Insulin-like growth factor-I mitigates motor coordination deficits associated with neonatal alcohol exposure in rats

Neurotoxicology and Teratology

Volumn 31, Issue 1, 2009, Pages 40-48

  McGough, Nancy N H ^a   Thomas, Jennifer D ^a   Dominguez, Hector D ^a   Riley, Edward P ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Cerebellum; Fetal alcohol; Motor coordination; Open field activity; Spatial learning

Indexed keywords

ALCOHOL; SOMATOMEDIN C;

ALCOHOL BLOOD LEVEL; ALCOHOL INTOXICATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; BODY WEIGHT; BRAIN DEVELOPMENT; CELL DEATH; CONTROLLED STUDY; DEPTH PERCEPTION; DEVELOPMENTAL COORDINATION DISORDER; FEMALE; LEARNING DISORDER; LOCOMOTION; MALE; MOTOR COORDINATION; MOTOR DYSFUNCTION; NEUROPROTECTION; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT;

AGING; ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; FEMALE; INSULIN-LIKE GROWTH FACTOR I; MALE; MAZE LEARNING; MOTOR ACTIVITY; NEUROTOXICITY SYNDROMES; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 57249094320     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2008.08.001     Document Type: Article

References (116)

1. Alcohol consumption among women who are pregnant or who might become pregnant-United States, 2002. MMWR Morb. Mortal. Wkly. Rep. 53 (2004) 1178-1181
2. Angelucci L., Patacchioli F.R., Scaccianoce S., Di Sciullo A., Cardillo A., and Maccari S. A model for later-life effects of perinatal drug exposure: maternal hormone mediation. Neurobehav. Toxicol. Teratol. 7 (1985) 511-517
3. Archibald S.L., Fennema-Notestine C., Gamst A., Riley E.P., Mattson S.N., and Jernigan T.L. Brain dysmorphology in individuals with severe prenatal alcohol exposure. Dev. Med. Child Neurol. 43 (2001) 148-154
4. Armstrong C.S., Waurin L., and Ishii D.N. Uptake of circulating insulin-like growth factor-I into the cerebrospinal fluid of normal and diabetic rats and normalization of IGF-II mRNA content in diabetic rat brain. J. Neurosci. Res. 59 (2000) 649-660
5. Autti-Ramo I., Fagerlund A., Ervalahti N., Loimu L., Korkman M., and Hoyme H.E. Fetal alcohol spectrum disorders in Finland: clinical delineation of 77 older children and adolescents. Am. J. Med. Genet. A 140 (2006) 137-143
6. Ayer-le Lievre C., Stahlbom P.A., and Sara V.R. Expression of IGF-I and -II mRNA in the brain and craniofacial region of the rat fetus. Development 111 (1991) 105-115
7. Azcona C., Preece M.A., Rose S.J., Fraser N., Rappaport R., Ranke M.B., and Savage M.O. Growth response to rhIGF-I 80 microg/kg twice daily in children with growth hormone insensitivity syndrome: relationship to severity of clinical phenotype. Clin. Endocrinol. (Oxf) 51 (1999) 787-792
8. Backeljauw P.F., and Underwood L.E. Therapy for 6.5-7.5 years with recombinant insulin-like growth factor I in children with growth hormone insensitivity syndrome: a clinical research center study. J. Clin. Endocrinol. Metab. 86 (2001) 1504-1510
9. Barclay D.C., Hallbergson A.F., Montague J.R., and Mudd L.M. Reversal of ethanol toxicity in embryonic neurons with growth factors and estrogen. Brain Res. Bull. 67 (2005) 459-465
10. Baron-Van Evercooren A., Olichon-Berthe C., Kowalski A., Visciano G., and Van Obberghen E. Expression of IGF-I and insulin receptor genes in the rat central nervous system: a developmental, regional, and cellular analysis. J. Neurosci. Res. 28 (1991) 244-253
11. Barron S., White A., Swartzwelder H.S., Bell R.L., Rodd Z.A., Slawecki C.J., Ehlers C.L., Levin E.D., Rezvani A.H., and Spear L.P. Adolescent vulnerabilities to chronic alcohol or nicotine exposure: findings from rodent models. Alcohol. Clin. Exp. Res. 29 (2005) 1720-1725
