Differential effects of chronic ethanol exposure on cytochrome P450 2E1 and the hypothalamic-pituitary-adrenal axis in the maternal-fetal unit of the guinea pig

Neurotoxicology and Teratology

Volumn 32, Issue 2, 2010, Pages 164-170

  Hewitt, Amy J ^a   Walker, Kevin R ^a   Kobus, Susan M ^a   Poklewska Koziell, Margo ^a   Reynolds, James N ^a,b   Brien, James F ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

CYP2E1; Ethanol teratogenicity; Fetal alcohol spectrum disorders; Guinea pig; HPA axis; Liver; Maternal fetal unit; Microsomal; Mitochondrial; Oxidative stress; Third trimester equivalent

Indexed keywords

ALCOHOL; CORTICOTROPIN; CYTOCHROME P450 2E1; HYDROCORTISONE;

ALCOHOL BLOOD LEVEL; ARTICLE; BODY WEIGHT; BRAIN WEIGHT; CELL FRACTIONATION; CONTROLLED STUDY; CORTICOTROPIN BLOOD LEVEL; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; FEMALE; FETOMATERNAL TRANSFUSION; FETUS; FETUS BLOOD; FETUS LIVER; GESTATION PERIOD; GESTATIONAL AGE; GUINEA PIG; HYDROCORTISONE BLOOD LEVEL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LIVER MICROSOME; LIVER MITOCHONDRION; LONG TERM EXPOSURE; MATERNAL BLOOD; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; THIRD TRIMESTER PREGNANCY;

ALCOHOL-INDUCED DISORDERS, NERVOUS SYSTEM; ANIMALS; CHILD, PRESCHOOL; COGNITION DISORDERS; CYTOCHROME P-450 CYP2E1; DEVELOPMENTAL DISABILITIES; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; ENERGY METABOLISM; FEMALE; FETAL ALCOHOL SYNDROME; GUINEA PIGS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LIVER; MICROSOMES, LIVER; MITOCHONDRIA; OXIDATIVE STRESS; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

ANIMALIA; CAVIA;

EID: 77649275548     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2009.12.002     Document Type: Article

References (75)

