Ethanol consumption during early pregnancy alters the disposition of tangentially migrating GABAergic interneurons in the fetal cortex

Journal of Neuroscience

Volumn 28, Issue 8, 2008, Pages 1854-1864

  Cuzon, Verginia C ^a   Yeh, Pamela W L ^a   Yanagawa, Yuchio ^b   Obata, Kunihiko ^c   Yeh, Hermes H ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Ambient GABA; Fetal alcohol syndrome; GABA A receptor; GFP+ MGE; Medial ganglionic eminence; Telencephalic slice culture

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL DENSITY; CELL DIFFERENTIATION; CELL MIGRATION; CHILD DEVELOPMENT; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FETAL ALCOHOL SYNDROME; FIRST TRIMESTER PREGNANCY; GANGLION; INTERNEURON; MOUSE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL;

ALCOHOL DRINKING; ANIMALS; CELL MOVEMENT; CEREBRAL CORTEX; COCULTURE TECHNIQUES; ETHANOL; FEMALE; FETUS; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PREGNANCY; TIME FACTORS;

EID: 39749083309     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5110-07.2008     Document Type: Article

References (91)

1. - current in mouse hippocampal and cortical neurons. Eur J Pharmacol 187:127-130.
2. A receptors as molecular sites of ethanol action. Direct or indirect actions? Curr Top Med Chem 2:869-885.
3. Anderson SA, Eisestat DD, Shi L, Rubenstein JL (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476.
4. Anderson S, Mione M, Yun K, Rubenstein JL (1999) Differential origins of neocortical projection and local circuit neurons: role for Dlx genes in neocortical interneuronogenesis. Cereb Cortex 9:646-654.
5. Anderson SA, Marin O, Horn C, Jennings K, Rubenstein JL (2001) Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353-363.
6. Bailey CD, Brien JF, Reynolds JN (2004) Chronic prenatal ethanol exposure alters the proportion of GABAergic neurons in layers II/III of the adult guinea pig somatosensory cortex. Neurotoxicol Teratol 26:59-63.
7. Behar TN, Schaffner AE, Colton CA, Somogyi R, Olah Z, Lehel C, Barker JL (1994) GABA-induced chemokinesis and NGF-induced chemotaxis of embryonic spinal cord neurons. J Neurosci 14:29-58.
8. Behar TN, Li YX, Tran HT, Ma W, Dunlap V, Scott C, Barker JL (1996) GABA stimulates chemotaxis and chemokinesis of embryonic neurons via calcium-independent mechanisms. J Neurosci 16:1808-1818.
9. Behar TN, Schaffner AE, Scott CA, Greene CL, Barker JL (2000) GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb Cortex 10:899-909.
10. Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature versus nurture. Nat Rev Neurosci 3:728-739.
11. Ben-Yaakov G, Golan H (2003) Cell proliferation in response to GABA in the postnatal hippocampal slice cultures. Int J Dev Neurosci 21:153-157.
12. Berger-Sweeney J, Hohmann CF (1997) Behavioral consequences of abnormal cortical development: insights into developmental disabilities. Behav Brain Res 86:121-142.
13. Bhave SV, Hoffman PL (1997) Ethanol promotes apoptosis in cerebellar granule cells by inhibiting the trophic effect of NMDA. J Neurochem 68:578-586.
14. A receptors containing the δ subunit. Neuropharmacol 43:492-502.
15. Boehm SL, Ponomarev I, Jennings AW, Whiting PJ, Rosahl TW, Garrett EM, Blendov YA, Harris RA (2004) γ-aminobutyric acid A receptor subunit mutant mice: new perspectives on alcohol actions. Biochem Pharmacol 68:1581-1602.
16. Butt SJ, Fuccillo M, Nery S, Noctor S, Kriegstein A, Corbin JG, Fishell G (2005) The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48:591-604.
17. Cancedda L, Fiumelli H, Chen K, Poo MM (2007) Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 27:5224-5235.
18. Caraiscos V, Elliott EM, You-Ten KE, Cheng VY, Belelli D, Newell JG, Jackson MF, Lambert JJ, Roshal TW, Wafford KA, Macdonald JF, Orser BA (2004) Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by α5 subunit-containing γ-aminobutyric acid type A receptors. Proc Natl Acad Sci USA 101:3662-3667.
19. Carta M, Mameli M, Valenzuela CF (2004) Alcohol enhances GABA-ergic transmission to cerebellar granule cells via an increase in golgi cell excitability. J Neurosci 24:3746-3751.
20. Cartwright MM, Tessmer LL, Smith SM (1998) Ethanol-induced neural crest apoptosis is coincident with their endogenous death, but is mechanistically distinct. Alcohol Clin Exp Res 22:142-149.
21. Cheema ZF, West JR, Miranda RC (2000) Ethanol induces FAS/Apo [apoptosis]-1 mRNA and cell suicide in the developing cerebral cortex. Alcohol Clin Exp Res 24:535-543.