12. Beck K.D., Powell-Braxton L., Widmer H.R., Valverde J., and Hefti F. Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14 (1995) 717-730
13. Bondy C.A. Transient IGF-I gene expression during the maturation of functionally related central projection neurons. J. Neurosci. 11 (1991) 3442-3455
14. Bondy C.A., and Cheng C.M. Signaling by insulin-like growth factor 1 in brain. Eur. J. Pharmacol. 490 (2004) 25-31
15. Bonthius D.J., Bonthius N.E., Napper R.M., and West J.R. Early postnatal alcohol exposure acutely and permanently reduces the number of granule cells and mitral cells in the rat olfactory bulb: a stereological study. J. Comp. Neurol. 324 (1992) 557-566
16. Bonthius D.J., Karacay B., Dai D., and Pantazis N.J. FGF-2, NGF and IGF-1, but not BDNF, utilize a nitric oxide pathway to signal neurotrophic and neuroprotective effects against alcohol toxicity in cerebellar granule cell cultures. Brain Res. Dev. Brain Res. 140 (2003) 15-28
17. Bonthius D.J., and West J.R. Blood alcohol concentration and microencephaly: a dose-response study in the neonatal rat. Teratology 37 (1988) 223-231
18. Bonthius D.J., and West J.R. Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt. Teratology 44 (1991) 147-163
19. Bradley D.M., Beaman F.D., Moore D.B., Kidd K., and Heaton M.B. Neurotrophic factors BDNF and GDNF protect embryonic chick spinal cord motoneurons from ethanol neurotoxicity in vivo. Brain Res. Dev. Brain Res. 112 (1999) 99-106
20. Breese C.R., D'Costa A., Ingram R.L., Lenham J., and Sonntag W.E. Long-term suppression of insulin-like growth factor-1 in rats after in utero ethanol exposure: relationship to somatic growth. J. Pharmacol. Exp. Ther. 264 (1993) 448-456
21. Bucuvalas J.C., Chernausek S.D., Alfaro M.P., Krug S.K., Ritschel W., and Wilmott R.W. Effect of insulinlike growth factor-1 treatment in children with cystic fibrosis. J. Pediatr. Gastroenterol. Nutr. 33 (2001) 576-581
22. Cao Y., Gunn A.J., Bennet L., Wu D., George S., Gluckman P.D., Shao X.M., and Guan J. Insulin-like growth factor (IGF)-1 suppresses oligodendrocyte caspase-3 activation and increases glial proliferation after ischemia in near-term fetal sheep. J. Cereb. Blood Flow Metab. 23 (2003) 739-747
23. Carrascosa C., Torres-Aleman I., Lopez-Lopez C., Carro E., Espejo L., Torrado S., and Torrado J.J. Microspheres containing insulin-like growth factor I for treatment of chronic neurodegeneration. Biomaterials 25 (2004) 707-714
24. Carroll P.V., Christ E.R., Umpleby A.M., Gowrie I., Jackson N., Bowes S.B., Hovorka R., Croos P., Sonksen P.H., and Russell-Jones D.L. IGF-I treatment in adults with type 1 diabetes: effects on glucose and protein metabolism in the fasting state and during a hyperinsulinemic-euglycemic amino acid clamp. Diabetes 49 (2000) 789-796
25. Carroll P.V., Umpleby M., Alexander E.L., Egel V.A., Callison K.V., Sonksen P.H., and Russell-Jones D.L. Recombinant human insulin-like growth factor-I (rhIGF-I) therapy in adults with type 1 diabetes mellitus: effects on IGFs, IGF-binding proteins, glucose levels and insulin treatment. Clin. Endocrinol. (Oxf) 49 (1998) 739-746
26. Chambers R.A., Potenza M.N., Hoffman R.E., and Miranker W. Simulated apoptosis/neurogenesis regulates learning and memory capabilities of adaptive neural networks. Neuropsychopharmacology 29 (2004) 747-758
27. Cheng C.M., Joncas G., Reinhardt R.R., Farrer R., Quarles R., Janssen J., McDonald M.P., Crawley J.N., Powell-Braxton L., and Bondy C.A. Biochemical and morphometric analyses show that myelination in the insulin-like growth factor 1 null brain is proportionate to its neuronal composition. J. Neurosci. 18 (1998) 5673-5681
