Ethanol-induced fetal dysmorphogenesis in the mouse is diminished by high antioxidative capacity of the mother

Toxicological Sciences

Volumn 92, Issue 2, 2006, Pages 416-422

  Wentzel, Parri ^a   Eriksson, Ulf J ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

8 epi PGF2 ; Ethanol; Isoprostane; Mouse; Oxygen radical; Targeted mutation; Transgene

Indexed keywords

8 ISOPROSTAGLANDIN F2 ALPHA; ALCOHOL; COPPER ZINC SUPEROXIDE DISMUTASE; DRINKING WATER; MESSENGER RNA; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; BREEDING; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; EXPOSURE; FEMALE; FETUS; FETUS MALFORMATION; FETUS WEIGHT; GENE MUTATION; GENOTYPE; GESTATION PERIOD; HETEROZYGOTE; KNOCKOUT MOUSE; LIVER LEVEL; MALE; MATING; MOTHER; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROGENY; RISK ASSESSMENT; TERATOLOGY; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; DINOPROST; ETHANOL; FEMALE; FETAL DEVELOPMENT; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; OXIDATIVE STRESS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SUPEROXIDE DISMUTASE;

EID: 33745786063     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfl024     Document Type: Article

References (52)

1. Addolorato, G., Gasbarrini, A., Marcoccia, S., Simoncini, M., Baccarini, P., Vagni, G., Grieco, A., Sbriccoli, A., Granato, A., Stefanini, G. F., et al. (1997). Prenatal exposure to ethanol in rats: Effects on liver energy level and antioxidant status in mothers, fetuses, and newborns. Alcohol 14, 569-573.
2. Ahlgren, S. C., Thakur, V., and Bronner-Fraser, M. (2002). Sonic hedgehog rescues cranial neural crest from cell death induced by ethanol exposure. Proc. Natl. Acad. Sci. U.S.A. 99, 10476-10481.
3. Armant, D. R., and Saunders, D. E. (1996). Exposure of embryonic cells to alcohol: Contrasting effects during preimplantation and postimplantation development. Semin. Perinatol. 20, 127-139.
4. Brault, S., Martinez-Bermudez, A. K., Marrache, A. M., Gobeil, F., Jr, Hou, X., Beauchamp, M., Quiniou, C., Almazan, G., Lachance, C., Roberts, J., II, et al. (2003). Selective neuromicrovascular endothelial cell death by 8-iso-prostaglandin F2alpha: Possible role in ischemic brain injury. Stroke 34, 776-782.
5. Cano, M. J., Ayala, A., Murillo, M. L., and Carreras, O. (2001). Protective effect of folic acid against oxidative stress produced in 21-day postpartum rats by maternal-ethanol chronic consumption during pregnancy and lactation period. Free Radic. Res. 34, 1-8.
6. Cartwright, M. M., and Smith, S. M. (1995). Stage-dependent effects of ethanol on cranial neural crest cell development: Partial basis for the phenotypic variations observed in fetal alcohol syndrome. Alcohol Clin. Exp. Res. 19, 1454-1462.
7. Cartwright, M. M., Tessmer, L. L., and Smith, S. M. (1998). Ethanol-induced neural crest apoptosis is coincident with their endogenous death, but is mechanistically distinct. Alcohol Clin. Exp. Res. 22, 142-149.
8. Charness, M. E., Safran, R. M., and Perides, G. (1994). Ethanol inhibits neural cell-cell adhesion. J. Biol. Chem. 269, 9304-9309.
9. Chen, S. Y., Dehart, D. B., and Sulik, K. K. (2004). Protection from ethanol-induced limb malformations by the superoxide dismutase/catalase mimetic, EUK-134. FASEB J. 18, 1234-1236.
10. Chen, S. Y., Periasamy, A., Yang, B., Herman, B., Jacobson, K., and Sulik, K. K. (2000). Differential sensitivity of mouse neural crest cells to ethanol-induced toxicity. Alcohol 20, 75-81.
11. Chen, S. Y., and Sulik, K. K. (1996). Free radicals and ethanol-induced cytotoxicity in neural crest cells. Alcohol Clin. Exp. Res. 20, 1071-1076.
12. Cohen-Kerem, R., and Koren, G. (2003). Antioxidants and fetal protection against ethanol teratogenicity. I. Review of the experimental data and implications to humans. Neurotoxicol. Teratol. 25, 1-9.
13. Cornell, N. W., and Veech, R. L. (1983). Enzymatic measurement of ethanol or NAD in acid extracts of biological samples. Anal. Biochem. 132, 418-423.
