Intrauterine ethanol exposure results in hypothalamic oxidative stress and neuroendocrine alterations in adult rat offspring

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 291, Issue 3, 2006, Pages

  Dembele, Korami ^a   Yao, Xing Hai ^a   Chen, Li ^a,b   Nyomba, B L Grégoire ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b JILIN UNIVERSITY   (China)

Author keywords

Fetal growth restriction; Lipid peroxides; Neuropeptides; Protein carbonyls; Superoxide dismutases

Indexed keywords

ALCOHOL; CARBONYL DERIVATIVE; GLUTATHIONE; LIPID PEROXIDE; MELANOCORTIN; MESSENGER RNA; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN;

ANIMAL EXPERIMENT; APPETITE; ARTICLE; CATCH UP GROWTH; CONTROLLED STUDY; ENERGY; EXPOSURE; FEMALE; HOMEOSTASIS; HYPOTHALAMUS; IMPAIRED GLUCOSE TOLERANCE; INSULIN RESISTANCE; LOW BIRTH WEIGHT; NEUROSECRETORY CELL; NONHUMAN; OXIDATIVE STRESS; PERINATAL PERIOD; PREGNANCY; PRENATAL PERIOD; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RAT; WEIGHT GAIN;

ANIMALS; BODY COMPOSITION; ETHANOL; FEMALE; HYPOTHALAMUS; INSULIN RESISTANCE; NEUROPEPTIDES; OXIDATIVE STRESS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; WEIGHT GAIN;

EID: 33748456961     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00633.2005     Document Type: Article

References (70)

