The role of cortisol in chronic binge alcohol-induced cerebellar injury: Ovine model

Alcohol

Volumn 47, Issue 1, 2013, Pages 53-61

  Washburn, Shannon E ^a   Tress, Ursula ^b   Lunde, Emilie R ^a   Chen, Wei Jung A ^c   Cudd, Timothy A ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b LABOKLIN GMBH AND CO KG   (Germany)

^c TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

Cerebellum; Cortisol; Ethanol; Fetal alcohol spectrum disorder; Fetal alcohol syndrome; Sheep

Indexed keywords

ALCOHOL; GLUCOCORTICOID; HYDROCORTISONE; SODIUM CHLORIDE;

ALCOHOL BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINGE DRINKING; BRAIN INJURY; CELL COUNT; CELL DENSITY; CELL LOSS; CELL VOLUME; CONTROLLED STUDY; ENCEPHALE ISOLE; EWE; FEMALE; FETAL ALCOHOL SYNDROME; FETUS; GESTATION PERIOD; HYDROCORTISONE BLOOD LEVEL; MATERNAL BLOOD; NONHUMAN; PURKINJE CELL; THIRD TRIMESTER PREGNANCY;

ALCOHOLIC INTOXICATION; ANIMALS; CEREBELLUM; DISEASE MODELS, ANIMAL; FEMALE; FETAL ALCOHOL SYNDROME; HYDROCORTISONE; PREGNANCY; PURKINJE CELLS; SHEEP, DOMESTIC;

ANIMALIA; OVIS; OVIS ARIES;

EID: 84872373971     PISSN: 07418329     EISSN: 18736823     Source Type: Journal    
DOI: 10.1016/j.alcohol.2012.10.004     Document Type: Article

References (94)

