Prenatal nicotine exposure induced a hypothalamic-pituitary-adrenal axis-associated neuroendocrine metabolic programmed alteration in intrauterine growth retardation offspring rats

Toxicology Letters

Volumn 214, Issue 3, 2012, Pages 307-313

  Liu, L ^a   Liu, F ^a   Kou, H ^a   Zhang, B J ^a   Xu, D ^a,b   Chen, B ^c   Chen, L B ^c   Magdalou, J ^d   Wang, H ^a,b  

^a WUHAN UNIVERSITY   (China)

^b WUHAN UNIVERSITY   (China)

^c ZHONGNAN HOSPITAL OF WUHAN UNIVERSITY   (China)

^d Biopôle de l Université de Lorraine   (France)

Author keywords

Glucocorticoid; Glucose and lipid metabolism; Hypothalamic pituitary adrenal axis; Intrauterine growth retardation; Nicotine

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; CHOLESTEROL; CORTICOSTERONE; CORTICOTROPIN; GLUCOCORTICOID RECEPTOR; GLUCOSE; MESSENGER RNA; MINERALOCORTICOID RECEPTOR; NICOTINE; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHRONIC STRESS; CONTROLLED STUDY; DISEASE PREDISPOSITION; FEMALE; FETUS; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INTRAUTERINE GROWTH RETARDATION; LIPID METABOLISM; MALE; METABOLIC DISORDER; METABOLIC SYNDROME X; NEUROENDOCRINE SYSTEM; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROGENY; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT CHANGE;

ANIMALS; FEMALE; FETAL DEVELOPMENT; FETAL GROWTH RETARDATION; GANGLIONIC STIMULANTS; GLUCOSE; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LIPID METABOLISM; MALE; MATERNAL EXPOSURE; MATERNAL-FETAL EXCHANGE; NEUROSECRETION; NICOTINE; PHYSICAL CONDITIONING, ANIMAL; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; STRESS, PHYSIOLOGICAL; SWIMMING;

RATTUS;

EID: 84867234990     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2012.09.001     Document Type: Article

References (41)