14. Da Lee, R., Rhee, G. S., An, S. M., Kim, S. S., Kwack, S. J., Seok, J. H., Chae, S. Y., Park, C. H., Yoon, H. J., Cho, D. H., et al. (2004). Differential gene profiles in developing embryo and fetus after in utero exposure to ethanol. J. Toxicol. Environ. Health A 67, 2073-2084.
15. Davis, W. L., Crawford, L. A., Cooper, O. J., Farmer, G. R., Thomas, D. L., and Freeman, B. L. (1990). Ethanol induces the generation of reactive free radicals by neural crest cells in vitro. J. Craniofac. Genet. Dev. Biol. 10, 277-293.
16. Devi, B. G., Henderson, G. I., Frosto, T. A., and Schenker, S. (1993). Effect of ethanol on rat fetal hepatocytes: Studies on cell replication, lipid peroxidation and glutathione. Hepatology 18, 648-659.
17. Devi, B. G., Henderson, G. I., Frosto, T. A., and Schenker, S. (1994). Effect of acute ethanol exposure on cultured fetal rat hepatocytes: Relation to mitochondrial function. Alcohol Clin. Exp. Res. 18, 1436-1442.
18. Devi, B. G., Schenker, S., Mazloum, B., and Henderson, G. I. (1996). Ethanol-induced oxidative stress and enzymatic defenses in cultured fetal rat hepatocytes. Alcohol 13, 327-332.
19. Dreosti, I. E., Ballard, F. J., Belling, G. B., Record, I. R., Manuel, S. J., and Hetzel, B. S. (1981). The effect of ethanol and acetaldehyde on DNA synthesis in growing cells and on fetal development in the rat. Alcohol Clin. Exp. Res. 5, 357-362.
20. Epstein, C. J., Avraham, K. B., Lovett, S., Elroy-Stein, O., Rotman, G., Bry, C., and Groner, Y. (1987). Transgenic mice with increased CuZn-superoxide dismutase activity: An animal model of dosage effects in Down's syndrome. Proc. Natl. Acad. Sci. U.S.A. 84, 8044-8048.
21. Goodlett, C. R., and Horn, K. H. (2001). Mechanisms of alcohol-induced damage to the developing nervous system. Alcohol Res. Health 25, 175-184.
22. Guerri, C., Montoliu, C., and Renau-Piqueras, J. (1994). Involvement of free radical mechanism in the toxic effects of alcohol: Implications for fetal alcohol syndrome. Adv. Exp. Med. Biol. 366, 291-305.
23. Henderson, G., Devi, B., Perez, A., and Schenker, S. (1995). In utero ethanol exposure elicits oxidative stress in the rat fetus. Alcohol Clin. Exp. Res. 19, 714-720.
24. Henderson, G. I., Chen, J. J., and Schenker, S. (1999). Ethanol, oxidative stress, reactive aldehydes, and the fetus. Front. Biosci. 4, D541-D550.
25. Jones, K. L., Smith, D. W., Ulleland, C. N., and Streissguth, P. (1973). Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1, 1267-1271.
26. Kay, H. H., Grindle, K. M., and Magness, R. R. (2000). Ethanol exposure induces oxidative stress and impairs nitric oxide availability in the human placental villi: A possible mechanism of toxicity. Am. J. Obstet. Gynecol. 182, 682-688.
27. Kotch, L. E., Chen, S.-E., and Sulik, K. K. (1995). Ethanol-induced teratogenesis: Free radical damage as a possible mechanism. Teratology 52, 128-136.
28. Lee, R. D., An, S. M., Kim, S. S., Rhee, G. S., Kwack, S. J., Seok, J. H., Chae, S. Y., Park, C. H., Choi, Y. W., Kim, H. S., et al. (2005). Neurotoxic effects of alcohol and acetaldehyde during embryonic development. J. Toxicol. Environ. Health A 68, 2147-2162.
29. Lemoine, P., Harousseau, H., Borteyru, J. P., and Menuet, J. C. (1968). Children of alcoholic parents: Abnormalities observed in 127 cases. Ouest Med. 8, 476-482.
30. Lindsley, T. A., Kerlin, A. M., and Rising, L. J. (2003). Time-lapse analysis of ethanol's effects on axon growth in vitro. Brain Res. Dev. Brain. Res. 147, 191-199.
31. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
32. Ma, W., Li, B. S., Maric, D., Zhao, W. Q., Lin, H. J., Zhang, L., Pant, H. C., and Barker, J. L. (2003). Ethanol blocks both basic fibroblast growth factor- and carbachol-mediated neuroepithelial cell expansion with differential effects on carbachol-activated signaling pathways. Neuroscience 118, 37-47.
33. Matzuk, M. M., Dionne, L., Guo, Q., Kumar, T. R., and Lebovitz, R. M. (1998). Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology 139, 4008-4011.
34. Miller, M. W., and Dow-Edwards, D. L. (1988). Structural and metabolic alterations in rat cerebral cortex induced by prenatal exposure to ethanol. Brain Res. 474, 316-326.
