Third trimester-equivalent ethanol exposure is characterized by an acute cellular stress response and an ontogenetic disruption of genes critical for synaptic establishment and function in mice

Developmental Neuroscience

Volumn 36, Issue 6, 2014, Pages 499-519

  Kleiber, Morgan L ^a   Laufer, Benjamin I ^a   Stringer, Randa L ^a   Singh, Shiva M ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Epigenetics; Fetal alcohol spectrum disorders; Gene expression; MicroRNA; Mouse; Neurodevelopment; Synaptogenesis

Indexed keywords

ALCOHOL; BCL2 LIKE 11; CYSTEINE SERINE RICH NUCLEAR PROTEIN 3; GLUTAMATE RECEPTOR SUBUNIT EPSILON 2; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; MICRORNA; NUCLEAR FMRP INTERACTING PROTEIN 1; NUCLEAR PROTEIN; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53; RETINOID X RECEPTOR; SOMATOMEDIN BINDING PROTEIN 3; STEROID RECEPTOR; THYROID HORMONE RECEPTOR; UNCLASSIFIED DRUG;

ACUTE STRESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL INTERACTION; CELL PROLIFERATION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE DISRUPTION; GENE EXPRESSION; GENE ONTOLOGY; GENETIC ASSOCIATION; HISTONE MODIFICATION; MALE; MOUSE; NEWBORN; NONHUMAN; PRENATAL EXPOSURE; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; THIRD TRIMESTER PREGNANCY; UPREGULATION; ANIMAL; BRAIN; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; FETAL ALCOHOL SYNDROME; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; BRAIN; DISEASE MODELS, ANIMAL; EPIGENESIS, GENETIC; ETHANOL; FEMALE; FETAL ALCOHOL SPECTRUM DISORDERS; GENE EXPRESSION; MALE; MICE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; SYNAPTIC TRANSMISSION;

EID: 84910620549     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000365549     Document Type: Article

References (82)

