Effects of early postnatal exposure to ethanol on retinal ganglion cell morphology and numbers of neurons in the dorsolateral geniculate in mice

Alcoholism: Clinical and Experimental Research

Volumn 35, Issue 11, 2011, Pages 2063-2074

  Dursun, Ilknur ^a   Jakubowska Doǧru, Ewa ^a   van der List, Deborah ^b   Liets, Lauren C ^b   Coombs, Julie L ^b   Berman, Robert F ^b  

^a MIDDLE EAST TECHNICAL UNIVERSITY   (Turkey)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Postnatal ethanol; Retinal ganglion cell morphology; Stereological cell counts; Yellow fluorescent protein mice

Indexed keywords

ALCOHOL; YELLOW FLUORESCENT PROTEIN;

ALCOHOL BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; FEMALE; LATERAL GENICULATE BODY; MALE; MOUSE; NERVE CELL; NEWBORN; NONHUMAN; PERINATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA GANGLION CELL;

ANIMALS; ANIMALS, NEWBORN; BACTERIAL PROTEINS; BODY WEIGHT; CELL COUNT; DENDRITES; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; FEMALE; GENICULATE BODIES; LUMINESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; MODELS, ANIMAL; NEURONS; RETINAL GANGLION CELLS;

MUS; MUS MUSCULUS;

EID: 80055118366     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2011.01557.x     Document Type: Article

References (104)

