A single exposure to alcohol during brain development induces microencephaly and neuronal losses in genetically susceptible mice, but not in wild type mice

NeuroToxicology

Volumn 30, Issue 3, 2009, Pages 459-470

  de Licona, Hannah Klein ^a   Karacay, Bahri ^a   Mahoney, Jo ^a   McDonald, Elizabeth ^a   Luang, Thirath ^a   Bonthius, Daniel J ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Fetal alcohol syndrome; Neuronal nitric oxide synthase; Nitric oxide; nNOS

Indexed keywords

ALCOHOL; NEURONAL NITRIC OXIDE SYNTHASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DAMAGE; BRAIN DEVELOPMENT; BRAIN GROWTH; BRAIN SIZE; CELL COUNT; CELL LOSS; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENETIC SUSCEPTIBILITY; HIPPOCAMPUS; INJECTION; MALE; MICROCEPHALY; MOUSE; NERVE CELL; NERVE CELL NECROSIS; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRENATAL EXPOSURE; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; CELL COUNT; CEREBRAL CORTEX; ETHANOL; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICROCEPHALY; NEURONS; NEUROTOXICITY SYNDROMES; NITRIC OXIDE SYNTHASE TYPE I; RANDOM ALLOCATION; TIME FACTORS;

MUS;

EID: 67349123382     PISSN: 0161813X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuro.2009.01.010     Document Type: Article

References (70)