1. Guerri C, Bazinet A, Riley EP: Foetal alcohol spectrum disorders and alterations in brain and behaviour. Alcohol Alcohol 2009;44:108-114.
2. Riley EP, Infante MA, Warren KR: Fetal alcohol spectrum disorders: an overview. Neuropsychol Rev 2011;21:73-80.
3. Green CR, Mihic AM, Nikkel SM, Stade BC, Rasmussen C, Munoz DP, Reynolds JN: Executive function deficits in children with fetal alcohol spectrum disorders (FASD) measured using the Cambridge Neuropsychological Tests Automated Battery (CANTAB). J Child Psychol Psychiatry 2009;50:688-697.
4. Zhou FC, Zhao Q, Liu Y, Goodlett CR, Liang T, McClintick JN, Edenberg HJ, Li L: Alteration of gene expression by alcohol exposure at early neurulation. BMC Genomics 2011;12:124.
5. Hard ML, Abdolell M, Robinson BH, Koren G: Gene-expression analysis after alcohol exposure in the developing mouse. J Lab Clin Med 2005;145:47-54.
6. Bartlett PF, Dutton R, Likiardopoulos V, Brooker G: Regulation of neurogenesis in the embryonic and adult brain by fibroblast growth factors. Alcohol Alcohol Suppl 1994;2:387-394.
7. Green ML, Singh AV, Zhang Y, Nemeth KA, Sulik KK, Knudsen TB: Reprogramming of genetic networks during initiation of the fetal alcohol syndrome. Dev Dyn 2007;236:613-631.
8. Bayer SA, Altman J, Russo RJ, Zhang X: Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 1993;14:83-144.
9. Cohen-Cory S: The developing synapse: construction and modulation of synaptic structures and circuits. Science 2002;298:770-776.
10. Cline H, Haas K: The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: a review of the synaptotrophic hypothesis. J Physiol 2008;586:1509-1517.
11. Wondolowski J, Dickman D: Emerging links between homeostatic synaptic plasticity and neurological disease. Front Cell Neurosci 2013;7:223.
12. Ikonomidou C, Bittigau P, Ishimaru MJ, Wozniak DF, Koch C, Genz K, Price MT, Stefovska V, Horster F, Tenkova T, Dikranian K, Olney JW: Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 2000;287:1056-1060.
13. Olney JW, Wozniak DF, Farber NB, Jevtovic-Todorovic V, Bittigau P, Ikonomidou C: The enigma of fetal alcohol neurotoxicity. Ann Med 2002;34:109-119.
14. Wozniak DF, Hartman RE, Boyle MP, Vogt SK, Brooks AR, Tenkova T, Young C, Olney JW, Muglia LJ: Apoptotic neurodegeneration induced by ethanol in neonatal mice is associated with profound learning/memory deficits in juveniles followed by progressive functional recovery in adults. Neurobiol Dis 2004;17:403-414.
15. Mantha K, Kleiber ML, Singh SM: Neurodevelopmental timing of ethanol exposure may contribute to observed heterogeneity of behavioral deficits in a mouse model of fetal alcohol spectrum disorder (FASD). J Behav Brain Sci 2013;3:85-99.
16. Brocardo PS, Boehme F, Patten A, Cox A, Gil-Mohapel J, Christie BR: Anxiety- and depressionlike behaviors are accompanied by an increase in oxidative stress in a rat model of fetal alcohol spectrum disorders: protective effects of voluntary physical exercise. Neuropharmacology 2012;62:1607-1618.
17. Kleiber ML, Mantha K, Stringer RL, Singh SM: Neurodevelopmental alcohol exposure elicits long-term changes to gene expression that alter distinct molecular pathways dependent on timing of exposure. J Neurodev Disord 2013;5:6.
18. Galindo R, Zamudio PA, Valenzuela CF: Alcohol is a potent stimulant of immature neuronal networks: implications for fetal alcohol spectrum disorder. J Neurochem 2005;94:1500-1511.
19. Servais L, Hourez R, Bearzatto B, Gall D, Schiffmann SN, Cheron G: Purkinje cell dysfunction and alteration of long-term synaptic plasticity in fetal alcohol syndrome. Proc Natl Acad Sci USA 2007;104:9858-9863.
20. Olney JW, Tenkova T, Dikranian K, Qin YQ, Labruyere J, Ikonomidou C: Ethanol-induced apoptotic neurodegeneration in the developing C57BL/6 mouse brain. Brain Res Dev Brain Res 2002;133:115-126.
21. Jorge JC, McIntyre KL, Henderson LP: The function and the expression of forebrain GABA A receptors change with hormonal state in the adult mouse. J Neurobiol 2002;50:137-149.
22. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP: Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003;31:e15.
23. Huang Da W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57.
24. Schmittgen TD, Livak KJ: Analyzing realtime PCR data by the comparative C T method. Nat Protoc 2008;3:1101-1108.
25. Moir RD, Willis IM: Regulation of pol III transcription by nutrient and stress signaling pathways. Biochim Biophys Acta 2013;1829:361-375.
26. Thomas G: An encore for ribosome biogenesis in the control of cell proliferation. Nat Cell Biol 2000;2:E71-E72.
27. Arsenijevic T, Vujovic A, Libert F, Op De Beeck A, Hebrant A, Janssens S, Gregoire F, Lefort A, Bolaky N, Perret J, Caspers L, Willermain F, Delporte C: Hyperosmotic stress induces cell cycle arrest in retinal pigmented epithelial cells. Cell Death Dis 2013;4:e662.