1. Aguilera Y, Ruiz-Gutiérrez V, Prada FA, Martínez JJ, Quesada A, Dorado ME (2004) Alcohol-induced lipid and morphological changes in chick retinal development. Alcohol Clin Exp Res 28:816-823.
2. Andersen SL, Teicher MH (2004) Delayed effects of early stress on hippocampal development. Neuropsychopharmacology 29:1988-1993.
3. Ashwell KW, Zhang LL (1994) Optic nerve hypoplasia in an acute exposure model of the fetal alcohol syndrome. Neurotoxicol Teratol 16:161-167.
4. Badea TC, Nathans J (2004) Quantitative analysis of neuronal morphologies in the mouse retina visualized by using a genetically directed reporter. J Comp Neurol 480:331-351.
5. Barnes DE, Walker DW (1981) Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in the rat hippocampus. Dev Brain Res 1:333-340.
6. Bartesaghi R, Severi S (2002) Effects of early environment on field CA3a pyramidal neuron morphology in the guinea-pig. Neuroscience 110:475-488.
7. Berman RF, Hannigan JH (2000) Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy. Hippocampus 10:94-110.
8. Bhalla S, Kaur K, Akhtar Mahmood A, Mahmood S (2005) Postnatal development of alcohol dehydrogenase in liver & intestine of rats exposed to ethanol in utero. Indian J Med Res 121:39-45.
9. Bonthius DJ, West JR (1990) Alcohol-induced neuronal loss in developing rats: increased brain damage with binge exposure. Alcohol Clin Exp Res 14:107-118.
10. Bruce BB, Biousse V, Dean AL, Newman NJ (2009) Neurologic and ophthalmic manifestations of fetal alcohol syndrome. Rev Neurol Dis 6:13-20.
11. Burrows RC, Shetty AK, Phillips DE (1995) Effects of prenatal alcohol exposure on the postnatal morphology of the rat oculomotor nucleus. Teratology 51:318-328.
12. Calvet MC, Calvet J (1984) Computer assisted analysis of HRP labeled and Golgi stained Purkinje neurons. Prog Neurobiol 23:251-272.
13. Chalupa LM, Williams RW (2008) Eye, Retina, and Visual System of the Mouse. The MIT Press, Cambridge, MA, and London.
14. Chmielewski CE, Hernandez LM, Quesada A, Pozas JA, Picabea L, Prada FA (1997) Effects of ethanol on the inner layers of chick retina during development. Alcohol 14:313-317.
15. Clarren SK, Alvord EC Jr, Sumi SM, Streissguth AP, Smith DW (1978) Brain malformations related to prenatal exposure to ethanol. J Pediatr 92:64-67.
16. Clarren SK, Astley SJ, Bowden DM, Lai H, Milam AH, Rudeen PK, Shoemaker WJ (1990) Neuroanatomic and neurochemical human primate infants exposed abnormalities in non- to weekly doses of ethanol during gestation. Alcohol Clin Exp Res 14:674-683.
17. Climent E, Pascual M, Renau-Piqueras J, Guerri C (2002) Ethanol exposure enhances cell death in the developing cerebral cortex: role of brain-derived neurotrophic factor and its signaling pathways. J Neurosci Res 68:213-225.
18. Coleman LA, Friedlander MJ (2002) Postnatal dendritic development of Y-like geniculocortical relay neurons. Int J Dev Neurosci 20:137-159.
19. Cook CS, Nowotny AZ, Sulik KK (1987) Fetal alcohol syndrome. Eye malformations in a mouse model. Arch Ophthalmol 105:1576-1581.
20. Coombs JL, Van Der List D, Chalupa LM (2007) Morphological properties of mouse retinal ganglion cells during postnatal development. J Comp Neurol 503:803-814.
21. Coombs JL, Van Der List D, Wang GY, Chalupa LM (2006) Morphological properties of mouse retinal ganglion cells. Neuroscience 140:123-136.
22. Dangata YY, Kaufman MH (1997) Morphometric analysis of the postnatal mouse optic nerve following prenatal exposure to alcohol. J Anat 191:49-56.
23. Davies DL, Smith DE (1981) A Golgi study of mouse hippocampal CA1 pyramidal neurons following perinatal ethanol exposure. Neurosci Lett 26:49-54.
24. Diao L, Sun W, Deng Q, He S (2004) Development of the mouse retina: emerging morphological diversity of the ganglion cells. J Neurobiol 61:236-249.
25. Dlugos CA, Rabin RA (2007) Ocular deficits associated with alcohol exposure during zebrafish development. J Comp Neurol 502:497-506.
26. Dobbing J, Sands J (1979) Comparative aspects of the brain growth spurt. Early Hum Dev 311:79-83.
27. Dohrman DP, West JR, Pantazis NJ (1997) 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 21:882-893.
28. Feng G, Mellow RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