1. Abdollah S., Catlin M.C., and Brien J.F. Ethanol neuro-behavioural teratogenesis in the guinea pig: behavioural dysfunction and hippocampal morphologic change. Can. J. Physiol. Pharmacol. 71 (1993) 776-782
2. Abel E.L., and Hannigan J.H. Maternal risk factors in fetal alcohol syndrome: provocative and permissive influences. Neurotoxicol. Teratol. 17 (1995) 445-462
3. Anderson Jr. R.A. Endocrine balance as a factor in the etiology of the fetal alcohol syndrome. Neurobehav. Toxicol. Teratol. 3 (1981) 89-104
4. Bai J., and Cederbaum A.I. Overexpression of CYP2E1 in mitochondria sensitizes HepG2 cells to the toxicity caused by depletion of glutathione. J. Biol. Chem. 281 (2006) 5128-5136
5. Bakker J.M., van Bel F., and Heijnen C.J. Neonatal glucocorticoids and the developing brain: short-term treatment with life-long consequences?. Trends Neurosci. 24 (2001) 649-653
6. Barnes D.E., and Walker D.W. Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in rat hippocampus. Brain Res. 227 (1981) 333-340
7. Bondy S.C., and Naderi S. Contribution of hepatic cytochrome P450 systems to the generation of reactive oxygen species. Biochem. Pharmacol. 48 (1994) 155-159
8. Brien J.F., and Clarke D.W. Disposition and fetal effects of ethanol during pregnancy. In: Kacew S., and Lock S. (Eds). Toxicology and Pharmacological Principles in Pediatrics (1988), Hemisphere Publishing, New York 199-222
9. Brien J.F., and Smith G.N. Effects of alcohol (ethanol) on the fetus. J. Dev. Physiol. 15 (1991) 21-32
10. Campbell A.L., and Murphy B.E. The maternal-fetal cortisol gradient during pregnancy and at delivery. J. Clin. Endocrinol. Metab. 45 (1977) 435-440
11. Carpenter S.P., Savage D.D., Schultz E.D., and Raucy J.L. Ethanol-mediated transplacental induction of CYP2E1 in fetal rat liver. J. Pharmacol. Exp. Ther. 282 (1997) 1028-1036
12. Cicero T.J. Neuroendocrinological effects of alcohol. Annu. Rev. Med. 32 (1981) 123-142
13. Clarke D.W., Steenaart N.A., Slack C.J., and Brien J.F. Pharmacokinetics of ethanol and its metabolite, acetaldehyde, and fetolethality in the third-trimester pregnant guinea pig for oral administration of acute, multiple-dose ethanol. Can. J. Physiol. Pharmacol. 64 (1986) 1060-1067
14. Clarke D.W., Smith G.N., Patrick J., Richardson B., and Brien J.F. Disposition of ethanol and its proximate metabolite, acetaldehyde, in the near-term pregnant ewe for short term maternal administration of moderate-dose ethanol. Drug. Metab. Dispos. 16 (1988) 464-468
15. Clarren S.K., and Smith D.W. The fetal alcohol syndrome. N. Engl. J. Med. 298 (1978) 1063-1067
16. 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
17. Cudd T.A., Chen W.-J.A., and West J.R. Fetal and maternal sheep hypothalamus pituitary adrenal axis responses to chronic binge ethanol exposure during the third trimester equivalent. Alcohol. Clin. Exp. Res. 25 (2001) 1065-1071
18. Dalle M., and Delost P. Plasma and adrenal cortisol concentrations in foetal, newborn and mother guinea-pigs during the perinatal period. J. Endocrinol. 70 (1976) 207-214
19. Dobbing J., and Sands J. Comparative aspects of the brain growth spurt. Early Hum. Dev. 3 (1979) 79-83
20. Duescher R.J., and Elfarra A.A. Determination of p-nitrophenol hydroxylase activity of rat liver microsomes by high-pressure liquid chromatography. Anal. Biochem. 212 (1993) 311-314
21. Elbarbry F., Wilby K., and Alcorn J. Validation of a HPLC method for the determination of p-nitrophenol hydroxylase activity in rat hepatic microsomes. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 834 (2006) 199-203
22. Elvidge H. Production of dated pregnant guinea pigs without postpartum matins. J. Inst. Anim. Technol. 23 (1972) 111-117
23. Ferreira M.P., and Willoughby D. Alcohol consumption: the good, the bad, and the indifferent. Appl. Physiol. Nutr. Metab. 33 (2008) 12-20
24. Gerdin E., Tyden O., and Eriksson U.J. The development of antioxidant enzymatic defense in the perinatal rat lung: activities of superoxide dismutase, glutathione peroxidase, and catalase. Pediatr. Res. 19 (1985) 687-691
25. Gibson M.A., Butters N.S., Reynolds J.N., and Brien J.F. Effects of chronic prenatal ethanol exposure on locomotor activity, and hippocampal weight, neurons, and nitric oxide synthase activity of the young postnatal guinea pig. Neurotoxicol. Teratol. 22 (2000) 183-192
26. Gitau R., Fisk N.M., Teixeita J.M.A., Cameron A., and Glover V. Fetal hypothalamic-pituitary-adrenal stress responses to invasive procedures are independent of maternal responses. J. Clin. Endocrinol. Metab. 86 (2001) 104-109