28. Perez-Cadahia B, Drobic B, Davie JR: Activation and function of immediate-early genes in the nervous system. Biochem Cell Biol 2011;89:61-73.
29. Ruzhynsky VA, McClellan KA, Vanderluit JL, Jeong Y, Furimsky M, Park DS, Epstein DJ, Wallace VA, Slack RS: Cell cycle regulator E2F4 is essential for the development of the ventral telencephalon. J Neurosci 2007;27:5926-5935.
30. Rosenstein JM, Krum JM, Ruhrberg C: VEGF in the nervous system. Organogenesis 2010;6:107-114.
31. Dikranian K, Qin YQ, Labruyere J, Nemmers B, Olney JW: Ethanol-induced neuroapoptosis in the developing rodent cerebellum and related brain stem structures. Brain Res Dev Brain Res 2005;155:1-13.
32. Avdulov NA, Wood WG, Harris RA: Effects of ethanol on structural parameters of rat brain membranes: relationship to genetic differences in ethanol sensitivity. Alcohol Clin Exp Res 1994;18:53-59.
33. Kleene R, Schachner M: Glycans and neural cell interactions. Nat Rev Neurosci 2004;5:195-208.
34. De Wit J, O'Sullivan ML, Savas JN, Condomitti G, Caccese MC, Vennekens KM, Yates JR 3rd, Ghosh A: Unbiased discovery of glypican as a receptor for LRRTM4 in regulating excitatory synapse development. Neuron 2013;79:696-711.
35. Tomas M, Fornas E, Megias L, Duran JM, Portoles M, Guerri C, Egea G, Renau-Piqueras J: Ethanol impairs monosaccharide uptake and glycosylation in cultured rat astrocytes. J Neurochem 2002;83:601-612.
36. Binkhorst M, Wortmann SB, Funke S, Kozicz T, Wevers RA, Morava E: Glycosylation defects underlying fetal alcohol spectrum disorder: a novel pathogenetic model. 'When the wine goes in, strange things come out' - ST Coleridge, The Piccolomini. J Inherit Metab Dis 2012;35:399-405.
37. Vazquez DM: Stress and the developing limbichypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology 1998;23:663-700.
38. Hellemans KG, Sliwowska JH, Verma P, Weinberg J: Prenatal alcohol exposure: fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci Biobehav Rev 2010;34:791-807.
39. Hellemans KG, Verma P, Yoon E, Yu W, Weinberg J: Prenatal alcohol exposure increases vulnerability to stress and anxiety-like disorders in adulthood. Ann NY Acad Sci 2008;1144:154-175.
40. Weinberg J, Sliwowska JH, Lan N, Hellemans KG: Prenatal alcohol exposure: foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome. J Neuroendocrinol 2008;20:470-488.
41. Weinstock M: Intrauterine factors as determinants of depressive disorder. Isr J Psychiatry Relat Sci 2010;47:36-45.
42. Li QX, Ke N, Sundaram R, Wong-Staal F: NR4A1, 2, 3: an orphan nuclear hormone receptor family involved in cell apoptosis and carcinogenesis. Histol Histopathol 2006;21:533-540.
43. Nakajima Y, Yamada M, Taguchi R, Shibusawa N, Ozawa A, Tomaru T, Hashimoto K, Saito T, Tsuchiya T, Okada S, Satoh T, Mori M: NR4A1 (Nur77) mediates thyrotropin-releasing hormone-induced stimulation of transcription of the thyrotropin β gene: analysis of TRH knockout mice. PLoS One 2012;7:e40437.
44. Dawson MI, Xia Z: The retinoid X receptors and their ligands. Biochim Biophys Acta 2012;1821:21-56.
45. Grummer MA, Zachman RD: Prenatal ethanol consumption alters the expression of cellular retinol binding protein and retinoic acid receptor mRNA in fetal rat embryo and brain. Alcohol Clin Exp Res 1995;19:1376-1381.
46. Kane MA, Folias AE, Wang C, Napoli JL: Ethanol elevates physiological all-trans-retinoic acid levels in select loci through altering retinoid metabolism in multiple loci: a potential mechanism of ethanol toxicity. FASEB J 2010;24:823-832.
47. Kumar A, Singh CK, Di Pette DD, Singh US: Ethanol impairs activation of retinoic acid receptors in cerebellar granule cells in a rodent model of fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2010;34:928-937.
48. Huang JK, Jarjour AA, Nait Oumesmar B, Kerninon C, Williams A, Krezel W, Kagechika H, Bauer J, Zhao C, Baron-Van Evercooren A, Chambon P, Ffrench-Constant C, Franklin RJ: Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat Neurosci 2011;14:45-53.
49. Lu L, Airey DC, Williams RW: Complex trait analysis of the hippocampus: mapping and biometric analysis of two novel gene loci with specific effects on hippocampal structure in mice. J Neurosci 2001;21:3503-3514.
50. Alarcon JM, Hodgman R, Theis M, Huang YS, Kandel ER, Richter JD: Selective modulation of some forms of Schaffer collateral-CA1 synaptic plasticity in mice with a disruption of the CPEB-1 gene. Learn Mem 2004;11:318-327.
51. Berger-Sweeney J, Zearfoss NR, Richter JD: Reduced extinction of hippocampal-dependent memories in CPEB knockout mice. Learn Mem 2006;13:4-7.
52. Wells DG, Richter JD, Fallon JR: Molecular mechanisms for activity-regulated protein synthesis in the synapto-dendritic compartment. Curr Opin Neurobiol 2000;10:132-137.
53. Cserep C, Szabadits E, Szonyi A, Watanabe M, Freund TF, Nyiri G: NMDA receptors in GABAergic synapses during postnatal development. PLoS One 2012;7:e37753.