22. Copp AJ, Harding BN (1999) Neuronal migration disorders in humans and in mouse models-an overview. Epilepsy Res 36:133-141.
23. Cuzon VC, Yeh PW, Cheng Q, Yeh HH (2006) Ambient GABA promotes cortical entry of tangentially migrating cells derived from the medial ganglionic eminence. Cereb Cortex 16:1377-1388.
24. A receptor subunit mRNAs in rat cerebral cortex: competitive, quantitative reverse transcriptase-polymerase chain reaction analysis. Mol Pharmacol 48:861-868.
25. A receptor subunit peptide levels in rat cortex during chronic ethanol consumption and withdrawal. J Neurochem 69:126-130.
26. Dikranian K, Qin YQ, Labruyere J, Nemmers B, Olney J (2005) Ethanol-induced neuroapoptosis in the developing rodent cerebellum and related brain stem structures. Dev Brain Res 155:1-13.
27. Flames N, Marin O (2005) Developmental mechanisms underlying the generation of cortical interneuron diversity. Neuron 46:377-381.
28. Fritschy JM, Brunig I (2003) Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol Ther 98:299-323.
29. A-receptor subtypes during postnatal development: an immunohistochemical study. J Neurosci 14:5302-5324.
30. Ge S, Goh ELK, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 493:589-593.
31. A receptor gating kinetics on the α-subunit isoform: implications for structure-function relations and synaptic transmission. J Physiol (Lond) 489:529-543.
32. Gleeson JG, Walsh CA (2000) Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci 23:352-359.
33. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Scahmbra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925.
34. A receptor subunits in rat cortex in a region-specific manner. Alcohol Clin Exp Res 24:1137-1144.
35. A receptor expression: potential mechanisms. Neurochem Inter 37:453-461.
36. Guillemot F (2007) Cell fate specification in the mammalian telencephalon. Prog Neurobiol 83:37-52.
37. Hanchar HJ, Wallner M, Olsen RW (2004) Alcohol effects on γ-aminobutyric acid type A receptors: are extrasynaptic receptors the answer? Life Sci 76:1-8.
38. Hayward ML, Martin AE, Brien JF, Dringenberg HC, Olmstead MC, Reynolds JN (2004) Chronic prenatal ethanol exposure impairs conditioned responding and enhances GABA release in the hippocampus of the adult guinea pig. J Pharmacol Exp Therap 308:644-650.
39. A receptors regulate neocortical neuronal migration in vitro and in vivo. Cereb Cortex 17:138-148.
40. Heng JI, Moonen G, Nguyen L (2007) Neurotransmitters regulate cell migration in the telencephalon. Eur J Neurosci 26:537-546.
41. Herman MA, Jahr CE (2007) Extracellular glutamate concetration in hippocampal slice. J Neurosci 27:9736-9741.
42. + currents. J Neurosci 27:2112-2123.
43. Jimenez D, Lopez-Mascaraque LM, Valverde F, De Carlos JA (2002) Tangential migration in neocortical development. Dev Biol 244:155-169.
44. Kirmse K, Kirischuk S (2006) Ambient GABA constraints the strength of GABAergic synaspses at Cajal-Retzius cells in the developing visual cortex. J Neurosci 26:4216-4227.
45. 2+ fluctuations. J Neurobiol 37:110-130.
46. A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12:4151-4172.
47. Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG (1999) The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci 19:7881-7888.
48. LeMeur K, Galante M, Angulo MC, Audinat E (2007) Tonic activation of NMDA receptors by ambient glutamate of non-synaptic origin in the rat hippocampus. J Physiol (Lond) 580:373-383.
49. LoTurco JJ, Owens DF, Heath JS, Davis MBE, Kriegstein AR (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287-1298.
50. A receptors and alcohol. Alcohol 41:139-143.
51. A receptor subunits. Trends Pharmacol Sci 12:49-51.
52. Manent J-B, Demarque M, Jorquera I, Pellegrino C, Ben-Ari Y, Aniksztejn L, Represa A (2005) A noncanonical release of GABA and glutamate modulates neuronal migration. J Neurosci 25:4755-4765.
53. - channels. J Neurosci 21:2343-2360.
54. Marin O, Rubenstein JL (2001) A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2:780-790.
55. Miller MW (1986) Effects of alcohol on the generation and migration of cerebral cortical neurons. Science 233:1308-1311.
56. Miller MW (1992) Circadian rhythm of cell proliferation in the telencephalic ventricular zone: effect of in utero exposure to ethanol. Brain Res 595:17-24.
57. Miller MW (1993) Migration of cortical neurons is altered by gestational exposure to ethanol. Alcohol Clin Exp Res 17:304-314.