28. Chrysis D., Calikoglu A.S., Ye P., and D'Ercole A.J. Insulin-like growth factor-I overexpression attenuates cerebellar apoptosis by altering the expression of Bcl family proteins in a developmentally specific manner. J. Neurosci. 21 (2001) 1481-1489
29. Climent E., Pascual M., Renau-Piqueras J., and Guerri C. Ethanol exposure enhances cell death in the developing cerebral cortex: role of brain-derived neurotrophic factor and its signaling pathways. J. Neurosci. Res. 68 (2002) 213-225
30. Coffin J.M., Baroody S., Schneider K., and O'Neill J. Impaired cerebellar learning in children with prenatal alcohol exposure: a comparative study of eyeblink conditioning in children with ADHD and dyslexia. Cortex 41 (2005) 389-398
31. Coles C.D., Platzman K.A., Raskind-Hood C.L., Brown R.T., Falek A., and Smith I.E. Comparison of children affected by prenatal alcohol exposure and attention deficit, hyperactivity disorder. Alcohol. Clin. Exp. Res. 21 (1997) 150-161
32. D'Mello S.R., Galli C., Ciotti T., and Calissano P. Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 10989-10993
33. de la Monte S.M., Ganju N., Banerjee K., Brown N.V., Luong T., and Wands J.R. Partial rescue of ethanol-induced neuronal apoptosis by growth factor activation of phosphoinositol-3-kinase. Alcohol. Clin. Exp. Res. 24 (2000) 716-726
34. de la Monte S.M., Xu X.J., and Wands J.R. Ethanol inhibits insulin expression and actions in the developing brain. Cell. Mol. Life Sci. 62 (2005) 1131-1145
35. Dobbing J., and Sands J. Comparative aspects of the brain growth spurt. Early Hum. Dev. 3 (1979) 79-83
36. Dohrman D.P., West J.R., and Pantazis N.J. Ethanol reduces expression of the nerve growth factor receptor, but not nerve growth factor protein levels in the neonatal rat cerebellum. Alcohol. Clin. Exp. Res. 21 (1997) 882-893
37. Dore S., Kar S., Zheng W.H., and Quirion R. Rediscovering good old friend IGF-I in the new millennium: possible usefulness in Alzheimer's disease and stroke. Pharm. Acta. Helv. 74 (2000) 273-280
38. Feldman E.L., Sullivan K.A., Kim B., and Russell J.W. Insulin-like growth factors regulate neuronal differentiation and survival. Neurobiol. Dis. 4 (1997) 201-214
39. Galli C., Meucci O., Scorziello A., Werge T.M., Calissano P., and Schettini G. Apoptosis in cerebellar granule cells is blocked by high KCl, forskolin, and IGF-1 through distinct mechanisms of action: the involvement of intracellular calcium and RNA synthesis. J. Neurosci. 15 (1995) 1172-1179
40. Gatford K.L., Dalitz P.A., Cock M.L., Harding R., and Owens J.A. Acute ethanol exposure in pregnancy alters the insulin-like growth factor axis of fetal and maternal sheep. Am. J. Physiol. Endocrinol. Metab. 292 (2007) E494-500
41. Ghiselli G., Chen J., Kaou M., Hallak H., and Rubin R. Ethanol inhibits fibroblast growth factor-induced proliferation of aortic smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 1808-1813
42. Goodlett C.R., and Eilers A.T. Alcohol-induced Purkinje cell loss with a single binge exposure in neonatal rats: a stereological study of temporal windows of vulnerability. Alcohol. Clin. Exp. Res. 21 (1997) 738-744
43. Goodlett C.R., and Horn K.H. Mechanisms of alcohol-induced damage to the developing nervous system. Alcohol. Res. Health 25 (2001) 175-184
44. Goodlett C.R., and Johnson T.B. Neonatal binge ethanol exposure using intubation: timing and dose effects on place learning. Neurotoxicol. Teratol. 19 (1997) 435-446