27. Goodlett C.R., Horn K.H., and Zhou F.C. Alcohol teratogenesis: mechanisms of damage and strategies for intervention. Exp. Biol. Med. (Maywood) 230 (2005) 394-406
28. Gornall A.G., Bardawill C.J., and David M.M. Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 177 (1949) 751-766
29. Green C.R., Kobus S.M., Ji Y., Bennett B.M., Reynolds J.N., and Brien J.F. Chronic prenatal ethanol exposure increases apoptosis in the hippocampus of the term fetal guinea pig. Neurotoxicol. Teratol. 27 (2005) 871-881
30. Green C.R., Watts L.T., Kobus S.M., Henderson G.I., Reynolds J.N., and Brien J.F. Effects of chronic prenatal ethanol exposure on mitochondrial glutathione and 8-iso-prostaglandin F2alpha concentrations in the hippocampus of the perinatal guinea pig. Reprod. Fertil. Dev. 18 (2006) 517-524
31. Guaza C., Torrellas A., and Borrell S. Adrenocortical response to acute and chronic ethanol administration in rats. Psychopharmacology (Berl.) 79 (1983) 173-176
32. Guerri C., Bazinet A., and Riley E.P. Foetal alcohol spectrum disorders and alterations in brain and behaviour. Alcohol Alcohol. 44 (2009) 108-114
33. Hakkola J., Pelkonen O., Pasanen M., and Raunio H. Xenobiotic-metabolizing cytochrome P450 enzymes in the human feto-placental unit: role in intrauterine toxicity. Crit. Rev. Toxicol. 28 (1998) 35-72
34. Henderson G.I., Chen J.J., and Schenker S. Ethanol, oxidative stress, reactive aldehydes, and the fetus. Front Biosci. 4 (1999) D541-D550
35. Henderson G.I., Devi B.G., Perez A., and Schenker S. In utero ethanol exposure elicits oxidative stress in the rat fetus. Alcohol. Clin. Exp. Res. 19 (1995) 714-720
36. Iqbal U., Brien J.F., Kapoor A., Matthews S.G., and Reynolds J.N. Chronic prenatal ethanol exposure increases glucocorticoid-induced glutamate release in the hippocampus of the near-term foetal guinea pig. J. Neuroendocrinol. 18 (2006) 826-834
37. Jacobson M.D. Reactive oxygen species and programmed cell death. Trends Biochem. Sci. 21 (1996) 83-86
38. Jenkins J.S., and Connolly J. Adrenocortical response to ethanol in man. Br. Med. J. 2 (1968) 804-805
39. Kapoor A., Petropoulos S., and Matthews S.G. Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids. Brain Res. Rev. 57 (2008) 586-595
40. Kimura K.A., Reynolds J.N., and Brien J.F. Ethanol neurobehavioral teratogenesis and the role of the hippocampal glutamate-N-methyl-D-aspartate receptor-nitric oxide synthase system. Neurotoxicol. Teratol. 22 (2000) 607-616
41. Koop D.R. Alcohol metabolism's damaging effects on the cell: a focus on reactive oxygen generation by the enzyme cytochrome P450 2E1. Alcohol Res. Health 29 (2006) 274-280
42. Koren G., Nulman I., Chudley A.E., and Loock C. Fetal alcohol spectrum disorder. CMAJ 169 (2003) 1181-1185
43. Livy D.J., Miller E.K., Maier S.E., and West J.R. Fetal alcohol exposure and temporal vulnerability: effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicol. Teratol. 25 (2003) 447-458
44. Mari M., and Cederbaum A.I. Induction of catalase, alpha, and microsomal glutathione S-transferase in CYP2E1 overexpressing HepG2 cells and protection against short-term oxidative stress. Hepatology 33 (2001) 652-661
45. Mariucci G., Ambrosini M.V., Colarieti L., and Bruschelli G. Differential changes in Cu, Zn and Mn superoxide dismutase activity in developing rat brain and liver. Experientia 46 (1990) 753-755
46. Martensson L. The pregnant rabbit, guinea pig, sheep and rhesus monkey as models in reproductive physiology. Eur. J. Obstet. Gynecol. Reprod. Biol. 18 (1984) 169-182
47. Matthews S.G. Dynamic changes in glucocorticoid and mineralocorticoid receptor mRNA in the developing guinea pig brain. Brain Res. Dev. Brain Res. 107 (1998) 123-132
48. Matthews S.G. Antenatal glucocorticoids and programming of the developing CNS. Pediatr. Res. 47 (2000) 291-300
49. Matthews S.G., Owen D., Banjanin S., and Andrews M.H. Glucocorticoids, hypothalamo-pituitary-adrenal (HPA) development, and life after birth. Endocr. Res. 28 (2002) 709-718
50. McGoey T.N., Reynolds J.N., and Brien J.F. Chronic prenatal ethanol exposure-induced decrease of guinea pig hippocampal CA1 pyramidal cell and cerebellar purkinje cell density. Can. J. Physiol. Pharmacol. 81 (2003) 476-484
51. Montoliu C., Sancho-Tello M., Azorin I., Burgal M., Valles S., Renau-Piqueras J., and Guerri C. Ethanol increases cytochrome P4502E1 and induces oxidative stress in astrocytes. J. Neurochem. 65 (1995) 2561-2570