1. Abbasi S., Hirsch D., Davis J., Tolosa J., Stouffer N., Debbs R., et al. Effect of single versus multiple courses of antenatal corticosteroids on maternal and neonatal outcome. American Journal of Obstetrics and Gynecology 2000, 182:1243-1249.
2. Andrews M.H., Matthews S.G. Regulation of glucocorticoid receptor mRNA and heat shock protein 70 mRNA in the developing sheep brain. Brain Research 2000, 878:174-182.
3. Autti-Ramo I., Autti T., Korkman M., Kettunen S., Salonen O., Valanne L. MRI findings in children with school problems who had been exposed prenatally to alcohol. Developmental Medicine & Child Neurology 2002, 44:98-106.
4. Beitins I.Z., Kowarski A., Shermeta D.W., De Lemos R.A., Migeon C.J. Fetal and maternal secretion rate of cortisol in sheep: diffusion resistance of the placenta. Pediatric Research 1970, 4:129-134.
5. Bodnoff S.R., Humphreys A.G., Lehman J.C., Diamond D.M., Rose G.M., Meaney M.J. Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. Journal of Neuroscience 1995, 15:61-69.
6. Bohn M. Glucocorticoid induced teratologies of the nervous system 1984, Elsevier, Amsterdam/New York.
7. Bonthius D.J., Bonthius N.E., Napper R.M., Astley S.J., Clarren S.K., West J.R. Purkinje cell deficits in nonhuman primates following weekly exposure to ethanol during gestation. Teratology 1996, 53:230-236.
8. Bonthius D.J., West J.R. Alcohol-induced neuronal loss in developing rats: increased brain damage with binge exposure. Alcoholism: Clinical and Experimental Research 1990, 14:107-118.
9. Caetano R., Ramisetty-Mikler S., Floyd L.R., McGrath C. The epidemiology of drinking among women of child-bearing age. Alcoholism: Clinical and Experimental Research 2006, 30:1023-1030.
10. Clarren S.K., Alvord E.C., Sumi S.M., Streissguth A.P., Smith D.W. Brain malformations related to prenatal exposure to ethanol. The Journal of Pediatrics 1978, 92:64-67.
11. Clarren S.K., Smith D.W. The fetal alcohol syndrome. New England Journal of Medicine 1978, 298:1063-1067.
12. Coles C. Critical periods for prenatal alcohol exposure. Alcohol Health & Research World 1994, 18:22-29.
13. Coles C.D., Brown R.T., Smith I.E., Platzman K.A., Erickson S., Falek A. Effects of prenatal alcohol exposure at school age. I. Physical and cognitive development. Neurotoxicology and Teratology 1991, 13:357-367.
14. Cragg B., Phillips S. Natural loss of Purkinje cells during development and increased loss with alcohol. Brain Research 1985, 325:151-160.
15. Cudd T.A., Chen W.J., Parnell S.E., West J.R. Third trimester binge ethanol exposure results in fetal hypercapnea and acidemia but not hypoxemia in pregnant sheep. Alcoholism: Clinical and Experimental Research 2001, 25:269-276.
16. Cudd T.A., Chen W.J., West J.R. Acute hemodynamic, pituitary, and adrenocortical responses to alcohol in adult female sheep. Alcoholism: Clinical and Experimental Research 1996, 20:1675-1681.
17. Cudd T.A., Chen W.J., West J.R. Fetal and maternal sheep hypothalamus pituitary adrenal axis responses to chronic binge ethanol exposure during the third trimester equivalent. Alcoholism: Clinical and Experimental Research 2001, 25:1065-1071.
18. Dobbing J., Sands J. Quantitative growth and development of human brain. Archives of Disease in Childhood 1973, 48:757-767.
19. Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Human Development 1979, 3:79-83.
20. Ebrahim S.H., Diekman S.T., Floyd R.L., Decoufle P. Comparison of binge drinking among pregnant and nonpregnant women, United States, 1991-1995. American Journal of Obstetrics and Gynecology 1999, 180:1-7.
21. Edwards H.E., Burnham W.M. The impact of corticosteroids on the developing animal. Pediatric Research 2001, 50:433-440.
22. Gabriel K., Hofmann C., Glavas M., Weinberg J. The hormonal effects of alcohol use on the mother and fetus. Alcohol Health & Research World 1998, 22:170-177.
23. Gilstrap L.C., Hightower E.S., Clewell W.H., D'Alton M.E., Damon V.G., Escobedo M.B., et al. Antenatal corticosteroids revisited: repeat courses - National Institutes of Health consensus development conference statement, August 17-18, 2000. Obstetrics & Gynecology 2001, 98:144-150.
24. Gitau R., Cameron A., Fisk N.M., Glover V. Fetal exposure to maternal cortisol. Lancet 1998, 352:707-708.
25. Gladstone J., Nulman I., Koren G. Reproductive risks of binge drinking during pregnancy. Reproductive Toxicology 1996, 10:3-13.
26. Gonzalez-Burgos I., Alejandre-Gomez M. Cerebellar granule cell and Bergmann glial cell maturation in the rat is disrupted by pre- and post-natal exposure to moderate levels of ethanol. International Journal of Developmental Neuroscience 2005, 23:383-388.