45. Goodlett C.R., Thomas J.D., and West J.R. Long-term deficits in cerebellar growth and rotarod performance of rats following "binge-like" alcohol exposure during the neonatal brain growth spurt. Neurotoxicol. Teratol. 13 (1991) 69-74
46. Granato A. Altered organization of cortical interneurons in rats exposed to ethanol during neonatal life. Brain Res. 1069 (2006) 23-30
47. Guevara-Aguirre J., Rosenbloom A.L., Vasconez O., Martinez V., Gargosky S.E., Allen L., and Rosenfeld R.G. Two-year treatment of growth hormone (GH) receptor deficiency with recombinant insulin-like growth factor I in 22 children: comparison of two dosage levels and to GH-treated GH deficiency. J. Clin. Endocrinol. Metab. 82 (1997) 629-633
48. Hallak H., Seiler A.E., Green J.S., Henderson A., Ross B.N., and Rubin R. Inhibition of insulin-like growth factor-I signaling by ethanol in neuronal cells. Alcohol. Clin. Exp. Res. 25 (2001) 1058-1064
49. Harris S.J., Wilce P., and Bedi K.S. Exposure of rats to a high but not low dose of ethanol during early postnatal life increases the rate of loss of optic nerve axons and decreases the rate of myelination. J. Anat. 197 Pt 3 (2000) 477-485
50. Heaton M.B., Mitchell J.J., Paiva M., and Walker D.W. Ethanol-induced alterations in the expression of neurotrophic factors in the developing rat central nervous system. Brain Res. Dev. Brain Res. 121 (2000) 97-107
51. Heaton M.B., 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 (2003) 249-262
52. Heaton M.B., Paiva M., Swanson D.J., and Walker D.W. Alterations in responsiveness to ethanol and neurotrophic substances in fetal septohippocampal neurons following chronic prenatal ethanol exposure. Brain Res. Dev. Brain Res. 85 (1995) 1-13
53. Kar S., Chabot J.G., and Quirion R. Quantitative autoradiographic localization of [125I]insulin-like growth factor I, [125I]insulin-like growth factor II, and [125I]insulin receptor binding sites in developing and adult rat brain. J Comp. Neurol. 333 (1993) 375-397
54. Kelly S.J., Day N., and Streissguth A.P. Effects of prenatal alcohol exposure on social behavior in humans and other species. Neurotoxicol. Teratol. 22 (2000) 143-149
55. Kumada T., Jiang Y., Cameron D.B., and Komuro H. How does alcohol impair neuronal migration?. J. Neurosci. Res. 85 (2007) 465-470
56. Lee W.H., Javedan S., and Bondy C.A. Coordinate expression of insulin-like growth factor system components by neurons and neuroglia during retinal and cerebellar development. J. Neurosci. 12 (1992) 4737-4744
57. Light K.E., Brown D.P., Newton B.W., Belcher S.M., and Kane C.J. Ethanol-induced alterations of neurotrophin receptor expression on Purkinje cells in the neonatal rat cerebellum. Brain Res. 924 (2002) 71-81
58. Liu X.F., Fawcett J.R., Thorne R.G., DeFor T.A., and Frey II W.H. Intranasal administration of insulin-like growth factor-I bypasses the blood-brain barrier and protects against focal cerebral ischemic damage. J. Neurol. Sci. 187 (2001) 91-97
59. Liu X.F., Fawcett J.R., Thorne R.G., and Frey II W.H. Non-invasive intranasal insulin-like growth factor-I reduces infarct volume and improves neurologic function in rats following middle cerebral artery occlusion. Neurosci. Lett. 308 (2001) 91-94
60. 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
61. Luo J., and Miller M.W. Ethanol inhibits basic fibroblast growth factor-mediated proliferation of C6 astrocytoma cells. J. Neurochem. 67 (1996) 1448-1456
62. Luo J., and Miller M.W. Growth factor-mediated neural proliferation: target of ethanol toxicity. Brain. Res. Brain. Res. Rev. 27 (1998) 157-167
