Embryonic catalase protects against endogenous and phenytoin-enhanced DNA oxidation and embryopathies in acatalasemic and human catalase-expressing mice

FASEB Journal

Volumn 25, Issue 7, 2011, Pages 2188-2200

  Abramov, Julia P ^a   Wells, Peter G ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Birth defects; Hydrogen peroxide; Oxidative stress; Protein therapy; Teratology

Indexed keywords

CATALASE; PHENYTOIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATALASE DEFICIENCY; CONTROLLED STUDY; DNA DETERMINATION; EMBRYO; EMBRYOPATHY; ENZYME ACTIVITY; FEMALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TERATOGENESIS; TRANSGENIC MOUSE;

ABNORMALITIES, DRUG-INDUCED; ACATALASIA; ANIMALS; ANTICONVULSANTS; BRAIN; CATALASE; DNA; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OXIDATION-REDUCTION; PHENYTOIN; PREGNANCY; SURVIVAL RATE;

MUS; MUS MUSCULUS;

EID: 79960161408     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-182444     Document Type: Article

References (59)

1. Ogata, M. (1991) Acatalasemia. Hum. Genet. 86, 331-340
2. Halliwell, B., and Gutteridge, J. M. C. (2007) Free Radicals in Biology and Medicine, 4th Edition, Oxford University Press, Oxford, UK
3. Wells, P. G., McCallum, G. P., Chen, C. S., Henderson, J. T., Lee, C. J. J., Perstin, J., Preston, T. J., Wiley, M. J., and Wong, A. W. (2009) Oxidative stress in developmental origins of disease: teratogenesis, neurodevelopmental deficits and cancer. Toxicol. Sci. 108, 4-18
4. Wells, P. G., Bhuller, Y., Chen, C. S., Jeng, W., Kasapinovic, S., Kennedy, J. C., Kim, P. M., Laposa, R. R., McCallum, G. P., Nicol, C. J., Parman, T., Wiley, M. J., and Wong, A. W. (2005) Molecular and biochemical mechanisms in teratogenesis involving reactive oxygen species. Toxicol. Appl. Pharmacol. 207, 354-366
5. Padmanabhan, R. V., Gudapaty, R., Liener, I. E., Schwartz, B. A., and Hoidal, J. R. (1985) Protection against pulmonary oxygen toxicity in rats by the intratracheal administration of liposome-encapsulated superoxide dismutase or catalase. Am. Rev. Respir. Dis. 132, 264-267
6. Liu, T. H., Beckman, J. S., Freeman, B. A., Hogan, E. L., and Hsu, C. Y. (1989) Polyethylene glycol-conjugated superoxide dismutase and catalase reduce ischemic brain injury. Am. J. Physiol. 256, H589-593
7. Oda, T., Nakai, I., Mituo, M., Yamagishi, H., Oka, T., and Yoshikawa, T. (1992) Role of oxygen radicals and synergistic effect of superoxide dismutase and catalase on ischemia-reperfusion injury of the rat pancreas. Transplant. Proc. 24, 797-798
8. Das, D. K., Russell, J. C., and Jones, R. M. (1991) Reduction of cold injury by superoxide dismutase and catalase. Free Rad. Res. Comm. 12/13, 653-662
9. Gaetani, G. F., Rolfo, M., Arena, S., Mangerini, R., Meloni, G. F., and Ferraris, A. M. (1996) Active involvement of catalase during hemolytic crises of favism. Blood 88, 1084-1088
10. Winn, L. M., and Wells, P. G. (1995) Phenytoin-initiated DNA oxidation in murine embryo culture, and embryo protection by the antioxidative enzymes superoxide dismutase and catalase: evidence for reactive oxygen species-mediated DNA oxidation in the molecular mechanism of phenytoin teratogenicity. Mol. Pharmacol. 48, 112-120
11. Erickson, U. J., and Borg, L. A. H. (1991) Protection by free oxygen radical scavenging enzymes against glucose-induced embryonic malformations in vitro. Diabetologia 34, 325-331