58. Miller MW (1996) Limited ethanol exposure selectively alters the proliferation of precursor cells in the cerebral cortex. Alcohol Clin Exp Res 20:139-143.
59. Mody I, Glykys J, Wei W (2007) A new meaning for "Gin and Tonic": tonic inhibition as the target for ethanol action in the brain. Alcohol 41:145-153.
60. Moore DB, Quintero MA, Ruygrok AC, Walker DW, Heaton MB (1998) Prenatal ethanol exposure reduces parvalbumin-immunoreactive GABAergic neuronal number in the adult rat cingulate cortex. Neurosci Lett 249:25-28.
61. A receptors to ethanol. Alcohol Clin Exp Res 24:965-971.
62. Nakahiro M, Arakawa O, Narahashi T (1991) Modulation of γ-aminobutyric acid receptor-channel complex by alcohols. J Pharmacol Exp Ther 259:235-240.
63. Nakajima K (2007) Control of tangential/non-radial migration of neurons in the developing cerebral cortex. Neurochem Int 51:121-131.
64. Nery S, Fishell G, Corbin JG (2002) The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 5:1279-1287.
65. Nery S, Corbin JG, Fishell G (2003) Dlx2 progenitor migration in wildtype and Nkx2.1 mutant telencephalon. Cereb Cortex 13:895-903.
66. Nguyen L, Rigo JM, Rocher V, Belachew S, Malgrange B, Rogister B, Leprince P, Moonen G (2001) Neurotransmitters as early signals for central nervous system development. Cell Tissue Res 35:187-202.
67. Nishio M, Narahashi T (1990) Ethanol enhancement of GABA-activated chloride current in rat dorsal root ganglion neurons. Brain Res 518:283-286.
68. Nusser Z, Mody I (2002) Selective modulation of tonic and phasic inhibitions in dentate granule cells. J Neurophysiol 87:2624-2628.
69. Okabe M, Ikawa M, Kominani K, Nakanishi T, Nishimune Y (1997) "Green mice" as a source of ubiquitous green cells. FEBS Lett 407:313-319.
70. Owens DF, Boyce LH, Davis MBE, Kriegstein AR (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16:6414-6423.
71. Owens F, Kriegstein AR (2002) Is there more to GABA than synaptic inhibition? Nat Neurosci 3:715-727.
72. A receptor-mediated 36Cl(-) uptake in mesocorticolimbic regions of rat brain. Alcohol Clin Exp Res 25:1270-1275.
73. Paul SM (2006) Alcohol-sensitive GABA receptors and alcohol antagonists. Proc Natl Acad Sci USA 103:8307-8308.
74. A receptor alpha-subunit mRNAs in the developing rat CNS. J Neurosci 12:2888-2900.
75. A receptor beta 2, beta 3, and gamma 2 subunit messenger RNAs during embryogenesis and early postnatal development of the rat central nervous system. Neuroscience 53:1019-1033.
76. A receptor stimulation. J Neurochem 68:631-639.
77. Roberto M, Madamba SG, Moore SD, Tallent MK, Siggins GR (2003) Ethanol increases GABAergic transmission at both pre- and post synaptic sites in rat central amygdala neurons. Proc Natl Acad Sci USA 100:2053-2058.
78. A receptor subtypes: dissecting their pharmacological functions. Trends Pharmacol Sci 22:188-194.
79. Sanchis R, Sancho-Tello M, Guerri C (1986) The effects of chronic alcohol consumption on pregnant rats and their offspring. Alcohol Alcohol 21:295-305.
80. A receptors to increase tonic inhibition. Alcohol 41:211-221.
81. A receptor interactions: a comparison between cell lines and cerebellar purkinjie cells. J Pharmacol Exp Ther 284:768-776.
82. Siggins GR, Roberto M, Nie Z (2005) The tipsy terminal: presynaptic effects of ethanol. Pharmacol Ther 107:80-98.
83. Tamamaki N, Fujimori KE, Takauji R (1997) Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J Neurosci 17:8313-8323.
84. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J-I, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79.
85. Tanaka DH, Maekawa K, Yanagawa Y, Obata K, Murakami F (2006) Multidirectional and multizonal migration of GABAergic interneurons in the developing cerebral cortex. Development 133:2167-2176.
86. Tatebayashi H, Motomura H, Narahashi T (1998) Alcohol modulation of single GABA(A) receptor-channel kinetics. NeuroReport 9:1769-1775.
87. A receptors depend upon subunit composition. Neuron 4:919-928.
88. A receptors expressed in Xenopus oocytes. Science 249:291-293.
89. A receptor expressed in Xenopus oocytes requires 8 amino acids contained in the γ2L subunit. Neuron 7:27-33.
90. Weiner JL, Valenzuela CF (2006) Ethanol modulation of GABAergic transmission: the view from the slice. Pharmacol Ther 111:533-554.
91. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA (2004) Origins of cortical interneuron subtypes. J Neurosci 24:2612-2622.