63. Luo J., West J.R., and Pantazis N.J. Nerve growth factor and basic fibroblast growth factor protect rat cerebellar granule cells in culture against ethanol-induced cell death. Alcohol. Clin. Exp. Res. 21 (1997) 1108-1120
64. Ma W., Li B.S., Maric D., Zhao W.Q., Lin H.J., Zhang L., Pant H.C., and Barker J.L. Ethanol blocks both basic fibroblast growth factor- and carbachol-mediated neuroepithelial cell expansion with differential effects on carbachol-activated signaling pathways. Neuroscience 118 (2003) 37-47
65. Ma X., Coles C.D., Lynch M.E., Laconte S.M., Zurkiya O., Wang D., and Hu X. Evaluation of corpus callosum anisotropy in young adults with fetal alcohol syndrome according to diffusion tensor imaging. Alcohol. Clin. Exp. Res. 29 (2005) 1214-1222
66. Marcussen B.L., Goodlett C.R., Mahoney J.C., and West J.R. Developing rat Purkinje cells are more vulnerable to alcohol-induced depletion during differentiation than during neurogenesis. Alcohol 11 (1994) 147-156
67. Martin-Algarra R.V., Polache A., Fernandez-Villalba E., Pla Delfina J.M., and Guerri C. Influence of chronic alcohol intake on intestinal taurine and antipyrine transport in pregnant rats. Alcohol. Clin. Exp. Res. 22 (1998) 463-467
68. Mattson S.N., Schoenfeld A.M., and Riley E.P. Teratogenic effects of alcohol on brain and behavior. Alcohol. Res. Health 25 (2001) 185-191
69. McAlhany Jr. R.E., Miranda R.C., Finnell R.H., and West J.R. Ethanol decreases Glial-Derived Neurotrophic Factor (GDNF) protein release but not mRNA expression and increases GDNF-stimulated Shc phosphorylation in the developing cerebellum. Alcohol. Clin. Exp. Res. 23 (1999) 1691-1697
70. McAlhany Jr. R.E., West J.R., and Miranda R.C. Glial-derived neurotrophic factor (GDNF) prevents ethanol-induced apoptosis and JUN kinase phosphorylation. Brain Res. Dev. Brain Res. 119 (2000) 209-216
71. McGee C.L., and Riley E.P. Brain imaging and fetal alcohol spectrum disorders. Ann. Ist. Super. Sanita 42 (2006) 46-52
72. McMorris F.A., Mozell R.L., Carson M.J., Shinar Y., Meyer R.D., and Marchetti N. Regulation of oligodendrocyte development and central nervous system myelination by insulin-like growth factors. Ann. N. Y. Acad. Sci. 692 (1993) 321-334
73. Mitchell J.J., Paiva M., Moore D.B., Walker D.W., and Heaton M.B. A comparative study of ethanol, hypoglycemia, hypoxia and neurotrophic factor interactions with fetal rat hippocampal neurons: a multi-factor in vitro model developmental ethanol effects. Brain Res. Dev. Brain Res. 105 (1998) 241-250
74. Phillips D.E., and Kreuger S.K. Effects of postnatal ethanol exposure on glial cell development in rat optic nerve. Exp. Neurol. 103 (1990) 90-100
75. Pucilowski O., Ayensu W.K., and D'Ercole A.J. Insulin-like growth factor I expression alters acute sensitivity and tolerance to ethanol in transgenic mice. Eur. J. Pharmacol. 305 (1996) 57-62
76. Resnicoff M., Rubini M., Baserga R., and Rubin R. Ethanol inhibits insulin-like growth factor-1-mediated signalling and proliferation of C6 rat glioblastoma cells. Lab. Invest. 71 (1994) 657-662
77. Rienhardt R.R., and Bondy C.A. Insulin-like growth factors cross the blood-brain barrier. Endocrinology 135 (1994) 1753-1761
78. 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
79. Riley E.P., McGee C.L., and Sowell E.R. Teratogenic effects of alcohol: a decade of brain imaging. Am. J. Med. Genet. C Semin. Med. Genet. 127 (2004) 35-41
80. Roebuck T.M., Mattson S.N., and Riley E.P. Behavioral and psychosocial profiles of alcohol-exposed children. Alcohol. Clin. Exp. Res. 23 (1999) 1070-1076