1. Ajilore O.A., Sapolsky R.M. In vivo characterization of 11beta-hydroxysteroid dehydrogenase in rat hippocampus using glucocorticoid neuroendangerment as an endpoint. Neuroendocrinology 1999, 69:138-144.
2. Anagnostis P., Athyros V.G., Tziomalos K., Karagiannis A., Mikhailidis D.P. Clinical review: the pathogenetic role of cortisol in the metabolic syndrome: a hypothesis. Journal of Clinical Endocrinology and Metabolism 2009, 94:2692-2701.
3. Barker D.J., Hales C.N., Fall C.H., Osmond C., Phipps K., Clark P.M. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993, 36:62-67.
4. Brabant G., Muller G., Horn R., Anderwald C., Roden M., Nave H. Hepatic leptin signaling in obesity. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2005, 19:1048-1050.
5. Chang L., Chiang S.H., Saltiel A.R. Insulin signaling and the regulation of glucose transport. Molecular Medicine 2004, 10:65-71.
6. Chen H., Iglesias M.A., Caruso V., Morris M.J. Maternal cigarette smoke exposure contributes to glucose intolerance and decreased brain insulin action in mice offspring independent of maternal diet. PLoS ONE 2011, 6:e27260.
7. Chen M., Wang T., Liao Z.X., Pan X.L., Feng Y.H., Wang H. Nicotine-induced prenatal overexposure to maternal glucocorticoid and intrauterine growth retardation in rat. Experimental and Toxicologic Pathology: Official Journal of the Gesellschaft fur Toxikologische Pathologie 2007, 59:245-251.
8. Contal M., Masson G., Boyer C., Cazevielle C., Mares P. Neonatal consequences of maternal smoking during pregnancy. Journal de Gynecologie, Obstetrique et Biologie de la reproduction 2005, 34(1):3S215-222S.
9. De Kloet E.R., Vreugdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocrine Reviews 1998, 19:269-301.
10. de Quervain D.J., Aerni A., Schelling G., Roozendaal B. Glucocorticoids and the regulation of memory in health and disease. Frontiers in Neuroendocrinology 2009, 30:358-370.
11. Delaunay F., Khan A., Cintra A., Davani B., Ling Z.C., Andersson A., Ostenson C.G., Gustafsson J., Efendic S., Okret S. Pancreatic beta cells are important targets for the diabetogenic effects of glucocorticoids. Journal of Clinical Investigation 1997, 100:2094-2098.
12. Desai M., Gayle D., Babu J., Ross M.G. Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 2005, 288:R91-R96.
13. Engelbregt M.J., van Weissenbruch M.M., Popp-Snijders C., Lips P., Delemarre-van de Waal H.A. Body mass index, body composition, and leptin at onset of puberty in male and female rats after intrauterine growth retardation and after early postnatal food restriction. Pediatric Research 2001, 50:474-478.
14. Fowden A.L., Forhead A.J., Coan P.M., Burton G.J. The placenta and intrauterine programming. Journal of Neuroendocrinology 2008, 20:439-450.
15. Higgins S. Smoking in pregnancy. Current Opinion in Obstetrics & Gynecology 2002, 14:145-151.
16. Holloway A.C., Cuu D.Q., Morrison K.M., Gerstein H.C., Tarnopolsky M.A. Transgenerational effects of fetal and neonatal exposure to nicotine. Endocrine 2007, 31:254-259.
17. Hotta K., Funahashi T., Bodkin N.L., Ortmeyer H.K., Arita Y., Hansen B.C., Matsuzawa Y. Circulating concentrations of the adipocyte protein adiponectin are decreased in parallel with reduced insulin sensitivity during the progression to type 2 diabetes in rhesus monkeys. Diabetes 2001, 50:1126-1133.
18. Huang L.Z., Liu X., Griffith W.H., Winzer-Serhan U.H. Chronic neonatal nicotine increases anxiety but does not impair cognition in adult rats. Behavioral Neuroscience 2007, 121:1342-1352.
19. Imdad A., Yakoob M.Y., Siddiqui S., Bhutta Z.A. Screening and triage of intrauterine growth restriction (IUGR) in general population and high risk pregnancies: a systematic review with a focus on reduction of IUGR related stillbirths. BMC Public Health 2011, 3(11 Suppl.):S1.
20. Kanaka-Gantenbein C. Fetal origins of adult diabetes. Annals of the New York Academy of Sciences 2010, 1205:99-105.
21. Kim C.K., Giberson P.K., Yu W., Zoeller R.T., Weinberg J. Effects of prenatal ethanol exposure on hypothalamic-pituitary-adrenal responses to chronic cold stress in rats. Alcoholism, Clinical and Experimental Research 1999, 23:301-310.
22. Lingas R.I., Matthews S.G. A short period of maternal nutrient restriction in late gestation modifies pituitary-adrenal function in adult guinea pig offspring. Neuroendocrinology 2001, 73:302-311.
23. Lopez-Bermejo A., Botas P., Funahashi T., Delgado E., Kihara S., Ricart W., Fernandez-Real J.M. Adiponectin, hepatocellular dysfunction and insulin sensitivity. Clinical Endocrinology 2004, 60:256-263.
24. McCormick C.M., Smythe J.W., Sharma S., Meaney M.J. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Research Developmental Brain Research 1995, 84:55-61.
25. Oyama M., Nakamura K., Tsuchiya Y., Yamamoto M. Unhealthy maternal lifestyle leads to rapid infant weight gain: prevention of future chronic diseases. Tohoku Journal of Experimental Medicine 2009, 217:67-72.
26. Qiu X.S., Huang T.T., Shen Z.Y., Deng H.Y., Ke Z.Y. Effect of early nutrition on intestine development of intrauterine growth retardation in rats and its correlation to leptin. World Journal of Gastroenterology 2005, 11:4419-4422.
27. Radosavljevic T., Todorovic V., Vucevic D., Sikic B. The growth hormone axis and insulin-like growth factors. Medicinski Pregled 2005, 58:558-562.
28. Rajan V., Edwards C.R., Seckl J.R. 11 beta-Hydroxysteroid dehydrogenase in cultured hippocampal cells reactivates inert 11-dehydrocorticosterone, potentiating neurotoxicity. Journal of Neuroscience: Official Journal of the Society for Neuroscience 1996, 16:65-70.
29. Reynolds R.M. Corticosteroid-mediated programming and the pathogenesis of obesity and diabetes. Journal of Steroid Biochemistry and Molecular Biology 2010, 122:3-9.
30. Schaefer T.L., Skelton M.R., Herring N.R., Gudelsky G.A., Vorhees C.V., Williams M.T. Short- and long-term effects of (+)-methamphetamine and (+/-)-3,4-methylenedioxymethamphetamine on monoamine and corticosterone levels in the neonatal rat following multiple days of treatment. Journal of Neurochemistry 2008, 104:1674-1685.
31. Silveira V.M., Horta B.L. Birth weight and metabolic syndrome in adults: meta-analysis. Revista de Saude Publica 2008, 42:10-18.
32. Thamotharan M., Shin B.C., Suddirikku D.T., Thamotharan S., Garg M., Devaskar S.U. GLUT4 expression and subcellular localization in the intrauterine growth-restricted adult rat female offspring. American Journal of Physiology Endocrinology and Metabolism 2005, 288:E935-E947.
33. Van de Kar L.D., Richardson-Morton K.D., Rittenhouse P.A. Stress: neuroendocrine and pharmacological mechanisms. Methods and Achievements in Experimental Pathology 1991, 14:133-173.
34. Vieau D., Sebaai N., Leonhardt M., Dutriez-Casteloot I., Molendi-Coste O., Laborie C., Breton C., Deloof S., Lesage J. HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology 2007, 32(Suppl. 1):S16-S20.
35. Walker B.R. Cortisol - cause and cure for metabolic syndrome?. Diabetic Medicine: A Journal of the British Diabetic Association 2006, 23:1281-1288.
36. Wang T., Chen M., Yan Y.E., Xiao F.Q., Pan X.L., Wang H. Growth retardation of fetal rats exposed to nicotine in utero: possible involvement of CYP1A1, CYP2E1, and P-glycoprotein. Environmental Toxicology 2009, 24:33-42.
37. Welberg L.A., Seckl J.R., Holmes M.C. Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour. Neuroscience 2001, 104:71-79.
38. Xita N., Tsatsoulis A. Fetal origins of the metabolic syndrome. Annals of the New York Academy of Sciences 2010, 1205:148-155.
39. Xu D., Liang G., Yan Y.E., He W.W., Liu Y.S., Chen L.B., Magdalou J., Wang H. Nicotine-induced over-exposure to maternal glucocorticoid and activated glucocorticoid metabolism causes hypothalamic-pituitary-adrenal axis-associated neuroendocrine metabolic alterations in fetal rats. Toxicology Letters 2012, 209:282-290.
40. Yan Y.E., Wang H., Feng Y.H. Alterations of placental cytochrome P450 1A1 and P-glycoprotein in tobacco-induced intrauterine growth retardation in rats. Acta Pharmacologica Sinica 2005, 26:1387-1394.
41. Yildiz D. Nicotine, its metabolism and an overview of its biological effects. Toxicon: Official Journal of the International Society on Toxinology 2004, 43:619-632.