1. 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
2. Beg A.A., and Baltimore D. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274 (1996) 782-784
3. Bonthius D.J., and West J.R. Alcohol-induced neuronal loss in developing rats: Increased brain damage with binge exposure. Alcohol Clin Exp Res 14 (1990) 107-118
4. 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
5. Bonthius D.J., and West J.R. Acute and long-term neuronal deficits in the rat olfactory bulb following alcohol exposure during the brain growth spurt. Neurotoxicol Teratol 13 (1991) 611-619
6. Bonthius D.J., Goodlett C.R., and West J.R. Blood alcohol concentration and severity of microencephaly in neonatal rats depend on the pattern of alcohol administration. Alcohol 5 (1988) 209-214
7. Bonthius D.J., Bonthius N.E., Napper R.M.A., 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
8. Bonthius D.J., Pantazis N., Karacay B., Bonthius N.E., Taggard D.A., and Lothman E.W. Alcohol exposure during the brain growth spurt promotes hippocampal seizures, kindling and spreading depression. Alcohol Clin Exp Res 25 (2001) 734-745
9. Bonthius D.J., Woodhouse J., Bonthius N.E., Taggard D.A., and Lothman E.W. Reduced seizure threshold and hippocampal cell loss in rats exposed to alcohol during the brain growth spurt. Alcohol Clin Exp Res 25 (2001) 70-82
10. Bonthius D.J., Tzouras G., Karacay B., Mahoney J., Hutton A., McKim R., et al. Deficiency of neuronal nitric oxide synthase (nNOS) worsens alcohol-induced microencephaly and neuronal loss in developing mice. Dev Brain Res 138 (2002) 45-59
11. 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. Dev Brain Res 140 (2003) 15-28
12. Bonthius D.J., Karacay B., Dai D., Hutton A., and Pantazis N.J. The NO-cGMP-PKG pathway plays an essential role in the acquisition of ethanol resistance by cerebellar granule neurons. Neurotoxicol Teratol 26 (2004) 47-57
13. Bonthius D.J., McKim R., Koele L., Harb H., Karacay B., Mahoney J., et al. Use of frozen sections to determine neuronal number in the murine hippocampus and neocortex using the optical disector and optical fractionator. Brain Res Protocol 14 (2004) 45-57
14. Bonthius D.J., McKim R.A., Koele L., Harb H., Hutton-Kehrberg A., Mahoney J., et al. Severe alcohol-induced neuronal deficits in the hippocampus and neocortex of neonatal mice genetically deficient for neuronal nitric oxide synthase (nNOS). J Comp Neurol 499 (2006) 290-305
15. Bonthius D.J., Bonthius N.E., Li S., and Karacay B. The protective effect of neuronal nitric oxide synthase (nNOS) against alcohol toxicity depends upon the NO-cGMP-PKG pathway and NF-kappaB. Neurotoxicology 29 (2008) 1080-1091
16. Christoffel K.K., and Salafsky I. Fetal alcohol syndrome in dizygotic twins. J Pediatr 87 (1975) 963-967
17. Chung E., Curtis D., Chen G., Marsden P.A., Twells R., Xu W., et al. Genetic evidence for the neuronal nitric oxide synthase gene (NOS1) as a susceptibility locus for infantile pyloric stenosis. Am J Hum Genet 58 (1996) 363-370
18. Clarren S.K., Alvord E.C., Sumi S.M., Streissguth A.P., and Smith D.W. Brain malformations related to prenatal exposure to ethanol. J Pediatr 92 (1978) 64-67
19. Dawson V.L., Kizushi V.M., Huang P.L., Snyder S.H., and Dawson T.M. Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J Neurosci 16 (1996) 2479-2487
20. Dawson T.M., Sasaki M., Gonzalez-Zulueta M., and Dawson V.L. Regulation of neuronal nitric oxide synthase and identification of novel nitric oxide signaling pathways. In: Mize R.R., Dawson T.M., Dawson V.L., and Friedlander M.J. (Eds). Nitric oxide in brain development, plasticity and disease (1998), Elsevier, New York 3-11
21. Dobbing J., and Sands J. Quantitative growth and development of human brain. Arch Dis Child 48 (1973) 757-767
22. Dobbing J., and Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 3 (1979) 79-83
23. Elliason M.J., Blackshaw S., Schell M.J., and Snyder S.H. Neuronal nitric oxide synthase alternatively spliced forms: prominent functional localizations in the brain. Proc Natl Acad Sci USA 94 (1997) 3396-3410
24. Ethen M.K., Ramadhani T.A., Scheuerle A.E., Canfield M.A., Wyszynski D.F., Druschel C.M., et al. Alcohol consumption by women before and during pregnancy. Matern Child Health J (2008) 10.1007/s10995-008-0328-2
25. Floyd R.L., Decoufle P., and Hungerford D.W. Alcohol use prior to pregnancy recognition. Am J Prev Med 17 (1999) 101-107
26. Floyd R.L., Sobell M., Velasquez M.M., Ingersoll K., Netleman M., Sobell L., et al. Preventing alcohol-exposed pregnancies: a randomized controlled trial. Am J Prev Med 32 (2007) 1-10
27. Franklin K.B.J., and Paxinos G. The mouse brain in stereotaxic coordinates (1997), Academic Press, New York
28. Fryer S.L., Tapert S.F., Mattson S.N., Paulus M.P., Spandoni A.D., and Riley E.P. Prenatal alcohol exposure affects frontal-striatal BOLD response during inhibitory control. Alcohol Clin Exp Res 31 (2007) 1415-1424
29. 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
30. Goodlett C.R., and Johnson T.B. Temporal windows of vulnerability within the third trimester equivalent: why "knowing when" matters. In: Hanigan J., Spear L.P., Spear N.E., and Goodlett C.R. (Eds). Alcohol: effects on brain and development (1999), Lawrence Erlbaum, Mahwah, NJ 59-91
31. Goodlett C.R., Bonthius D.J., Wasserman E.A., and West J.R. An animal model of central nervous system dysfunction associated with fetal alcohol exposure: behavioral and neuroanatomical correlates. In: Wasserman E.A., and Gormezano I. (Eds). Learning and memory: behavioral and biological processes (1992), Lawrence Erlbaum, Englewood, NJ 183-208
32. Goodlett C.R., Pearlman A.D., and Lundahl K.R. Binge neonatal alcohol intubations induce dose-dependent loss of Purkinje cells. Neurotox Teratol 20 (1998) 285-292
33. Graseman H., Drazen J.M., Deykin A., Israel E., De Sanctis G.R.T., and Pillari A. Single tandem repeat polymorphisms in the neuronal nitric oxide synthase gene in different ethnic populations. Hum Hered 49 (1999) 139-141
34. Gundersen H.J.G. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J Microsc 143 (1986) 3-45
35. Gundersen H.J.G., and Jensen E.B. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147 (1987) 229-263