81. Rubert G., Minana R., Pascual M., and Guerri C. Ethanol exposure during embryogenesis decreases the radial glial progenitorpool and affects the generation of neurons and astrocytes. J. Neurosci. Res. 84 (2006) 483-496
82. Sampson P.D., Streissguth A.P., Bookstein F.L., Little R.E., Clarren S.K., Dehaene P., Hanson J.W., and Graham Jr. J.M. Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 56 (1997) 317-326
83. Sara V.R., and Carlsson-Skwirut C. The role of the insulin-like growth factors in the regulation of brain development. Prog. Brain Res. 73 (1988) 87-99
84. Seabold G.K., Luo J., and Miller M.W. Effect of ethanol on neurotrophin-mediated cell survival and receptor expression in cultures of cortical neurons. Brain Res. Dev. Brain Res. 108 (1998) 139-145
85. Seiler A.E., Ross B.N., Green J.S., and Rubin R. Differential effects of ethanol on insulin-like growth factor-I receptor signaling. Alcohol. Clin. Exp. Res. 24 (2000) 140-148
86. Seiler A.E., Ross B.N., and Rubin R. Inhibition of insulin-like growth factor-1 receptor and IRS-2 signaling by ethanol in SH-SY5Y neuroblastoma cells. J. Neurochem. 76 (2001) 573-581
87. Sherrard R.M., Richardson N.A., and Sara V.R. Localisation of insulin-like growth factor-I (IGF-I) immunoreactivity in the olivocerebellar system of developing and adult rats. Brain Res. Dev. Brain Res. 98 (1997) 102-113
88. Silva P.D., Miller K.D., Madden J., and Keegan Jr. K.A. Abnormal fetal heart rate pattern associated with severe intrapartum maternal ethanol intoxication. A case report. J. Reprod. Med. 32 (1987) 144-146
89. Singh S.P., Ehmann S., and Snyder A.K. Ethanol-induced changes in insulin-like growth factors and IGF gene expression in the fetal brain. Proc. Soc. Exp. Biol. Med. 212 (1996) 349-354
90. Sowell E.R., Jernigan T.L., Mattson S.N., Riley E.P., Sobel D.F., and Jones K.L. Abnormal development of the cerebellar vermis in children prenatally exposed to alcohol: size reduction in lobules I-V. Alcohol. Clin. Exp. Res. 20 (1996) 31-34
91. Sowell E.R., Mattson S.N., Kan E., Thompson P.M., Riley E.P., and Toga A.W. Abnormal cortical thickness and brain-behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cereb. Cortex 18 (2008) 136-144
92. Stanton M.E., and Goodlett C.R. Neonatal ethanol exposure impairs eyeblink conditioning in weanling rats. Alcohol. Clin. Exp. Res. 22 (1998) 270-275
93. Tateno M., Ukai W., Ozawa H., Yamamoto M., Toki S., Ikeda H., and Saito T. Ethanol inhibition of neural stem cell differentiation is reduced by neurotrophic factors. Alcohol. Clin. Exp. Res. 28 (2004) 134S-138S
94. Thomas J.D., Fleming S.L., and Riley E.P. MK-801 can exacerbate or attenuate behavioral alterations associated with neonatal alcohol exposure in the rat, depending on the timing of administration. Alcohol. Clin. Exp. Res. 25 (2001) 764-773
95. Thomas J.D., Garcia G.G., Dominguez H.D., and Riley E.P. Administration of eliprodil during ethanol withdrawal in the neonatal rat attenuates ethanol-induced learning deficits. Psychopharmacology (Berl) 175 (2004) 189-195
96. Thomas J.D., Garrison M., and O'Neill T.M. Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol. Teratol. 26 (2004) 35-45
97. Thomas J.D., Goodlett C.R., and West J.R. Alcohol-induced Purkinje cell loss depends on developmental timing of alcohol exposure and correlates with motor performance. Brain Res. Dev. Brain Res. 105 (1998) 159-166
98. Thomas J.D., Leany B.D., and Riley E.P. Differential vulnerability to motor deficits in second replicate HAS and LAS rats following neonatal alcohol exposure. Pharmacol. Biochem. Behav. 75 (2003) 17-24