29. Frade JM, Bovolenta P, Rodriguez-Tebar A (1999) Neurotrophins and other growth factors in the generation of retinal neurons. Microsc Res Tech 45:243-251.
30. Gonzalez-Burgos I, Alejandre-Gomez M, Olvera-Cortes ME, Perez-Vega MI, Evans S, Feria-Velasco A (2006) Prenatal-through-postnatal exposure to moderate levels of ethanol leads to damage on the hippocampal CA1 field of juvenile rats a stereology and golgi study. Neurosci Res 56:400-408.
31. Goodlett CR, Eilers AT (1997) 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 21:738-744.
32. Goodlett CR, Marcussen BL, West JR (1990) A single day of alcohol exposure during the brain growth spurt induces brain weight restriction and cerebellar Purkinje cell loss. Alcohol 7:107-114.
33. Goodlett CR, Pearlman AD, Lundahl KR (1997) Binge-like alcohol exposure of neonatal rats via intragastric intubation induces both Purkinje cell loss and cortical astrogliosis. Alcohol Clin Exp Res 21:1010-1017.
34. Goodlett CR, Pearlman AD, Lundahl KR (1998) Binge neonatal alcohol intubations induce dose-dependent loss of Purkinje cell. Neurotoxicol Teratol 20:285-292.
35. Green JT, Arenos JD, Dillon CJ (2006) The effects of moderate neonatal ethanol exposure on eyeblink conditioning and deep cerebellar nuclei neuron numbers in the rat. Alcohol 39:135-150.
36. 3H] corticosterone in chick brain during embryonic development. Neurochem Res 6:343-351.
37. Guerri C (2002) Mechanisms involved in central nervous system dysfunctions induced by prenatal ethanol exposure. Neurotox Res 4:327-335.
38. Han JY, Joo Y, Kim YS, Lee YK, Kim HJ, Cho GJ, Choi WS, Kang SS (2005) Ethanol induces cell death by activating caspase-3 in the rat cerebral cortex. Mol Cells 20:189-195.
39. Harris SJ, Wilce P, Bedi KS (2000) 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 197:477-485.
40. Hayashi A, Nagaoka M, Yamada K, Ichitani Y, Miake Y, Okado N (1998) Maternal stress induces synaptic loss and developmental disabilities of offspring maternal stress. Int J Dev Neurosci 16:209-216.
41. Heaton MB, Mitchell JJ, Paiva M (1999) Ethanol-induced alterations in neurotrophin expression in developing cerebellum: relationship to periods of temporal susceptibility. Alcohol Clin Exp Res 23:1637-1642.
42. Heaton MB, Mitchell JJ, Paiva M (2000a) Overexpression of NGF ameliorates ethanol neurotoxicity in the developing cerebellum. J Neurobiol 45:95-104.
43. Heaton MB, Mitchell JJ, Paiva M, Walker DW (2000b) Ethanol-induced alterations in the expression of neurotrophic factors in the developing rat central nervous system. Dev Brain Res 121:97-107.
44. Helfer JL, Calizo LH, Dong WK, Goodlett CR, Greenough WT, Klintsova AY (2009) Binge-like postnatal alcohol exposure triggers cortical gliogenesis in adolescent rats. J Comp Neurol 514:259-271.
45. Ikonomidou C, Bittigau P, Ishimaru MJ, Wozniak DF, Koch C, Genz K (2000) Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 287:1056-1060.
46. Jeon CJ, Strettoi E, Masland RH (1998) The major cell populations of the mouse retina. J Neurosci 18:8936-8946.
47. Jiang Q, Hu Y, Wu P, Cheng X, Li M, Yu D, Deng J (2007) Prenatal alcohol exposure and the neuroapoptosis with long-term effect in visual cortex of mice. Alcohol Alcohol 42:285-290.
48. Jones K, Smith D, Ulleland C, Streissguth A (1973) Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1:1267-1272.
49. Jones KL, Smith DW (1973) Recognition of the fetal alcohol syndrome in early infancy. Lancet 2:999-1001.
50. Kallinikos P, Berhanu M, O'Donnell C, Boulton AJM, Efron N, Malik RA (2004) Corneal nerve tortuosity in diabetic patients with neuropathy. Invest Ophthalmol Vis Sci 45:418-422.
51. Kashyap B, Frederickson LC, Stenkamp DL (2007) Mechanisms for persistent microphthalmia following ethanol exposure during retinal neurogenesis in zebrafish embryos. Vis Neurosci 24:409-421.
52. Kelly SJ, Lawrence CR (2008) Intragastric intubation of alcohol during the perinatal period. Methods Mol Biol 447:101-110.
53. Kennedy LA, Elliott MJ (1986) Ocular changes in the mouse embryo following acute maternal ethanol intoxication. Int J Dev Neurosci 4:311-317.
54. Koehler DE, Moscona AA (1975) Corticosteroid receptors in the neural retina and other tissues of the chick embryo. Arch Biochem Biophys 170:102-113.
