformation in the offspring of diabetic rats. Diabetologia 40 (1997) 1416-1424
27. Zaken V., Kohen R., and Ornoy A. Vitamins C and E improve rat embryonic antioxidant defense mechanism in diabetic culture medium. Teratology 64 (2001) 33-44
28. Elangovan V., Shohami E., Gati E., and Kohen R. Increased hepatic lipid soluble antioxidant capacity as compared to other organs of streptozotocin-induced diabetic rats: a cyclic voltammetry study. Free Radic Res 32 (2000) 125-134
29. Pani L., Horal M., and Loeken M.R. Polymorphic susceptibility to the molecular causes of neural tube defects during diabetic embryopathy. Diabetes 51 (2002) 2871-2874
30. Weksler-Zangen S., Yagil C., Zangen D.H., Ornoy A., Jacob H.J., and Yagil H. The newly inbred Cohen diabetic rat: a nonobese normolipidemic genetic model of diet-induced type 2 diabetes expressing sex differences. Diabetes 50 (2001) 2521-2529
31. Weksler-Zangen S., Yaffe P., Kohen R., and Ornoy A. Reduced SOD activity and increased neural tube defects in embryos of the sensitive but not of the resistant Cohen diabetic rats cultured under diabetic conditions. Birth Defects Res A Clin Mol Teratol 67 (2003) 429-437
32. Zangen W.S., Seonghun R., and Ornoy A. Alterations in the expression of antioxidant genes and the levels of transcription factor NF-kappa B in relation to diabetic embryopathy in the Cohen diabetic rat model. Birth Defects Res A 76 (2006) 107-114
33. Li R., Chase M., Jung S.K., Smith P.J.S., and Locken M.R. Hypoxic stress in diabetic pregnancy contributes to impaired embryo gene expression and defective development by inducing oxidative stress. Am J Physiol Endocrinol Metab 289 (2005) E591-E599
34. Zusman I., and Ornoy A. Effects of hyperglycemia and ketone bodies on the in vitro development of early somite rat embryos. Pediatr Pathol 7 (1987) 535-547
35. Ornoy A., Zaken V., Abir R., Yaffe P., and Raz I. Serum from women with gestational diabetes is teratogenic to rat embryos in culture. Toxicol In Vitro 9 (1995) 643-651
36. Curley F., and Ingalls T. Hypoxia at normal atmospheric pressure as a cause of congenital malformations in mice. Proc Soc Exp Biol Med 94 (1957) 87-88
37. Ergaz Z., Avgil M., and Ornoy A. Intrauterine growth restriction; etiology and consequences: what do we know about the human situation and experimental animal models. Reprod Toxicol 20 (2005) 301-322
38. Zenteno-Savin T., Clayton-Hanandez E., and Elsner R. Diving seals: are they a model for coping with oxidative stress?. Comp Biochem Physiol 133C (2002) 527-533
39. Ho E., and Bray T.M. Antioxidants, NF kappa B activation and diabetogenesis. Proc Soc Exp Biol Med (1999) 205-213
40. Dohlen G., Carlsen H., Blomboff R., Thaulow E., and Saugstat D.O. Reoxygenation of hypoxic mice with 100% oxygen induces brain nuclear factor-kappa B. Pediatr Res 58 (2005) 941-945
41. Chandel N.S., Trzyna W.C., McClintock D.S., and Schumacker P.T. Role of oxidant in NF-κB activation and TNF alfa gene transcription induced by hypoxia and endotoxin. J Immunol 165 (2000) 1014-1021
42. Foldes-Papp Z., Domej W., Demel U., and Tilz G.P. Oxidative stress caused by acute and chronic exposition to altitude. Wien Med Wochenschr 155 (2005) 136-142
43. Harris A.I. Hypoxia: a key regulatory factor in tumor growth. Nat Rev Cancer 2 (2002) 38-47
44. Johnson P., Elsner R., and Zentaeno-Savin T. Hypoxia-inducible factor-1 proteomics and diving adaptations in ringed seal. Free Radic Biol Med 39 (2005) 205-212
45. Catrina S.B., Okamoto k, Pereira T., and Brismar K. Hyperglycemia regulates hypoxia-inducible factor-1 α protien stability and function. Diabetes 53 (2004) 3226-3232
46. Yamada N., Horikawa Y., Oda N., Iizuka K., Shihara N., Kishi S., et al. Genetic variation in the hypoxia-inducible factor-1 α gene is associated with type 2 diabetes in Japanese. J Clin Endocrinol Metab 90 (2005) 5841-5847
47. Hoyme H.E., Jones K.L., Dixon S.D., Jewet T., Hanson J.W., Robinson L.K., et al. Prenatal cocaine exposure and fetal vascular disruption. Pediatrics 85 (1990) 743-747