99. Thomas J.D., Wasserman E.A., West J.R., and Goodlett C.R. Behavioral deficits induced by bingelike exposure to alcohol in neonatal rats: importance of developmental timing and number of episodes. Dev. Psychobiol. 29 (1996) 433-452
100. Thorne R.G., Pronk G.J., Padmanabhan V., and Frey II W.H. Delivery of insulin-like growth factor-I to the rat brain and spinal cord along olfactory and trigeminal pathways following intranasal administration. Neuroscience 127 (2004) 481-496
101. Torres-Aleman I. Serum growth factors and neuroprotective surveillance: focus on IGF-1. Mol. Neurobiol. 21 (2000) 153-160
102. Tran T.D., and Kelly S.J. Critical periods for ethanol-induced cell loss in the hippocampal formation. Neurotoxicol. Teratol. 25 (2003) 519-528
103. Tsai J., Floyd R.L., Green P.P., and Boyle C.A. Patterns and average volume of alcohol use among women of childbearing age. Matern. Child Health J. 11 (2007) 437-445
104. West J.R. Acute and long-term changes in the cerebellum following developmental exposure to ethanol. Alcohol. Alcohol. Suppl. 2 (1993) 199-202
105. Woods K.A., Camacho-Hubner C., Barter D., Clark A.J., and Savage M.O. Insulin-like growth factor I gene deletion causing intrauterine growth retardation and severe short stature. Acta. Paediatr. Suppl. 423 (1997) 39-45
106. Woolfrey K.M., Hunt P.S., and Burk J.A. Postnatal ethanol exposure disrupts signal detection in adult rats. Neurotoxicol. Teratol. 27 (2005) 815-823
107. Yao D.L., Liu X., Hudson L.D., and Webster H.D. Insulin-like growth factor-I given subcutaneously reduces clinical deficits, decreases lesion severity and upregulates synthesis of myelin proteins in experimental autoimmune encephalomyelitis. Life. Sci. 58 (1996) 1301-1306
108. Ye P., Carson J., and D'Ercole A.J. In vivo actions of insulin-like growth factor-I (IGF-I) on brain myelination: studies of IGF-I and IGF binding protein-1 (IGFBP-1) transgenic mice. J. Neurosci. 15 (1995) 7344-7356
109. Ye P., and D'Ercole A.J. Insulin-like growth factor I protects oligodendrocytes from tumor necrosis factor-alpha-induced injury. Endocrinology 140 (1999) 3063-3072
110. Ye P., Lee K.H., and D'Ercole A.J. Insulin-like growth factor-I (IGF-I) protects myelination from undernutritional insult: studies of transgenic mice overexpressing IGF-I in brain. J. Neurosci. Res. 62 (2000) 700-708
111. Ye P., Li L., Richards R.G., DiAugustine R.P., and D'Ercole A.J. Myelination is altered in insulin-like growth factor-I null mutant mice. J. Neurosci. 22 (2002) 6041-6051
112. Ye P., Xing Y., Dai Z., and D'Ercole A.J. In vivo actions of insulin-like growth factor-I (IGF-I) on cerebellum development in transgenic mice: evidence that IGF-I increases proliferation of granule cell progenitors. Brain Res. Dev. Brain Res. 95 (1996) 44-54
113. Zhang F.X., Rubin R., and Rooney T.A. Ethanol induces apoptosis in cerebellar granule neurons by inhibiting insulin-like growth factor 1 signaling. J. Neurochem. 71 (1998) 196-204
114. Zhang W., Ghetti B., and Lee W.H. Decreased IGF-I gene expression during the apoptosis of Purkinje cells in pcd mice. Brain Res. Dev. Brain Res. 98 (1997) 164-176
115. Zhong J., Deng J., Huang S., Yang X., and Lee W.H. High K+ and IGF-1 protect cerebellar granule neurons via distinct signaling pathways. J. Neurosci. Res. 75 (2004) 794-806
116. Zoeller R.T., Butnariu O.V., Fletcher D.L., and Riley E.P. Limited postnatal ethanol exposure permanently alters the expression of mRNAS encoding myelin basic protein and myelin-associated glycoprotein in cerebellum. Alcohol. Clin. Exp. Res. 18 (1994) 909-916