1. Aebi H. Catalase in vitro. Methods Enzymol 105: 121-126, 1984.
2. Aird F, Halasz I, and Redei E. Ontogeny of hypothalamic corticotropin-releasing factor and anterior pituitary pro-opiomelanocortin expression in male and female offspring of alcohol-exposed and adrenalectomized dams. Alcohol Clin Exp Res 21: 1560-1566, 1997.
3. Anderson ME. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113: 548-555, 1985.
4. Angelogianni P and Gianoulakis C. Chronic ethanol increases proopiomelanocortin gene expression in the rat hypothalamus. Neuroendocrinology 57: 106-114, 1993.
5. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, and Clark PM. Type 2 (noninsulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36: 62-67, 1993.
6. Benediktsson R, Lindsay RS, Noble J, Seckl JR, and Edwards CR. Glucocorticoid exposure in utero: new model for adult hypertension. Lancet 341: 339-341, 1993.
7. Bingol N, Schuster C, Fuchs M, Iosub S, Turner G, Stone RK, and Gromisch DS. The influence of socioeconomic factors on the occurrence of fetal alcohol syndrome. Adv Alcohol Subst Abuse 6: 105-118, 1987.
8. Brown AP, Dinger N, and Levine BS. Stress produced by gavage administration in the rat. Contemp Top Lab Anim Sci 39: 17-21, 2000.
9. Carlberg I and Mannervik B. Glutathione reductase. Methods Enzymol 113: 484-490, 1985.
10. Castells S, Mark E, Abaci F, and Schwartz E. Growth retardation in fetal alcohol syndrome. Unresponsiveness to growth-promoting hormones. Dev Pharmacol Ther 3: 232-241, 1981.
11. Cettour-Rose P, Samec S, Russell AP, Summermatter S, Mainieri D, Carrillo-Theander C, Montani JP, Seydoux J, Rohner-Jeanrenaud F, and Dulloo AG. Redistribution of glucose from skeletal muscle to adipose tissue during catch-up fat: a link between catch-up growth and later metabolic syndrome. Diabetes 54: 751-756, 2005.
12. Chen L and Nyomba BL. Effects of prenatal alcohol exposure on glucose tolerance in the rat offspring. Metabolism 52: 454-462, 2003.
13. Chen L and Nyomba BL. Glucose intolerance and resistin expression in rat offspring exposed to ethanol in utero: modulation by postnatal high-fat diet. Endocrinology 144: 500-508, 2003.
14. Chen L and Nyomba BL. Whole body insulin resistance in rat offspring of mothers consuming alcohol during pregnancy or lactation: comparing prenatal and postnatal exposure. J Appl Physiol 96: 167-172, 2004.
15. Chen L, Yao XH, and Nyomba BL. In vivo insulin signaling through PI3-kinase is impaired in skeletal muscle of adult rat offspring exposed to ethanol in utero. J Appl Physiol 99: 528-534, 2005.
16. Chen L, Zhang T, and Nyomba BL. Insulin resistance of gluconeogenic pathways in neonatal rats after prenatal ethanol exposure. Am J Physiol Regul Integr Comp Physiol 286: R554-R559, 2004.
17. Clarren SK and Smith DW. The fetal alcohol syndrome. N Engl J Med 298: 1063-1067, 1978.
18. 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: 1-9, 2003.
19. Crescenzo R, Samec S, Antic V, Rohner-Jeanrenaud F, Seydoux J, Montani JP, and Dulloo AG. A role for suppressed thermogenesis favoring catch-up fat in the pathophysiology of catch-up growth. Diabetes 52: 1090-1097, 2003.
20. Cripps RL, Martin-Gronert MS, and Ozanne SE. Fetal and perinatal programming of appetite. Clin Sci (Lond) 109: 1-11, 2005.
21. De A, Boyadjieva NI, Pastorcic M, Reddy BV, and Sarkar DK. Cyclic AMP and ethanol interact to control apoptosis and differentiation in hypothalamic beta-endorphin neurons. J Biol Chem 269: 26697-26705, 1994.
22. Dubern B, Clement K, Pelloux V, Froguel P, Girardet JP, Guy-Grand B, and Tounian P. Mutational analysis of melanocortin-4 receptor, agouti-related protein, and alpha-melanocyte-stimulating hormone genes in severely obese children. J Pediatr 139: 204-209, 2001.
23. Elton CW, Pennington JS, Lynch SA, Carver FM, and Pennington SN. Insulin resistance in adult rat offspring associated with maternal dietary fat and alcohol consumption. J Endocrinol 173: 63-71, 2002.
24. Fan W, Boston BA, Kesterson RA, Hruby VJ, and Cone RD. Role of melanocortinergic neurons in feeding and the agouti obesity syndrome. Nature 385: 165-168, 1997.
25. Fernandez-Checa JC, Garcia-Ruiz C, Ookhtens M, and Kaplowitz N. Impaired uptake of glutathione by hepatic mitochondria from chronic ethanol-fed rats. Tracer kinetic studies in vitro and in vivo and susceptibility to oxidant stress. J Clin Invest 87: 397-405, 1991.