52. Morimoto M., Zern M.A., Hagbjork A.L., Ingelman-Sundberg M., and French S.W. Fish oil, alcohol, and liver pathology: role of cytochrome P450 2E1. Proc. Soc. Exp. Biol. Med. 207 (1994) 197-205
53. Nishimura H., and Shiota K. Summary of comparative embryology and teratology. In: Wilson J.G., and Fraser F.C. (Eds). Handbook of Teratology (1977), Plenum Press, New York 119-154
54. Noth R.H., and Walter Jr. R.M. The effects of alcohol on the endocrine system. Med. Clin. North Am. 68 (1984) 133-146
55. Pierce D.R., and West J.R. Alcohol-induced microencephaly during the third trimester equivalent: relationship to dose and blood alcohol concentration. Alcohol 3 (1986) 185-191
56. Ramachandran V., Perez A., Chen J., Senthil D., Schenker S., and Henderson G.I. In utero ethanol exposure causes mitochondrial dysfunction, which can result in apoptotic cell death in fetal brain: a potential role for 4-hydroxynonenal. Alcohol. Clin. Exp. Res. 25 (2001) 862-871
57. Ramachandran V., Watts L.T., Maffi S.K., Chen J., Schenker S., and Henderson G. Ethanol-induced oxidative stress precedes mitochondrially mediated apoptotic death of cultured fetal cortical neurons. J. Neurosci. Res. 74 (2003) 577-588
58. Rathinam M.L., Watts L.T., Stark A.A., Mahimainathan L., Stewart J., Schenker S., and Henderson G.I. Astrocyte control of fetal cortical neuron glutathione homeostasis: up-regulation by ethanol. J. Neurochem. 96 (2006) 1289-1300
59. Reinke L.A., and Moyer M.J. p-nitrophenol hydroxylation. A microsomal oxidation which is highly inducible by ethanol. Drug Metab. Dispos. 13 (1985) 548-552
60. Riikonen R., Salonen I., Partanen K., and Verho S. Brain perfusion SPECT and MRI in foetal alcohol syndrome. Dev. Med. Child Neurol. 41 (1999) 652-659
61. Riley E.P., and McGee C.L. Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior. Exp. Biol. Med. (Maywood) 230 (2005) 357-365
62. Rivier C., Bruhn T., and Vale W. Effect of ethanol on the hypothalamic-pituitary-adrenal axis in the rat: role of corticotropin-releasing factor (CRF). J. Pharmacol. Exp. Ther. 229 (1984) 127-131
63. Robin M.A., Sauvage I., Grandperret T., Descatoire V., Pessayre D., and Fromenty B. Ethanol increases mitochondrial cytochrome P450 2E1 in mouse liver and rat hepatocytes. FEBS Lett. 579 (2005) 6895-6902
64. Sapolsky R.M. Stress and plasticity in the limbic system. Neurochem. Res. 28 (2003) 1735-1742
65. Schenker S., Becker H.C., Randall C.L., Phillips D.K., Baskin G.S., and Henderson G.I. Fetal alcohol syndrome: current status of pathogenesis. Alcohol. Clin. Exp. Res. 14 (1990) 635-647
66. Sisk D.B. Physiology. In: Wagner J.E., and Manning P.J. (Eds). The Biology of the Guinea Pig (1976), Academic Press, New York 63-92
67. Smith G.N., Patrick J., Sinervo K.R., and Brien J.F. Effects of ethanol exposure on the embryo-fetus: experimental considerations, mechanisms, and the role of prostaglandins. Can. J. Physiol. Pharmacol. 69 (1991) 550-569
68. Steenaart N.A., Clarke D.W., and Brien J.F. Gas-liquid chromatographic analysis of ethanol and acetaldehyde in blood with minimal artifactual acetaldehyde formation. J. Pharmacol. Methods 14 (1985) 199-212
69. Streissguth A.P., Aase J.M., Clarren S.K., Randels S.P., LaDue R.A., and Smith D.F. Fetal alcohol syndrome in adolescents and adults. JAMA 265 (1991) 1961-1967
70. Watts L.T., Rathinam M.L., Schenker S., and Henderson G.I. Astrocytes protect neurons from ethanol-induced oxidative stress and apoptotic death. J. Neurosci. Res. 80 (2005) 655-666
71. Weinberg J., Sliwowska J.H., Lan N., and Hellemans K.G. Prenatal alcohol exposure: foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome. J. Neuroendocrinol. 20 (2008) 470-488
72. Welberg L.A., and Seckl J.R. Prenatal stress, glucocorticoids and the programming of the brain. J. Neuroendocrinol. 13 (2001) 113-128
73. West J.R., Chen W.J., and Pantazis N.J. Fetal alcohol syndrome: the vulnerability of the developing brain and possible mechanisms of damage. Metab. Brain Dis. 9 (1994) 291-322
74. Willoughby K.A., Sheard E.D., Nash K., and Rovet J. Effects of prenatal alcohol exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood. J. Int. Neuropsychol. Soc. 14 (2008) 1022-1033
75. Wu D., and Cederbaum A.I. Ethanol consumption by the nursing mother induces cytochrome P-4502E1 in neonatal rat liver. J. Pharmacol. Exp. Ther. 267 (1993) 560-566