48. Slutker L. Risks associated with cocaine use during pregnancy. Obstet Gynecol 79 (1992) 778-779
49. Lipton J.W., Vu T.Q., Ling Z., Gyawali S., Mayer J.R., and Carvey P.M. Prenatal cocaine exposure induces an attenuation of uterine blood flow in the rat. Neurotoxicol Teratol 24 (2002) 143-148
50. Lipton J.W., Gyawali S., Borys E.D., Koprich J.B., Ptaszny M., and McGuire S.O. Prenatal cocaine administration increases glutathione and alpha-tocopherol oxidation in fetal rat brain. Dev Brain Res 147 (2003) 77-84
51. Bashkatova V., Meunier J., Vanin A., and Maurice T. Nitric oxide and oxidative stress in the brain of rats exposed in utero to cocaine. Ann NY Acad Sci 1074 (2006) 632-642
52. Poon H.F., Abdullah L., Mullan M.A., Mullan M.J., and Crawford F.C. Cocaine-induced oxidative stress precedes cell death in human neuronal progenitor cells. Neurochem Int 50 (2007) 69-73
53. Schull W.J., and Otake M. Cognitive function and prenatal exposure to ionizing radiation. Teratology 59 (1999) 222-226
54. Boice J.D., and Miller R.W. Childhood and adult cancer after intrauterine exposure to ionizing radiation. Teratology 59 (1999) 227-233
55. De Santis M., Di Gianantonio E., Straface G., Cavaliere A.F., Caruso A., Schiavon F., et al. Ionizing radiations in pregnancy and teratogenesis. A review of the literature. Reprod Toxicol 20 (2005) 323-329
56. Verheyde J., and Benotmane M.A. Unraveling the fundamental molecular mechanisms of morphological and cognitive defects in the irradiated brain. Brain Res Rev 53 (2007) 312-320
57. Guelman L.R., Caban J.I., Pagott R.M.L., and Zieler L.M. Ionizing radiation-induced damage on developing celebellar granule cells cultures can be prevented by an early amifostine post-treatment. Int J Dev Neurosci 23 (2005) 1-7
58. Manda K., Ueno M., Moritake T., and Anzai K. Alpha lipoic acid attenuates x-irradiation-induced oxidative stress in mice. Cell Biol Toxicol 23 (2007) 129-137
59. von Deutch A.W., Mitchell C.D., Williams C.E., Dutt K., Silvestrov N.A., Klement B.J., et al. Polyamine protect against radiation-induced oxidative stress. Gravit Space Biol Bull 18 (2005) 109-110
60. Gisone P., Dubner D., Del Perez Rosarion M., Michelin S., and Puntarulo S. The role of nitric oxide in the radiation-induced effects in the developing brain. In Vivo 18 (2004) 281-292
61. Claren S.K. Recognition of fetal alcohol syndrome. JAMA 245 (1981) 1076-1078
62. Abel E.L. An update on the incidence of FAS: FAS is not an equal opportunity birth defect. Neurotoxicol Teratol 17 (1995) 437-443
63. Streissguth A.P., Aase J.M., Clarren S.K., RRandels S.P., LaDue R.A., and Smith D.F. Fetal alcohol syndrome in adolescents and adults. JAMA 265 (1991) 1961-1967
64. Windham G.C., Fenster L., Hopkins B., and Swan S.H. The association of moderate maternal and paternal alcohol consumption with birthweight and gestational age. Epidemiology 6 (1995) 591-597
65. Martinez-Frias K.R., Brmejo E., Rodrigez-Pinilla E., and Frias J.L. Risk for congenital anomalies with different sporadic and daily doses of alcohol consumption during pregnancy. A case control study. Birth Defects Res A 70 (2004) 194-200
66. Davis W.L., Crawford L.A., Cooper O.J., Farmer G.R., Thomas D.L., and Freeman B.L. Ethanol induces the generation of reactive free radicals by neural crest cells in vitro. J Craniofac Genet Dev Biol 10 (1990) 277-293
67. Kotch L.E., Chen S.Y., and Sulik K.K. Ethanol-induced teratogenesis: free radical damage as a possible mechanism. Teratology 52 (1995) 128-136
68. Heaton M.B., Paiva M., Mayer J., and Miller R. Ethanol-mediated generation of reactive oxygen species in developing rat cerebellum. Neurosci lett 334 (2002) 83-86
69. Dembele K., Yao X.Y., Chen L., and Nyomba B.L.G. Intrauterine ethanol exposure results in hypothalamic oxidative stress and neuroendocrine alterations in adult rat offspring. Am J Physiol Regul Integr Comp Physiol 291 (2006) R796-R802