12. Winn, L. M., and Wells, P. G. (1999) Maternal administration of superoxide dismutase and catalase in phenytoin teratogenicity. Free Radic. Biol. Med. 26, 266-274
13. El-Hage, S., and Singh, S. M. (1990) Temporal expression of genes with higher mRNA levels during in utero development in mice. Dev. Genetics. 11, 149-159
14. Abramov, J. P., and Wells, P. G. (2011) Embryoprotective role of endogenous catalase in acatalasemic and human catalase-expressing mouse embryos exposed in culture to developmental and phenytoin-enhanced oxidative stress. Toxicol. Sci. 120, 428-438
15. Barrow, M. V., and Taylor, W. J. (1969) A rapid method for detecting malformations in rat fetuses. J. Morphol. 127, 291-306
16. Liu, L., and Wells, P. G. (1995) DNA oxidation as a potential molecular mechanism mediating drug-induced birth defects: phenytoin and structurally related teratogens initiate the formation of 8-hydroxy-2′-deoxyguanosine in vitro and in vivo in murine maternal hepatic and embryonic tissues. Free Radic. Biol. Med. 19, 639-648
17. Jeng, W., Ramkissoon, A., Parman, T., and Wells, P. G. (2006) Prostaglandin H synthase-catalyzed bioactivation of amphetamines to free radical intermediates that cause CNS regional DNA oxidation and nerve terminal degeneration. FASEB J. 20, 638-650
18. Ravanat, J. L., Douki, T., Duez, P., Gremaud, E., Herbert, K., Hofer, T., Lasserre, L., Saint-Pierre, C., Favier, A., and Cadet, J. (2002) Cellular background level of 8-oxo-7,8-dihydro-2′-deoxyguanosine: an isotope based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up. Carcinogenesis 23, 1911-1918 (Pubitemid 35355940)
19. 2 in irradiated solutions. J. Microchem. 18, 363-374
20. Jiang, Z.-Y., Hunt, J. V., and Wolff, S. P. (1992) Ferrous ion oxidation in the presence of xylenol orange for the detection of lipid hydroperoxide in low density lipoprotein. Anal. Chem. 202, 384-389
21. 2 fluxes within cells. J. Pharmacol. Exper. Ther. 277, 945-953
22. Lum, J. T., Vassanji, N. A., and Wells, P. G. (1985) Analysis of the toxicologically relevant metabolites of phenytoin in biological samples by high-performance liquid chromatography. J. Chromatogr. 338, 242-248
23. Jeng, W., Wong, A. W., Ting-A-Kee, R., and Wells, P. G. (2005) Methamphetamine-enhanced embryonic oxidative DNA damage and neurodevelopmental deficits. Free Rad. Biol. Med. 39, 317-326
24. Wong, A. W., McCallum, G. P., and Wells, P. G. (2008) Oxoguanine glycosylase 1 protects against methamphetamine-enhanced fetal brain oxidative DNA damage and neurodevelopmental deficits. J. Neurosci. 28, 9047-9054
25. Wang, D. H., Ishii, K., Zhen, L. X., and Taketa, K. (1996) Enhanced liver injury in acatalasemic mice following exposure to carbon tetrachloride. Arch. Toxicol. 70, 189-194 (Pubitemid 26037738)
26. Ishii, K., Zhen, L. X., Wang, D. H., Funamori, Y., Ogawa, K., and Taketa, K. (1996) Prevention of mammary tumorigenesis in acatalasemic mice by vitamin E supplementation. Jpn. J. Cancer Res. 87, 680-684 (Pubitemid 26261687)
27. Yamada, K., Ito, A., Watanabe, H., Takahashi, T., Basaran, N. H., and Gotoh, T. (1997) High sensitivity to hepato-tumorigenesis in hypocatalasemic C3H/C(s) b/Gen mice exposed to low doses of 252Cf fission neutrons and 60Co gamma-rays. Anticancer Res. 17, 2041-2047 (Pubitemid 27320943)