55. Kong JH, Fish DR, Rockhill RL, Masland RH (2005) Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits. J Comp Neurol 489:293-310.
56. Krasner J, Eriksson M, Yaffe SJ (1974) Developmental changes in mouse liver alcohol dehydrogenase. Biochem Pharmacol 23:519-522.
57. Lemoine P, Harousseau H, Borteyru JP, Menuet JC (1968) Children of alcoholic parents: abnormalities observed in 127 cases. Ouest Med 8:476-482.
58. Light KE, Brown DP, Newton BW, Belcher SM, Kane CJM (2002) Ethanol-induced alterations of neurotrophin receptor expression on Purkinje cells in the neonatal rat cerebellum. Brain Res 924:71-81.
59. Livy DJ, Miller EK, Maier SE, West JR (2003) Fetal alcohol exposure and temporal vulnerability: effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicol Teratol 25:447-458.
60. Matsui JI, Egana AL, Sponholtz TR, Adolph AR, Dowling JE (2006) Effects of ethanol on photoreceptors and visual function in developing zebrafish. Invest Ophthalmol Vis Sci 47:4589-4597.
61. Miki T, Harris S, Wilce PA, Takeuchi Y, Bedi KS (1999) The effect of the timing of ethanol exposure during early postnatal life on total number of Purkinje cells in rat cerebellum. J Anat 194:423-431.
62. Miki T, Harris SJ, Wilce PA, Takeuchi Y, Bedi KS (2000) Neurons in the hilus region of the rat hippocampus are depleted in number by exposure to alcohol during early postnatal life. Hippocampus 10:284-295.
63. Miki T, Harris SJ, Wilce PA, Takeuchi Y, Bedi KS (2003) Effects of alcohol exposure during early life on neuron numbers in the rat hippocampus. I. Hilus neurons and granule cells. Hippocampus 13:388-398.
64. Miki T, Harris SJ, Wilce PA, Takeuchi Y, Bedi KS (2004) Effects of age and alcohol exposure during early life on pyramidal cell numbers in the CA1-CA3 region of the rat hippocampus. Hippocampus 14:124-134.
65. Miki T, Yokoyama T, Sumitani K, Kusaka T, Warita K, Matsumoto Y, Wang Z, Wilce PA, Bedi SK, Itoh S, Takeuchi Y (2008) Ethanol neurotoxicity and dentate gyrus development. Congenit Anom 48:110-117.
66. Miller MW (1995) Generation of neurons in the rat dentate gyrus and hippocampus: effects of prenatal and postnatal treatment with ethanol. Alcohol Clin Exp Res 19:1500-1509.
67. Mooney SM, Miller MW (2007) Time-specific effects of ethanol exposure on cranial nerve nuclei: gastrulation and neuronogenesis. Exp Neurol 205:56-63.
68. Mooney SM, Napper RM (2005) Early postnatal exposure to alcohol reduces the number of neurons in the occipital but not the parietal cortex of the rat. Alcohol Clin Exp Res 29:683-691.
69. Moulder KL, Fu T, Melbostad H, Cormier RJ, Isenberg KE, Zorumski CF, Mennerick S (2002) Ethanol-induced death of postnatal hippocampal neurons. Neurobiol Dis 10:396-409.
70. Murmu MS, Salomon S, Biala Y, Weinstock M, Braun K, Bock J (2006) Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci 24:1477-1487.
71. Paldino AM, Purpura DP (1979) Branching patterns of hippocampal neurons of human fetus during dendritic differentiation. Exp Neurol 64:620-631.
72. Parks EA, McMechan AP, Hannigan JH, Berman RF (2008) Environmental enrichment alters neurotrophins levels after fetal alcohol exposure in rats. Alcohol Clin Exp Res 32:1741-1751.
73. Parnell SE, Dehart DB, Wills TA, Chen S, Hodge CW, Besheer J, Waage-Baudet HG, Charness ME, Sulik KK (2006) Maternal oral intake mouse model for fetal alcohol spectrum disorders: ocular defects as a measure of effect. Alcohol Clin Exp Res 30:1791-1798.
74. Parson SH, Dhillon B, Findlater GS, Kaufman MH (1995) Optic nerve hypoplasia in the fetal alcohol syndrome: a mouse model. J Anat 186:313-320.
75. Parson SH, Sojitra NM (1995) Loss of myelinated axons is specific to the central nervous system in a mouse model of the fetal alcohol syndrome. J Anat 187:739-748.
76. Perez-Torrero E, Duran P, Granados P, Gutierrez-Ospina G, Cintra L, Diaz-Cintra S (1997) Effects of acute prenatal ethanol exposure on Bergmann glia cells early postnatal development. Brain Res 746:305-308.
77. Phillips DE, Krueger SK, Rydquist JE (1991) Short- and long-term effects of combined pre- and postnatal ethanol exposure (three trimester equivalency) on the development of myelin and axons in rat optic nerve. Int J Dev Neurosci 9:631-647.