70. Mithchell J., Paiva M., and Heaton M. The antioxidants vitamin E and beta carotene protect against ethanol-induced neurotoxicity in embryonic rat hippocampal cultures. Alcohol 17 (1999) 163-168
71. Wentzel P., Rydberg U., and Eriksson U.J. Antioxidative treatment diminishes ethano-induced congenital malformations in the rat. Alcohol Clin Exp Res 30 (2006) 1752-1760
72. Cano M.J., Ayele A., Murillo M.L., and Carreras O. Protective effects of folic acid against oxidative stress produced in 21 day postpartum rats by maternal ethanol chronic consumption during pregnancy and lactation period. Free Radic Biol Res 34 (2001) 1-8
73. Cohen-Kerem R., and Koren G. Antioxidants and fetal protection against ethanol teratogenicity. I. Review of the experimental data and implications to humans. Neurotoxicol Teratol 25 (2003) 1-9
74. Anonymous. Smoking and reproductive health. Am. College Obst. Gynecol. Technical bulletin number 180. Int J Gynecol Obstet 43 (1993) 75-81
75. Werler M.M. Teratogen update: smoking and reproductive outcome. Teratology 55 (1997) 382-388
76. Milberger S., Biederman J., Faraone S.V., Chen L., and Jones J. Is maternal smoking during pregnancy a risk factor for attention deficit hyperactivity disorder in children?. Am J Psychol 153 (1996) 1138-1142
77. Law K.L., Stroud L.R., LaGasse L.L., Niaura R., Liu J., and Lester B.M. Smoking during pregnancy and newborn neurobehavior. Pediatrics 111 (2003) 1318-1322
78. Schwarz K.B., Cox J.M., Sharma S., Clement L., Witter F., Abbey H., et al. Prooxidant effects of meternal smoking and formula in newborn infants. J Pediatr Gastroenterol Nutr 24 (1997) 68-72
79. Ermis B., Ors R., Yildirim A., Tastekin A., Kardas F., and Akcay F. Influence of smoking on maternal and neonatal serum malondialdehyde, superoxide dismutase and glutathione peroxidase levels. Ann Clin Lab Sci 34 (2004) 405-409
80. Noakes PS, Thomas R, Lane C, Mori TA, Barden AE, Devadason SG, Prescott SL. Maternal smoking is associated with increased infant oxidative stress at 3 months of age. Thorax 2007.
81. Li Y., and Wang H. In utero exposure to tobacco and alcohol modifies neurobehavioral development in mice offspring: consideration for a role of oxidative stress. Pharmacol Res 49 (2004) 467-473
82. Zhao Z., and Reece E.A. Nicotine-induced embryonic malformations mediated by apoptosis from increasing intracellular calcium and ocxidative stress. Birth Defects Res B 74 (2005) 383-391
83. Kim P.A., De Boni U., and Wells P.G. Peroxidase-dependent bioactivation and oxidation of DNA and protein in benzo[a]pyrene-initiated micronucleus formation. Free Radic Biol Med 23 (1997) 579-596
84. Parman T., and Wells P.G. Embryonic prostaglandin H synthase-2 (PHS-2) expression and benzo[a]pyrene teratogenicity in PHS-2 knockout mice. FASEB J 16 (2002) 1001-1009
85. Wells P.G., and Winn L.M. Biochemical toxicology of chemical teratogenesis. Crit Rev Biochem Mol Biol 31 (1996) 1-40
86. Parman T., Wiley M.J., and Wells P.G. Free radical-mediated oxidative DNA damage in the mechanism of thalidomide teratogenicity. Nat Med 5 (1999) 582-585
87. Jauniaux E., Poston L., and Burton G.J. Placental-related diseases of pregnancy: involvement of oxidative stress and implications in human evolution. Hum reprod update 12 (2006) 747-755
88. Tjoa M.L., Cindrova-Davies T., Spasic-Boskovic O., Bianchi D.W., and Burton G.J. Trophoblastic oxidative stress and the release of cell-free feto placental DNA. Am J Pathol 169 (2006) 400-404
89. Sugino N., Kakata M., Kashida S., Karube A., Takigushi S., and Kato H. Decreased superoxide dismutase expression and increased concentrations of lipid peroxides and prostaglandin F (2 alpha) in the deciduas of failed pregnancy. Mol Hum Reprod 16 (2000) 1644-1647
90. Baxter N., Sumiya M., Cheng S., Erlich H., Regan L., Simmons A., et al. Recurrent miscarriage and variant alleles of mannose binding lectin, tumor necrosis factor and lymphotoxin alpha genes. Clin Exp Immunol 126 (2001) 529-534