54. Wang DD, Kriegstein AR: GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J Neurosci 2008;28:5547-5558.
55. Lujan R, Shigemoto R, Lopez-Bendito G: Glutamate and GABA receptor signalling in the developing brain. Neuroscience 2005;130:567-580.
56. Yashiro K, Philpot BD: Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 2008;55:1081-1094.
57. Gambrill AC, Barria A: NMDA receptor subunit composition controls synaptogenesis and synapse stabilization. Proc Natl Acad Sci USA 2011;108:5855-5860.
58. Killisch I, Dotti CG, Laurie DJ, Luddens H, Seeburg PH: Expression patterns of GABA A receptor subtypes in developing hippocampal neurons. Neuron 1991;7:927-936.
59. Bolton MM, Blanpied TA, Ehlers MD: Localization and stabilization of ionotropic glutamate receptors at synapses. Cell Mol Life Sci 2000;57:1517-1525.
60. Malenka RC, Bear MF: LTP and LTD: an embarrassment of riches. Neuron 2004;44:5-21.
61. Chen CP, Kuhn P, Advis JP, Sarkar DK: Prenatal ethanol exposure alters the expression of period genes governing the circadian function of β-endorphin neurons in the hypothalamus. J Neurochem 2006;97:1026-1033.
62. Earnest DJ, Chen WJ, West JR: Developmental alcohol and circadian clock function. Alcohol Res Health 2001;25:136-140.
63. Sakata-Haga H, Dominguez HD, Sei H, Fukui Y, Riley EP, Thomas JD: Alterations in circadian rhythm phase shifting ability in rats following ethanol exposure during the third trimester brain growth spurt. Alcohol Clin Exp Res 2006;30:899-907.
64. Girotti M, Weinberg MS, Spencer RL: Differential responses of hypothalamus-pituitaryadrenal axis immediate early genes to corticosterone and circadian drive. Endocrinology 2007;148:2542-2552.
65. Bastien J, Rochette-Egly C: Nuclear retinoid receptors and the transcription of retinoidtarget genes. Gene 2004;328:1-16.
66. Chambon P: A decade of molecular biology of retinoic acid receptors. FASEB J 1996;10:940-954.
67. Wilcoxon JS, Kuo AG, Disterhoft JF, Redei EE: Behavioral deficits associated with fetal alcohol exposure are reversed by prenatal thyroid hormone treatment: a role for maternal thyroid hormone deficiency in FAE. Mol Psychiatry 2005;10:961-971.
68. Lane MA, Bailey SJ: Role of retinoid signalling in the adult brain. Prog Neurobiol 2005;75:275-293.
69. Alfos S, Boucheron C, Pallet V, Higueret D, Enderlin V, Beracochea D, Jaffard R, Higueret P: A retinoic acid receptor antagonist suppresses brain retinoic acid receptor overexpression and reverses a working memory deficit induced by chronic ethanol consumption in mice. Alcohol Clin Exp Res 2001;25:1506-1514.
70. Golini RS, Delgado SM, Navigatore Fonzo LS, Ponce IT, Lacoste MG, Anzulovich AC: Daily patterns of clock and cognition-related factors are modified in the hippocampus of vitamin A-deficient rats. Hippocampus 2012;22:1720-1732.
71. Laufer BI, Mantha K, Kleiber ML, Diehl EJ, Addison SM, Singh SM: Long-lasting alterations to DNA methylation and ncRNAs could underlie the effects of fetal alcohol exposure in mice. Dis Model Mech 2013;6:977-992.
72. Bekdash RA, Zhang C, Sarkar DK: Gestational choline supplementation normalized fetal alcohol-induced alterations in histone modifications, DNA methylation, and POMC gene expression in β-endorphin-producing POMC neurons of the hypothalamus. Alcohol Clin Exp Res 2013;37:1133-1142.
73. Miranda RC: MicroRNAs and fetal brain development: implications for ethanol teratology during the second trimester period of neurogenesis. Front Genet 2011;3:77.
74. Veazey KJ, Carnahan MN, Muller D, Miranda RC, Golding MC: Alcohol-induced epigenetic alterations to developmentally crucial genes regulating neural stemness and differentiation. Alcohol Clin Exp Res 2013;37:1111-1122.
75. Butler R, Bates GP: Histone deacetylase inhibitors as therapeutics for polyglutamine disorders. Nat Rev Neurosci 2006;7:784-796.
76. Vogel-Ciernia A, Wood MA: Neuron-specific chromatin remodeling: a missing link in epigenetic mechanisms underlying synaptic plasticity, memory, and intellectual disability disorders. Neuropharmacology 2014;80:18-27.
77. Conway GD, O'Bara MA, Vedia BH, Pol SU, Sim FJ: Histone deacetylase activity is required for human oligodendrocyte progenitor differentiation. Glia 2012;60:1944-1953.
78. Parra M, Verdin E: Regulatory signal transduction pathways for class IIA histone deacetylases. Curr Opin Pharmacol 2010;10:454-460.
79. Mejia LA, Litterman N, Ikeuchi Y, De La Torre-Ubieta L, Bennett EJ, Zhang C, Harper JW, Bonni A: A novel Hap1-Tsc1 interaction regulates neuronal mTORC1 signaling and morphogenesis in the brain. J Neurosci 2013;33:18015-18021.
80. Orlova KA, Crino PB: The tuberous sclerosis complex. Ann NY Acad Sci 2010;1184:87-105.
81. Olney JW: Fetal alcohol syndrome at the cellular level. Addict Biol 2004;9:137-149, discussion 151.
82. Dobbing J: The later growth of the brain and its vulnerability. Pediatrics 1974;53:2-6.