27. Goodlett C.R., Eilers A.T. Alcohol-induced Purkinje cell loss with a single binge exposure in neonatal rats: a stereological study of temporal windows of vulnerability. Alcoholism: Clinical and Experimental Research 1997, 21:738-744.
28. Goodlett C.R., Hamre K.M., West J.R. Regional differences in the timing of dendritic outgrowth of Purkinje cells in the vermal cerebellum demonstrated by MAP2 immunocytochemistry. Brain Research. Developmental Brain Research 1990, 53:131-134.
29. Goodlett C.R., Marcussen B.L., West J.R. A single day of alcohol exposure during the brain growth spurt induces brain weight restriction and cerebellar Purkinje cell loss. Alcohol 1990, 7:107-114.
30. Goodlett C.R., Pearlman A.D., Lundahl K.R. Binge neonatal alcohol intubations induce dose-dependent loss of Purkinje cells. Neurotoxicology and Teratology 1998, 20:285-292.
31. Hamre K.M., West J.R. The effects of the timing of ethanol exposure during the brain growth spurt on the number of cerebellar Purkinje and granule cell nuclear profiles. Alcoholism: Clinical and Experimental Research 1993, 17:610-622.
32. Hennessy D.P., Coghlan J.P., Hardy K.J., Scoggins B.A., Wintour E.M. The origin of cortisol in the blood of fetal sheep. Journal of Endocrinology 1982, 95:71-79.
33. Hoyme H.E., May P.A., Kalberg W.O., Kodituwakku P., Gossage J.P., Trujillo P.M., et al. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 institute of medicine criteria. Pediatrics 2005, 115:39-47.
34. Huang W.L., Beazley L.D., Quinlivan J.A., Evans S.F., Newnham J.P., Dunlop S.A. Effect of corticosteroids on brain growth in fetal sheep. Obstetrics & Gynecology 1999, 94:213-218.
35. Huang W.L., Harper C.G., Evans S.F., Newnham J.P., Dunlop S.A. Repeated prenatal corticosteroid administration delays astrocyte and capillary tight junction maturation in fetal sheep. International Journal of Developmental Neuroscience 2001, 19:487-493.
36. Huang W.L., Harper C.G., Evans S.F., Newnham J.P., Dunlop S.A. Repeated prenatal corticosteroid administration delays myelination of the corpus callosum in fetal sheep. International Journal of Developmental Neuroscience 2001, 19:415-425.
37. Fetal alcohol syndrome. Diagnosis, epidemiology, prevention, and treatment 1996, Institute of Medicine, Institute of Medicine, Washington DC.
38. Jacobson S.W., Bihun J.T., Chiodo L.M. Effects of prenatal alcohol and cocaine exposure on infant cortisol levels. Development and Psychopathology 1999, 11:195-208.
39. Jameson R.R., Seidler F.J., Qiao D., Slotkin T.A. Adverse neurodevelopmental effects of dexamethasone modeled in PC12 cells: identifying the critical stages and concentration thresholds for the targeting of cell acquisition, differentiation and viability. Neuropsychopharmacology 2006, 31:1647-1658.
40. Jensen E., Wood C.E., Keller-Wood M. Chronic alterations in ovine maternal corticosteroid levels influence uterine blood flow and placental and fetal growth. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2005, 288:R54-R61.
41. Jobe A.H., Wada N., Berry L.M., Ikegami M., Ervin M.G. Single and repetitive maternal glucocorticoid exposures reduce fetal growth in sheep. American Journal of Obstetrics and Gynecology 1998, 178:880-885.
42. Jones K.L., Smith D.W. Recognition of the fetal alcohol syndrome in early infancy. Lancet 1973, 302:999-1001.
43. Jones K.L., Smith D.W., Streissguth A.P., Myrianthopoulos N.C. Outcome in offspring of chronic alcoholic women. Lancet 1974, 1:1076-1078.
44. Jones K.L., Smith D.W., Ulleland C.N., Streissguth P. Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1973, 1:1267-1271.
45. Jones C.T., Luther E., Richie J.W.K., Worthington D. The clearance of ACTH from the plasma of adult and fetal sheep. Endocrinology 1975, 96:231-234.
46. Kakihana R., Butte J.C., Moore J.A. Endocrine effects of meternal alcoholization: plasma and brain testosterone, dihydrotestosterone, estradiol, and corticosterone. Alcoholism: Clinical and Experimental Research 1980, 4:57-61.
47. 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.
48. Kutzler M.A., Ruane E.K., Coksaygan T., Vincent S.E., Nathanielsz P.W. Effects of three courses of maternally administered dexamethasone at 0.7, 0.75, and 0.8 of gestation on prenatal and postnatal growth in sheep. Pediatrics 2004, 113:313-319.
49. Lemoine P., Harousseau H., Borteyru J.P., Menuet J.C. Children of alcoholic parents - observed anomalies: discussion of 127 cases. Therapeutic Drug Monitoring 2003, 25:132-136.