28. Ho, Y. S., Xiong, Y., Ma, W., Spector, A., and Ho, D. S. (2004) Mice lacking catalase develop normally but show differential sensitivity to oxidant tissue injury. J. Biol. Chem. 279, 32804-32812 (Pubitemid 39014740)
29. Winn, L. M., and Wells, P. G. (1995) Free radical-mediated mechanisms of anticonvulsant teratogenicity. Eur. J. Neurol. 2, 5-29
30. Nicol, C. J., Zielenski, J., Tsui, L. C., and Wells, P. G. (2000) An embryoprotective role for glucose-6-phosphate dehydrogenase in developmental oxidative stress and chemical teratogenesis. FASEB J. 14, 111-127
31. Perstin, J. P., and Wells, P. G. (2010) Embryoprotective role of constitutive antioxidative catalase in wild-type and acatalasemic mice in vivo and in embryo culture. Toxicol. Lett. 196S, P204-003
32. Kim, P. M., and Wells, P. G. (1996) Phenytoin-initiated hydroxyl radical formation: characterization by enhanced salicylate hydroxylation. Mol. Pharmacol. 49, 172-181
33. Beyerlein, A., Ness, A. R., Streuling, I., Hadders-Algra, M., and von Kries, R. (2010) Early rapid growth: no association with later cognitive functions in children born not small for gestational age. [Review] Am. J. Clin. Nutr. 92, 585-593
34. Abel, K. M., Wicks, S., Susser, E. S., Dalman, C., Pedersen, M. G., Mortensen, P. B., and Webb, R. T. (2010) Birth weight, schizophrenia, and adult mental disorder: is risk confined to the smallest babies? Arch. Gen. Psych. 67, 923-930
35. Fattal-Valevski, A., Toledano-Alhadef, H., Leitner, Y., Geva, R., Eshel, R., and Harel, S. (2009) Growth patterns in children with intrauterine growth retardation and their correlation to neurocognitive development. J. Child Neurol. 24, 846-851
36. Indredavik, M. S., Skranes, J. S., Vik, T., Heyerdahl, S., Romundstad, P., Myhr, G. E., and Brubakk, A. M. (2005) Low-birth-weight adolescents: psychiatric symptoms and cerebral MRI abnormalities. Pediatr. Neurol. 33, 259-266
37. Nair, M. K., Chacko, D. S., Paul, M. K., Nair, L., George, B., and Kumar, G. S. (2009) Low birthweight babies-outcome at 13 years. Indian Pediatr. 46(Suppl.), S71-S74
38. Reuner, G., Hassenpflug, A., Pietz, J., and Philippi, H. (2009) Long-term development of low-risk low birth weight preterm born infants: neurodevelopmental aspects from childhood to late adolescence. Early Hum. Dev. 85, 409-413
39. Roberts, G., Bellinger, D., and McCormick, M. C. (2007) A cumulative risk factor model for early identification of academic difficulties in premature and low birth weight infants. Matern. Child Health J. 11, 161-172
40. Himpel, S., Bartels, J., Zimdars, K., Huether, G., Adler, L., Dawirs, R. R., and Moll, G. H. (2006) Association between body weight of newborn rats and density of serotonin transporters in the frontal cortex at adulthood. J. Neural. Trans. 113, 295-302
41. Danielsson, B. R., Azarbayjani, F., Skold, A. C., and Webster, W. S. (1997) Initiation of phenytoin teratogenesis: pharmacologically induced embryonic bradycardia and arrhythmia resulting in hypoxia and possible free radical damage at reoxygenation. Teratology 56, 271-281 (Pubitemid 28017638)
42. Hansen, D. K. (1991) The embryotoxicity of phenytoin: an update on possible mechanisms. Proc. Soc. Exp. Biol. Med. 197, 361-368