26. Flohe L and Gunzler WA. Assays of glutathione peroxidase. Methods Enzymol 105: 114-121, 1984.
27. Franco MC, Akamine EH, Di Marco GS, Casarini DE, Fortes ZB, Tostes RC, Carvalho MH, and Nigro D. NADPH oxidase and enhanced superoxide generation in intrauterine undernourished rats: involvement of the renin-angiotensin system. Cardiovasc Res 59: 767-775, 2003.
28. Gabriel KI, Johnston S, and Weinberg J. Prenatal ethanol exposure and spatial navigation: effects of postnatal handling and aging. Dev Psychobiol 40: 345-357, 2002.
29. Goodlett CR, Horn KH, and Zhou FC. Alcohol teratogenesis: mechanisms of damage and strategies for intervention. Exp Biol Med (Maywood) 230: 394-406, 2005.
30. Hales CN and Ozanne SE. The dangerous road of catch-up growth. J Physiol 547: 5-10, 2003.
31. Hanson ES, Levin N, and Dallman MF. Elevated corticosterone is not required for the rapid induction of neuropeptide Y gene expression by an overnight fast. Endocrinology 138: 1041-1047, 1997.
32. Heaton MB, Paiva M, Madorsky I, and Shaw G. Ethanol effects on neonatal rat cortex: comparative analyses of neurotrophic factors, apoptosis-related proteins, and oxidative processes during vulnerable and resistant periods. Brain Res Dev Brain Res 145: 249-262, 2003.
33. Henderson GI, Devi BG, Perez A, and Schenker S. In utero ethanol exposure elicits oxidative stress in the rat fetus. Alcohol Clin Exp Res 19: 714-720, 1995.
34. Jeanrenaud B, Halimi S, and van de Werve G. Neuro-endocrine disorders seen as triggers of the triad: obesity-insulin resistance-abnormal glucose tolerance. Diabetes Metab Rev 1: 261-291, 1985.
35. Kim WH, Hong F, Jaruga B, Hu Z, Fan S, Liang TJ, and Gao B. Additive activation of hepatic NF-kappaB by ethanol and hepatitis B protein X (HBX) or HCV core protein: involvement of TNF-alpha receptor 1-independent and -dependent mechanisms. FASEB J 15: 2551-2553, 2001.
36. Koteish A and Diehl AM. Animal models of steatosis. Semin Liver Dis 21: 89-104, 2001.
37. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, and Stadtman ER. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186: 464-478, 1990.
38. Light KE, Kane CJ, Pierce DR, Jenkins D, Ge Y, Brown G, Yang H, and Nyamweya N. Intragastric intubation: important aspects of the model for administration of ethanol to rat pups during the postnatal period. Alcohol Clin Exp Res 22: 1600-1606, 1998.
39. Loos RJ, Rankinen T, Tremblay A, Perusse L, Chagnon Y, and Bouchard C. Melanocortin-4 receptor gene and physical activity in the Quebec Family Study. Int J Obes 29: 420-428, 2005.
40. Lopez-Tejero D, Llobera M, and Herrera E. Permanent abnormal response to a glucose load after prenatal ethanol exposure in rats. Alcohol 6: 469-473, 1989.
41. Marino MD, Aksenov MY, and Kelly SJ. Vitamin E protects against alcohol-induced cell loss and oxidative stress in the neonatal rat hippocampus. Int J Dev Neurosci 22: 363-377, 2004.
42. Marsh DJ, Hollopeter G, Huszar D, Laufer R, Yagaloff KA, Fisher SL, Burn P, and Palmiter RD. Response of melanocortin-4 receptor-deficient mice to anorectic and orexigenic peptides. Nat Genet 21: 119-122, 1999.
43. Marshall JA, Hamman RF, Baxter J, Mayer EJ, Fulton DL, Orleans M, Rewers M, and Jones RH. Ethnic differences in risk factors associated with the prevalence of noninsulin-dependent diabetes mellitus. The San Luis Valley Diabetes Study. Am J Epidemiol 137: 706-718, 1993.
44. Obici S, Feng Z, Tan J, Liu L, Karkanias G, and Rossetti L. Central melanocortin receptors regulate insulin action. J Clin Invest 108: 1079-1085, 2001.
45. Ogilvie KM, Lee S, and Rivier C. Divergence in the expression of molecular markers of neuronal activation in the parvocellular paraventricular nucleus of the hypothalamus evoked by alcohol administration via different routes. J Neurosci 18: 4344-4352, 1998.
46. Ohkawa H, Ohishi N, and Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 19: 351-358, 1979.
47. Ozanne SE and Hales CN. The long-term consequences of intra-uterine protein malnutrition for glucose metabolism. Proc Nutr Soc 58: 615-619, 1999.