78. Pierce DR, West JR (1986) Alcohol-induced microencephaly during the third trimester equivalent: relationship to dose and blood alcohol concentration. Alcohol 3:185-191.
79. Pinazo-Duran MD, Renau-Piqueras J, Guerri C (1993) Developmental changes in the optic nerve related to ethanol consumption in pregnant rats: analysis of the ethanol-exposed optic nerve. Teratology 48:305-322.
80. Pinazo-Duran MD, Renau-Piqueras J, Guerri C, Strömland K (1997) Optic nerve hypoplasia in fetal alcohol syndrome: an update. Eur J Ophthalmol 7:262-270.
81. Pons S, Zanon-Moreno V, Melo P, Vila V, Gallego-Pinazo R, Pinazo-Duran MD (2007) Optic neuropathy induced by prenatal drug or alcohol exposure. Arch Soc Esp Oftalmol 82:21-26.
82. Qiang M, Wang MW, Elberger AJ (2002) Second trimester prenatal alcohol exposure alters development of rat corpus callosum. Neurotoxicol Teratol 24:719-732.
83. Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108:511-533.
84. Riley EP, Mattson SN, Sowell ER, Jernigan TL, Sobel DF, Jones KL (1995) Abnormalities of the corpus callosum in children prenatally exposed to alcohol. Alcohol Clin Exp Res 19:1198-1202.
85. Samoraski T, Lancaster F, Wiggins RC (1986) Fetal ethanol exposure: a morphometric analysis of myelination in the optic nerve. Int J Dev Neurosci 4:369-374.
86. Serbus DC, Young MW, Light KE (1986) Blood ethanol concentrations following intragastric intubation of neonatal rat pups. Neurobehav Toxicol Teratol 8:403-406.
87. Smith DE, Foundas A, Canale J (1986) Effect of perinatally administered ethanol on the development of the cerebellar granule cell. Exp Neurol 92:491-501.
88. Stepanyants A, Tamás G, Chklovskii DB (2004) Class-specific features of neuronal wiring. Neuron 43:251-259.
89. Streissguth AP, Landesman-Dwyer S, Martin JC, Smith DW (1980) Teratogenic effects of alcohol in humans and laboratory animals. Science 209:353-361.
90. Strömland K (1987) Ocular involvement in the fetal alcohol syndrome. Surv Ophthalmol 31:277-284.
91. Strömland K (2004) Visual impairment and ocular abnormalities in children with fetal alcohol syndrome. Addict Biol 9:153-157.
92. Strömland K, Pinazo-Duran MD (1994) Optic nerve hypoplasia: comparative effects in children and rats exposed to alcohol during pregnancy. Teratology 50:100-111.
93. Strömland K, Pinazo-Duran MD (2002) Ophthalmic involvement in fetal alcohol syndrome: clinical and animal model studies. Alcohol Alcohol 37:2-8.
94. Sun W, Li N, He S (2002) Large-scale morphological survey of mouse retinal ganglion cells. Vis Neurosci 19:483-493.
95. Tenkova T, Young C, Dikranian K, Labruyere J, Olney JW (2003) Ethanol induced apoptosis in the developing visual system during synaptogenesis. Invest Ophthalmol Vis Sci 44:2809-2817.
96. Thomas JD, Goodlett CR, West JR (1998) Alcohol-induced Purkinje cell loss depends on developmental timing of alcohol exposure and correlates with motor performance. Dev Psychobiol 29:433-452.
97. Tran TD, Cronise K, Marino MD, Jenkins WJ, Kelly SJ (2000) Critical periods for the effects of alcohol exposure on brain weight, body weight, activity and investigation. Behav Brain Res 116:99-110.
98. Tran TD, Kelly SJ (2003) Critical periods for ethanol-induced cell loss in the hippocampal formation. Neurotoxicol Teratol 25:519-528.
99. Tufan AC, Abbana C, Akdogan I, Erdogan D, Ozogul C (2007) The effect of in ovo ethanol exposure on retina and optic nerve in a chick embryo model system. Reprod Toxicol 23:75-82.
100. Weinstock M (2001) Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65:427-451.
101. West MJ (1993) New stereological methods for counting neurons. Neurobiol Aging 14(4):275-285.
102. Whitcher LT, Klintsova AY (2008) Postnatal binge-like alcohol exposure reduces spine density without affecting dendritic morphology in rat mPFC. Synapse 62:566-573.
103. Yanni PA, Lindsley TA (2000) Ethanol inhibits development of dendrites and synapses in rat hippocampal pyramidal neuron cultures. Brain Res Dev Brain Res 120:233-243.
104. Zhang H, Li YC, Young AP (1993) Protein kinase A activation of glucocorticoid-mediated signaling in the developing retina. Proc Natl Acad Sci USA 90:3880-3884.