35. Mitchell, J., Paiva, M., and Heaton, M. (1999). Vitamin E and beta-carotene protect against ethanol combined with ischemia in an embryonic rat hippocampal culture model of fetal alcohol syndrome. Neurosci. Lett. 263, 189-192.
36. Morrow, J. D., Hill, K. E., Burk, R. F., Nammour, T. M., Badr, K. F., and Roberts, L. J., II. (1990). A series of prostaglandin F2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free radical-catalyzed mechanism. Proc. Natl. Acad. Sci. U.S.A. 87, 9383-9387.
37. Morrow, J. D., Minton, T. A., and Roberts, L. J., II. (1992). The F2-isoprostane, 8-epi-prostaglandin F2 alpha, a potent agonist of the vascular thromboxane/endoperoxide receptor, is a platelet thromboxane/ endoperoxide receptor antagonist. Prostaglandins 44, 155-163.
38. NIH. (1985). Committee on Care and Use of Laboratory Animals: Guide for the Care and Use of Laboratory Animals, NIH Publication No. 85-23. Government Printing Office, U.S. Department of Health and Human Services, Washington DC.
39. Peng, Y., Kwok, K. H., Yang, P. H., Ng, S. S., Liu, J., Wong, O. G., He, M. L., Kung, H. F., and Lin, M. C. (2005). Ascorbic acid inhibits ROS production, NF-kappa B activation and prevents ethanol-induced growth retardation and microencephaly. Neuropharmacology 48, 426-434.
40. Peng, Y., Yang, P. H., Guo, Y., Ng, S. S., Liu, J., Fung, P. C., Tay, D., Ge, J., He, M. L., Kung, H. F., et al. (2004). Catalase and peroxiredoxin 5 protect Xenopus embryos against alcohol-induced ocular anomalies. Investig. Ophthalmol. Vis. Sci. 45, 23-29.
41. Polache, A., Martin-Algarra, R. V., and Guerri, C. (1996). Effects of chronic alcohol consumption on enzyme activities and active methionine absorption in the small intestine of pregnant rats. Alcohol Clin. Exp. Res. 20, 1237-1242.
42. Ramachandran, V., Watts, L. T., Maffi, S. K., Chen, J., Schenker, S., and Henderson, G. (2003). Ethanol-induced oxidative stress precedes mitochondrially mediated apoptotic death of cultured fetal cortical neurons. J. Neurosci. Res. 74, 577-588.
43. Reyes, E., Ott, S., and Robinson, B. (1993). Effects of in utero administration of alcohol on glutathione levels in brain and liver. Alcohol Clin. Exp. Res. 17, 877-881.
44. Satiroglu-Tufan, N. L., and Tufan, A. C. (2004). Amelioration of ethanol-induced growth retardation by all-trans-retinoic acid and alpha-tocopherol in shell-less culture of the chick embryo. Reprod. Toxicol. 18, 407-412.
45. Siler-Marsiglio, K. I., Pan, Q., Paiva, M., Madorsky, I., Khurana, N. C., and Heaton, M. B. (2005). Mitochondrially targeted vitamin E and vitamin E mitigate ethanol-mediated effects on cerebellar granule cell antioxidant defense systems. Brain Res. 1052, 202-211.
46. Snyder, A. K., Singh, S. P., and Pullen, G. L. (1986). Ethanol-induced intrauterine growth retardation: Correlation with placental glucose transfer. Alcohol Clin. Exp. Res. 10, 167-170.
47. Takahashi, K., Nammour, T. M., Fukunaga, M., Ebert, J., Morrow, J. D., Roberts, L. J., Hoover, R. L., and Badr, K. F. (1992). Glomerular actions of a free radical-generated novel prostaglandin, 8-epi-prostaglandin F2 alpha, in the rat. Evidence for interaction with thromboxane A2 receptors. J. Clin. Investig. 90, 136-141.
48. Vaglenova, J., and Petkov, V. V. (1998). Fetal alcohol effects in rats exposed pre- and postnatally to a low dose of ethanol. Alcohol Clin. Exp. Res. 22, 697-703.
49. Wang, X., Williams, E., Haasch, M. L., and Dasmahapatra, A. K. (2006). Japanese medaka (Oryzias latipes): Developmental model for the study of alcohol teratology. Birth Defects Res. B Dev. Reprod. Toxicol. 77, 29-39.
50. Wentzel, P., and Eriksson, U. J. (2002). 8-Iso-PGF(2alpha) administration generates dysmorphogenesis and increased lipid peroxidation in rat embryos in vitro. Teratology 66, 164-168.
51. Wentzel, P., Jansson, L., and Eriksson, U. J. (1995). Diabetes in pregnancy: Uterine blood flow and embryonic development in the rat. Pediatr. Res. 38, 598-606.
52. Zhou, F. C., Sari, Y., Zhang, J. K., Goodlett, C. R., and Li, T. (2001). Prenatal alcohol exposure retards the migration and development of serotonin neurons in fetal C57BL mice. Brain Res. Dev. Brain Res. 126, 147-155.