48. Pennington JS, Shuvaeva TI, and Pennington SN. Maternal dietary ethanol consumption is associated with hypertriglyceridemia in adult rat offspring. Alcohol Clin Exp Res 26: 848-855, 2002.
49. Peterside IE, Selak MA, and Simmons RA. Impaired oxidative phosphorylation in hepatic mitochondria in growth-retarded rats. Am J Physiol Endocrinol Metab 285: E1258-E1266, 2003.
50. Pettitt DJ, Bennett PH, Saad MF, Charles MA, Nelson RG, and Knowler WC. Abnormal glucose tolerance during pregnancy in Pima Indian women. Long-term effects on offspring. Diabetes 40, Suppl 2: 126-130, 1991.
51. Rainero I, De Gennaro T, Visentin G, Brunetti E, Cerrato P, Torre E, Portaleone P, and Pinessi L. Effects of chronic ethanol treatment on alpha-MSH concentrations in rat brain and pituitary. Neuropeptides 15: 139-141, 1990.
52. Rasmussen DD, Boldt BM, Wilkinson CW, and Mitton DR. Chronic daily ethanol and withdrawal: 3. Forebrain pro-opiomelanocortin gene expression and implications for dependence, relapse, and deprivation effect. Alcohol Clin Exp Res 26: 535-546, 2002.
53. Ravelli AC, van der Meulen JH, Michels RP, Osmond C, Barker DJ, Hales CN, and Bleker OP. Glucose tolerance in adults after prenatal exposure to famine. Lancet 351: 173-177, 1998.
54. Ren J, Roughead ZK, Wold LE, Norby FL, Rakoczy S, Mabey RL, and Brown-Borg HM. Increases in insulin-like growth factor-1 level and peroxidative damage after gestational ethanol exposure in rats. Pharmacol Res 47: 341-347, 2003.
55. Reyes E, Ott S, and Robinson B. Effects of in utero administration of alcohol on glutathione levels in brain and liver. Alcohol Clin Exp Res 17: 877-881, 1993.
56. Scanlon MN, Lazar-Wesley E, Csikos T, and Kunos G. Rat hypothalamic proopiomelanocortin messenger RNA is unaffected by adrenalectomy. Biochem Biophys Res Commun 186: 418-425, 1992.
57. Selak MA, Storey BT, Peterside I, and Simmons RA. Impaired oxidative phosphorylation in skeletal muscle of intrauterine growth-retarded rats. Am J Physiol Endocrinol Metab 285: E130-E137, 2003.
58. Simmons RA, Templeton LJ, and Gertz SJ. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 50: 2279-2286, 2001.
59. Thiele TE, Navarro M, Sparta DR, Fee JR, Knapp DJ, and Cubero I. Alcoholism and obesity: overlapping neuropeptide pathways? Neuropeptides 37: 321-337, 2003.
60. Torres FK and Zimmerberg B. Effects of prepregnancy ethanol on neuromotor development, activity, and learning. Pharmacol Biochem Behav 41: 587-597, 1992.
61. Tran TD, Jackson HD, Horn KH, and Goodlett CR. Vitamin E does not protect against neonatal ethanol-induced cerebellar damage or deficits in eyeblink classical conditioning in rats. Alcohol Clin Exp Res 29: 117-129, 2005.
62. Tran TD and Kelly SJ. Alterations in hippocampal and hypothalamic monoaminergic neurotransmitter systems after alcohol exposure during all three trimester equivalents in adult rats. J Neural Transm 106: 773-786, 1999.
63. Urso T, Gavaler JS, and Van Thiel DH. Blood ethanol levels in sober alcohol users seen in an emergency room. Life Sci 28: 1053-1056, 1981.
64. Vaisse C, Clement K, Guy-Grand B, and Froguel P. A frameshift mutation in human MC4R is associated with a dominant form of obesity. Nat Genet 20: 113-114, 1998.
65. Van Assche F, Holemans K, and Aerts L. Fetal growth and consequences for later life. J Perinat Med 26: 337-346, 1998.
66. Vickers MH, Breier BH, Cutfield WS, Hofman PL, and Gluckman PD. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab 279: E83-E87, 2000.
67. Vorhees CV. A fostering/crossfostering analysis of the effects of prenatal ethanol exposure in a liquid diet on offspring development and behavior in rats. Neurotoxicol Teratol 11: 115-120, 1989.
68. Yao XH, Chen L, and Nyomba BL. Adult rats prenatally exposed to ethanol have increased gluconeogenesis and impaired insulin response of hepatic gluconeogenic genes. J Appl Physiol 100: 642-648, 2006.
69. Zhang M, Gong Y, Corbin I, Mellon A, Choy P, Uhanova J, and Minuk GY. Light ethanol consumption enhances liver regeneration after partial hepatectomy in rats. Gastroenterology 119: 1333-1339, 2000.
70. Zhou Y, Franck J, Spangler R, Maggos CE, Ho A, and Kreek MJ. Reduced hypothalamic POMC and anterior pituitary CRF1 receptor mRNA levels after acute, but not chronic, daily "binge" intragastric alcohol administration. Alcohol Clin Exp Res 24: 1575-1582, 2000.