50. Light K.E., Belcher S.M., Pierce D.R. Time course and manner of Purkinje neuron death following a single ethanol exposure on postnatal day 4 in the developing rat. Neuroscience 2002, 114:327-337.
51. Light K.E., Brown D.P., Newton B.W., Belcher S.M., Kane C.J. Ethanol-induced alterations of neurotrophin receptor expression on Purkinje cells in the neonatal rat cerebellum. Brain Research 2002, 924:71-81.
52. Lupton C., Burd L., Harwood R. Cost of fetal alcohol spectrum disorders. American Journal of Medical Genetics. Part C, Seminars in Medical Genetics 2004, 127C:42-50.
53. Magyar D.M., Fridshal D., Elsner C.W., Glatz T., Eliot J., Klein A.H., et al. Time-trend analysis of plasma cortisol concentrations in the fetal sheep in relation to parturition. Endocrinology 1980, 107:155-159.
54. Maier S.E., Miller J.A., Blackwell J.M., West J.R. Fetal alcohol exposure and temporal vulnerability: regional differences in cell loss as a function of the timing of binge-like alcohol exposure during brain development. Alcoholism: Clinical and Experimental Research 1999, 23:726-734.
55. Maier S.E., West J.R. Regional differences in cell loss associated with binge-like alcohol exposure during the first two trimesters equivalent in the rat. Alcohol 2001, 23:49-57.
56. Maloney S.E., Noguchi K.K., Wozniak D.F., Fowler S.C., Farber N.B. Long-term effects of multiple glucocorticoid exposures in neonatal mice. Behavioral Sciences 2011, 1:4-30.
57. Mastorakos G., Ilias I. Maternal and fetal hypothalamic-pituitary-adrenal axes during pregnancy and postpartum. Annals of the New York Academy of Sciences 2003, 997:136-149.
58. May P.A., Gossage J.P. Estimating the prevalence of fetal alcohol syndrome. A summary. Alcohol Research & Health 2001, 25:159-167.
59. McGowan J.E., Sysyn G., Petersson K.H., Sadowska G.B., Mishra O.P., Delivoria-Papadopoulos M., et al. Effect of dexamethasone treatment on maturational changes in the NMDA receptor in sheep brain. Journal of Neuroscience 2000, 20:7424-7429.
60. Miller S.L., Chai M., Loose J., Castillo-Melendez M., Walker D.W., Jenkin G., et al. The effects of maternal betamethasone administration on the intrauterine growth-restricted fetus. Endocrinology 2007, 148:1288-1295.
61. Milley J.R. Effects of increased cortisol concentration on ovine fetal leucine kinetics and protein metabolism. American Journal of Physiology 1995, 268:E1114-E1122.
62. Modi N., Lewis H., Al-Naqeeb N., Ajayi-Obe M., Dore C.J., Rutherford M. The effects of repeated antenatal glucocorticoid therapy on the developing brain. Pediatric Research 2001, 50:581-585.
63. Murphy B.P., Inder T.E., Huppi P.S., Warfield S., Zientara G.P., Kikinis R., et al. Impaired cerebral cortical gray matter growth after treatment with dexamethasone for neonatal chronic lung disease. Pediatrics 2001, 107:217-221.
64. Murphy V.E., Smith R., Giles W.B., Clifton V.L. Endocrine regulation of human fetal growth: the role of the mother, placenta, and fetus. Endocrine Reviews 2006, 27:141-169.
65. Newnham J.P., Evans S.F., Godfrey M., Huang W., Ikegami M., Jobe A. Maternal, but not fetal, administration of corticosteroids restricts fetal growth. Journal of Maternal-Fetal Medicine 1999, 8:81-87.
66. Effect of corticosteroids for fetal maturation on perinatal outcomes. NIH Consensus Development Panel on the Effect of Corticosteroids for Fetal Maturation on Perinatal Outcomes. Journal of the American Medical Association 1995, 273:413-418. NIH, C.D.P.
67. Noguchi K.K., Walls K.C., Wozniak D.F., Olney J.W., Roth K.A., Farber N.B. Acute neonatal glucocorticoid exposure produces selective and rapid cerebellar neural progenitor cell apoptotic death. Cell Death Differentiation 2008, 15:1582-1592.
68. Pauli J., Wilce P., Bedi K.S. Acute exposure to alcohol during early postnatal life causes a deficit in the total number of cerebellar Purkinje cells in the rat. Journal of Comparative Neurology 1995, 360:506-512.
69. Penton Z. Headspace measurement of ethanol in blood by gas chromatography with a modified autosampler. Clinical Chemistry 1985, 31:439-441.
70. Ramadoss J., Lunde E.R., Chen W.J., West J.R., Cudd T.A. Temporal vulnerability of fetal cerebellar Purkinje cells to chronic binge alcohol exposure: ovine model. Alcoholism: Clinical and Experimental Research 2007, 31:1738-1745.
71. Ramadoss J., Lunde E.R., Pina K.B., Chen W.J., Cudd T.A. All three trimester binge alcohol exposure causes fetal cerebellar Purkinje cell loss in the presence of maternal hypercapnea, acidemia, and normoxemia: ovine model. Alcoholism: Clinical and Experimental Research 2007, 31:1252-1258.