43. Vorhees, C. V. (1983) Fetal anticonvulsant syndrome in rats: dose- and period-response relationships of prenatal diphenylhydantoin, trimethadione and phenobarbital exposure on the structural and functional development of the offspring. J. Pharmacol. Exp. Ther. 227, 274-287
44. Elmazar, M. M. A., and Sullivan, F. M. (1981) Effect of prenatal phenytoin administration on postnatal development of the rat: a behavioral teratology study. Teratology 24, 115-124
45. Vorhees, C. V. (1994) Developmental neurotoxicity induced by therapeutic and illicit drugs. Environ. Health Perspect. 102, 145-153
46. Wells, P. G., McCallum, G. P., Lam, K. C. H., Henderson, J. T., and Ondovcik, S. L. (2010) Oxidative DNA damage and repair in teratogenesis and neurodevelopmental deficits. Birth Defects Res. C Embryo Today 90, 103-109
47. McCallum, G. P., Wong, A. W., and Wells, P. G. (2011) Cockayne syndrome B (CSB) protects against methamphetamine-enhanced oxidative DNA damage in murine fetal brain and postnatal neurodevelopmental deficits. Antiox. Redox Signal. 14, 747-756
48. Espeel, M., Briere, N., De Craemer, D., Jauniaux, E., and Roels, F. (1993) Catalase-negative peroxisomes in human embryonic liver. Cell Tissue Res. 272, 89-92 (Pubitemid 23101018)
49. Fromm, M. F. (2002) The influence of MDR1 polymorphisms on P-glycoprotein expression and function in humans. Adv. Drug Deliv. Rev. 54, 1295-1310
50. Potschka, H., and Loscher, W. (2001) In vivo evidence for P-glycoprotein-mediated transport of phenytoin at the blood-brain barrier of rats. Epilepsia 42, 1231-1240 (Pubitemid 33070662)
51. Ceckova-Novotna, M., Pavek, P., and Staud, F. (2006) P-glycoprotein in the placenta: expression, localization, regulation and function. Reprod. Toxicol. 22, 400-410 (Pubitemid 44344445)
52. Ballabh, P., Braun, A., and Nedergaard, M. (2004) The blood-brain barrier: an overview Structure, regulation, and clinical implications. Neurobiol. Dis. 16, 1-13 (Pubitemid 38569790)
53. Watson, R. E., DeSesso, J. M., Hurtt, M. E., and Cappon, G. D. (2006) Postnatal growth and morphological development of the brain: a species comparison. Birth Defects Res. B Dev. Reprod. Toxicol. 77, 471-484
54. Tishler, D. M., Weinberg, K. T., Hinton, D. R., Barbaro, N., Annett, G. M., and Raffel, C. (1995) MDR1 gene expression in brain of patients with medically intractable epilepsy. Epilepsia 36, 1-6
55. Tsai, C. E., Daood, M. J., Lane, R. H., Hansen, T. W. R., Gruetzmacher, E. M., and Watchko, J. F. (2002) P-glycoprotein expression in mouse brain increases with maturation. Biol. Neonate 81, 58-64
56. Mahmood, B., Daood, M. J., Hart, C., Hansen, T. W. R., and Watchko, J. F. (2001) Ontogeny of P-glycoprotein in mouse intestine, liver and kidney. J. Investig. Med. 49, 250-257
57. Perstin, J. and Wells, P.G. (2007) Protective role of low levels of constitutive catalase in embryonic and fetal development. Birth Defects Res. A Clin. Mol. Teratol. 79, 418 (P24; abstr.)
58. Perstin, J. and Wells, P.G. (2009) Tissue drug concentrations, oxidative DNA damage and embryopathies in acatalasemic and catalase-overexpressing embryos exposed in utero to phenytoin. Birth Defects Res. A Clin. Mol. Teratol. 85, 398 (2; abstr.)
59. Perstin, J., and Wells, P.G. (2009) Embryoprotective role of endogenous catalase in wild-type (C3HeB/FeJ) and acatalasemic (C3Ga.Cg-Catb/J) mice. Toxicol. Sci. (Suppl.: Toxicologist) 108, 355 (1708; abstr.)