36. Gundersen H.J.G., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., et al. The new stereological tools: disector, fractionator, nucleator, and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96 (1988) 857-881
37. Hall A.V., Antoniou H., Wang Y., Cheung A.H., Arbus M., and Olsen S.L. Structural organization of the human neuronal nitric oxide synthase gene (NOS1). Biol Chem 269 (1994) 33082-33090
38. Heese K., Fiebich B.L., Bauer J., and Otten U. NF-kB modulates liposaccharide-induced microglial nerve growth factor expression. Glia 22 (1998) 401-407
39. Huang P.L., Dawson T.M., Bredt D.S., Snyder S.H., and Fishman M.C. Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75 (1993) 1273-1286
40. Hutton A.M., Pantazis N.J., McKim R.A., and Bonthius D.J. A nitric oxide signaling pathway protects the developing brain against alcohol-induced neuronal death. In: Preedy V.R., and Watson R.R. (Eds). Comprehensive handbook of alcohol related pathology (2004), Elsevier Science, London 873-887
41. Jones K.L., and Smith D.W. Recognition of fetal alcohol syndrome in early infancy. Lancet 2 (1973) 999-1001
42. Karacay B., Li G., Pantazis N.J., and Bonthius D.J. Stimulation of the cAMP pathway protects cultured cerebellar granule neurons against alcohol-induced cell death by activating the neuronal nitric oxide synthase (nNOS) gene. Brain Res 1143 (2007) 34-45
43. Karacay B., Li S., Klein De Licona H., and Bonthius D.J. shRNA mediated CREB silencing increases vulnerability of cerebellar granule neurons to alcohol toxicity. Alcohol Clin Exp Res 31 (2007) 40A
44. Karacay B., Li S., and Bonthius D.J. Maturation-dependent alcohol resistance in the developing mouse: cerebellar neuronal loss and gene expression during alcohol-vulnerable and -resistant periods. Alcohol Clin Exp Res 32 (2008) 1439-1450
45. Kelly S.J., Bonthius D.J., and West J.R. Developmental changes in alcohol pharmacokinetics in rats. Alcohol Clin Exp Res 11 (1987) 281-286
46. Kesmodel U., and Kesmodel P.S. Drinking during pregnancy: attitudes and knowledge among pregnant Danish women, 1998. Alcohol Clin Exp Res 26 (2002) 1553-1560
47. Levecque C., Elbaz A., Clavel J., Richard F., Vidal J.S., Amouyel P., et al. Association between Parkinson's disease and polymorphisms in the nNOS and iNOS genes in a community-based case control study. Hum Mol Genet 12 (2003) 79-86
48. Little R.F. Moderate alcohol use during pregnancy and decreased infant birth weight. Am J Public Health 65 (1977) 1154-1156
49. Mattson S.N., and Riley E.P. A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res 22 (1998) 279-294
50. Monti B., Marri L., and Contestabile A. NMDA receptor-dependent CREB activation in survival of cerebellar granule cells during in vivo and in vitro development. Eur J Neurosci 16 (2002) 1490-1498
51. Nelson R.J., Demas G.E., Huang P.L., Fishman M.C., Dawson V.L., Dawson T.M., et al. Behavioral abnormalities in mice lacking neuronal nitric oxide synthase. Nature 378 (1995) 383-386
52. Olney J.W., Ishimaru M.J., Bittigau P., and Ikonomidou C. Ethanol-induced apoptotic neurodegeneration in the developing brain. Apoptosis 5 (2000) 515-521
53. Peiffer J., Majewski F., Fischbach H., Bierich J.R., and Volk B. Alcohol embry-and fetopathy. Neuropathology of three children and three fetuses. J Neurol Sci 41 (1979) 125-137
54. Riccio A., Ahn S., Davenport C.M., Blendy J.A., and Ginty D.D. Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286 (1999) 2358-2361
55. Riikonen R., Salonen I., Partanen K., and Verho S. Brain perfusion SPECT and MRI in fetal alcohol syndrome. Dev Med Child Neurol 41 (1999) 652-659
56. Sampson P.D., Streissguth A.P., Bookstein F.L., Little R.F., Clarren S.K., Dehaene P., et al. Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 56 (1997) 317-326
57. Sayitoglu M.A., Satik S., Unlucerci Y., Ozbek U., Bekpinar S., Eskazan E., et al. Neuronal Nos (Nos 1) polymorphism in patients with epilepsy: a pilot study. J Neurol Sci (Turkish) 23 (2006) 20-25
58. Sidman R.L., Angevine J.B., and Pierce E.T. Atlas of the mouse brain and spinal cord (1971), Harvard University Press, Cambridge, MA
59. Stephens C.J. Alcohol consumption during pregnancy among southern city women. Drug Alcohol Depend 16 (1985) 19-29
60. Sterio D.C. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134 (1984) 127-136
61. Stratton K., Howe C., and Battaglia F. Fetal alcohol syndrome: diagnosis, epidemiology, prevention and treatment (1996), National Academy Press, Washington, DC 213 pp.
62. Streissguth A.P., and Dehaene P. Fetal alcohol syndrome in twins of alcoholic mothers: concordance of diagnosis and IQ. Am J Med Genet 47 (1993) 857-861
63. Streissguth A.P., and O'Malley K. Neuropsychiatric implications and long-term consequences of fetal alcohol spectrum disorders. Semin Clin Neuropsychol 5 (2000) 177-190
64. Thomas S.E., Kelly S.J., Mattson S.N., and Riley E.P. Comparison of social abilities of children with fetal alcohol syndrome to those of children with similar IQ scores and normal controls. Alcohol Clin Exp Res 22 (1998) 528-533
65. United States Department of Health and Human Services Surgeon General releases advisory on alcohol use in pregnancy, available at: http://www.surgeongeneral/gov//pressreleases/sg0222005.html; 2005 [Accessed 04 November 2008].
66. Walker D.S., Darling Fisher C.S., Sherman A., Wybrecht B., and Kyndely K. Fetal alcohol spectrum disorders prevention: an exploratory study of women's use of, attitudes toward, and knowledge about alcohol. J Am Acad Nurse Pract 17 (2005) 187-193
67. Walton M., Woodgate A.M., Muravlev A., Xu R., During M.J., and Dragunow M. CREB phosphorylation promotes nerve cell survival. J Neurochem 73 (1999) 1836-1842
68. Warren K.R., and Li T.K. Genetic polymorphisms: impact on the risk for fetal alcohol spectrum disorders. Birth Defects Res A Clin Mol Teratol 73 (2005) 195-203
69. West M.J., Coleman P.D., and Flood D.G. Estimating the number of granule cells in the dentate gyrus with the disector. Brain Res 448 (1988) 167-172
70. Xiong H., Yamada K., Jourki H., Kawamura M., Takei N., Han D., et al. Regulation of nerve growth factor release by nitric oxide through cyclic GMP pathway in cortical glial cells. Mol Pharmacol 56 (1999) 339-347