72. Ramadoss J., Lunde E.R., Ouyang N., Chen W.J., Cudd T.A. Acid-sensitive channel inhibition prevents fetal alcohol spectrum disorders cerebellar Purkinje cell loss. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2008, 295:R596-R603.
73. Ramadoss J., Tress U., Chen W.J., Cudd T.A. Maternal adrenocorticotropin, cortisol, and thyroid hormone responses to all three-trimester equivalent repeated binge alcohol exposure: ovine model. Alcohol 2008, 42:199-205.
74. Rees S., Harding R. The effects of intrauterine growth retardation on the development of the Purkinje cell dendritic tree in the cerebellar cortex of fetal sheep: a note on the ontogeny of the Purkinje cell. International Journal of Developmental Neuroscience 1988, 6:461-469.
75. Renwick J.H., Asker R.L. Ethanol-sensitive times for the human conceptus. Early Human Development 1983, 99-111.
76. Riley E.P., McGee C.L., Sowell E.R. Teratogenic effects of alcohol: a decade of brain imaging. American Journal of Medical Genetics. Part C, Seminars in Medical Genetics 2004, 127C:35-41.
77. Rose J.C., Kute T.E., Winkler L. Glucocorticoid receptors in sheep brain tissues during development. American Journal of Physiology 1985, 249:E345-E349.
78. Rosenfeld P., van Eekelen J.A., Levine S., de Kloet E.R. Ontogeny of corticosteroid receptors in the brain. Cellular and Molecular Neurobiology 1993, 13:295-319.
79. Rosett H.L. A clinical perspective of the fetal alcohol syndrome. Alcoholism: Clinical and Experimental Research 1980, 4:119-122.
80. Rugerio-Vargas C., Ramirez-Escoto M., DelaRosa-Rugerio C., Rivas-Manzano P. Prenatal corticosterone influences the trajectory of neuronal development, delaying or accelerating aspects of the Purkinje cell differentiation. Histology and Histopathology 2007, 22:963-969.
81. Sah R., Pritchard L.M., Richtand N.M., Ahlbrand R., Eaton K., Sallee F.R., et al. Expression of the glucocorticoid-induced receptor mRNA in rat brain. Neuroscience 2005, 133:281-292.
82. Salouci M., Engelen V., Gyan M., Antoine N., Jacqmot O., Mignon Y., et al. Development of Purkinje cells in the ovine brain. Anatomia Histologia Embryologia 2012, 41:227-232.
83. Sawant, O. B., Lunde, E. R., Washburn, S. E., Chen, W. A., Goodlett, C. R., & Cudd, T. A. Different patterns of regional Purkinje cell loss in the cerebellar vermis as a function of the timing of prenatal ethanol exposure in an ovine model. Neurotoxicology and Teratology, in press.
84. Schneider M.L., Moore C.F., Kraemer G.W., Roberts A.D., DeJesus O.T. The impact of prenatal stress, fetal alcohol exposure, or both on development: perspectives from a primate model. Psychoneuroendocrinology 2002, 27:285-298.
85. Sokol R.J., Clarren S.K. Guidelines for use of terminology describing the impact of prenatal alcohol on the offspring. Alcoholism: Clinical and Experimental Research 1989, 13:597-598.
86. Sokol R.J., Delaney-Black V., Nordstrom B. Fetal alcohol spectrum disorder. Journal of the American Medical Association 2003, 290:2996-2999.
87. Speirs H.J., Seckl J.R., Brown R.W. Ontogeny of glucocorticoid receptor and 11beta-hydroxysteroid dehydrogenase type-1 gene expression identifies potential critical periods of glucocorticoid susceptibility during development. Journal of Endocrinology 2004, 181:105-116.
88. Uno H., Eisele S., Sakai A., Shelton S., Baker E., DeJesus O., et al. Neurotoxicity of glucocorticoids in the primate brain. Hormones and behavior 1994, 28(4):336-348. doi:10.1006/hbeh.1994.1030.
89. Velazquez P.N., Romano M.C. Corticosterone therapy during gestation: effects on the development of rat cerebellum. International Journal of Developmental Neuroscience 1987, 5:189-194.
90. Weinberg J. Prenatal ethanol exposure alters adrenocortical development of offspring. Alcoholism: Clinical and Experimental Research 1989, 13:73-83.
91. West J.R., Goodlett C.R., Bonthius D.J., Hamre K.M., Marcussen B.L. Cell population depletion associated with fetal alcohol brain damage: mechanisms of BAC-dependent cell loss. Alcoholism: Clinical and Experimental Research 1990, 14:813-818.
92. West J.R., Parnell S.E., Chen W.J., Cudd T.A. Alcohol-mediated Purkinje cell loss in the absence of hypoxemia during the third trimester in an ovine model system. Alcoholism: Clinical and Experimental Research 2001, 25:1051-1057.
93. Wilson S.E., Cudd T.A. Focus on: the use of animal model for the study of fetal alcohol spectrum disorders. Alcohol Research & Health 2011, 34:92-98.
94. Wood C.E. Negative-feedback inhibition of fetal ACTH secretion by maternal cortisol. American Journal of Physiology 1987, 252:R743-R748.