Ethanol effects on GABA-gated current in a model of increased α4βδ GABAA receptor expression depend on time course and preexposure to low concentrations of the drug

Alcohol

Volumn 41, Issue 3, 2007, Pages 223-231

  Smith, Sheryl S ^a   Gong, Qi Hua ^a  

^a SUNY Downstate Medical Center   (United States)

Author keywords

Acute tolerance; Alcohol; Allopregnanolone; Delta subunit; Ethanol; GABA; GABAA receptor

Indexed keywords

3 ALPHA HYDROXIDE 5 BETA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; ALCOHOL; STEROID; UNCLASSIFIED DRUG;

CELL ISOLATION; CONTROLLED STUDY; DESENSITIZATION; DOSE RESPONSE; FEMALE; HIPPOCAMPUS; MEMBRANE CURRENT; NONHUMAN; PATCH CLAMP; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; REVIEW; WHOLE CELL;

ANIMALS; BLOTTING, WESTERN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHYSIOLOGY; ETHANOL; FEMALE; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; ION CHANNEL GATING; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, LONG-EVANS; RECEPTORS, GABA-A; STEROIDS;

RATTUS;

EID: 34250776138     PISSN: 07418329     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.alcohol.2007.04.007     Document Type: Review

References (71)

1. Akk G., Bracamontes J., and Steinbach J.H. Activation of GABA (A) receptors containing the alpha4 subunit by GABA and pentobarbital. J. Physiol. 556 (2004) 387-399
2. Akk G., Li P., Manion B.D., Evers A.S., and Steinback J.H. Ethanol modulates the interaction of the endogenous neurosteroid allopregnanolone with the alpha1beta2gamma2 L GABA-A receptor. Mol. Pharmacol. 71 (2007) 461-472
3. Bennett R.H., Cherek D.R., and Spiga R. Acute and chronic alcohol tolerance in humans: effects of dose and consecutive days of exposure. Alcohol. Clin. Exp. Res. 17 (2005) 740-745
4. Borghese C.M., Storustovu S., Ebert B., Herd M.B., Belelli D., Lambert J.J., Marshall G., Wafford K.A., and Harris R.A. The delta subunit of GABA-A receptors does not confer sensitivity to low doses of ethanol. J. Pharmacol. Exp. Ther. 316 (2006) 1360-1368
5. Brown N., Kerby J., Bonnert T.P., Whiting P.J., and Wafford K.A. Pharmacological characterization of a novel cell line expressing human alpha (4)beta (3)delta GABA (A) receptors. Br. J. Pharmacol. 136 (2002) 965-974
6. Buck K., and Harris R. BDZ agonist and inverse agonist actions on GABA-A receptor-operated chloride channels. II. Chronic effects of ethanol. J. Pharmacol. Exp. Ther. 253 (1990) 713-719
7. Burkat P., Yang J., and Gingrich K. Dominant gating governing transient GABA (A) receptor activity: a first latency and Po/o analysis. J. Neurosci. 21 (2001) 7026-7036
8. Caraiscos V.B., Elliott E.M., You-Ten K.E., Cheng V.Y., Belelli D., Newell J.G., Jackson M.F., Lambert J.J., Rosahl T.W., Wafford K., et al. Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha 5 subunit-containing gamma-aminobutyric acid type A receptors. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 3662-3667
9. Carta M., Mameli M., and Valenzuela C.F. Alcohol enhances GABAergic transmission to cerebellar granule cells via an increase in Golgi cell excitability. J. Neurosci. 24 (2004) 3746-3751
10. Chang Y., Ghanasah E., Chen Y., Ye J., and Weiss D.S. Desensitization mechanism of GABA receptors revealed by single oocyte binding and receptor function. J. Neurosci. 22 (2002) 7982-7990
11. Chang Y., Wang R., Barot S., and Weiss D.S. Stoichiometry of a recombinant GABA-A receptor. J. Neurosci. 16 (1990) 534-541
12. Choi D.S., Wang D., Dadgar J., Chang W.S., and Messing R.O. Conditional rescue of protein kinase C epsilon regulates ethanol preference and hypnotic sensitivity in adult mice. J. Neurosci. 22 (2002) 9905-9911
13. Cohen H.L., Poresz B., and Begleiter H. The effects of ethanol on EEG activity in males at risk for alcoholism. Electroencephalogr. Clin. Neurophysiol. 86 (1993) 368-376
14. A receptor subunit peptide levels in rat cortex during chronic ethanol consumption and withdrawal. J. Neurochem. 69 (1997) 126-130
15. Doty P., Kirk J.M., Cramblett M.J., and de Wit H. Behavioral responses to ethanol in light and moderate social drinkers following naltrexone pretreatment. Drug Alcohol Depend. 47 (1997) 109-116
16. Endicott J., Amsterdam J., Eriksson E., Frank E., Freeman E., Hirschfeld R., Ling F., Parry B., Pearlstein T., Rosenbaum J., et al. Is premenstrual dysphoric disorder a distinct clinical entity?. J. Womens Health Gend. Based Med. 8 (1999) 663-679
17. Engel S.R., Purdy R.H., and Grant K.A. Characterization of discriminative stimulus effects of the neuroactive steroid pregnanolone. J. Pharmacol. Exp. Ther. 297 (2001) 489-495
18. Glykys J., Peng Z., Chandra D., Homanics G.E., Houser C.R., and Mody I. A new naturally occurring GABA-A receptor subunit partnership with high sensitivity to ethanol. Nat. Neurosci. 10 (2007) 40-48
19. A receptor subunit levels in association with increased anxiety. Brain Res. 910 (2001) 55-66
20. Gulinello M., and Smith S.S. Anxiogenic effects of neurosteroid exposure: sex differences and altered GABA-A receptor pharmacology in adult rats. J. Pharmacol. Exp. Ther. 305 (2003) 541-548
21. A receptor currents in mouse fibroblasts. J. Physiol. 514 (1999) 27-45
22. Hanchar H.J., Chutsrinopkun P., Meera P., Supavilai P., Sieghart W., Wallner M., and Olsen R.W. Ethanol potently and competitively inhibits binding of the alcohol antagonist Ro15-4513 to alpha4/6-beta3-delta GABA-A receptors. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 8546-8551
23. Hanchar H.J., Dodson P.D., Olsen R.W., Otis T.S., and Wallner M. Alcohol-induced motor impairment caused by increased extrasynaptic GABA (A) receptor activity. Nat. Neurosci. 8 (2005) 339-345
24. Hiltunen A.J. Acute alcohol tolerance in social drinkers: changes in subjective effects dependent on the alcohol dose and prior alcohol experience. Alcohol 14 (1997) 373-378
25. Hiltunen A.J., Saxon L., Skagerberg S., and Borg S. Acute tolerance during intravenous infusion of alcohol: comparison of performance during ascending and steady state concentrations-a pilot study. Alcohol 22 (2000) 69-74
26. Jones A.E., McBride W.J., Murphy J.M., Lumeng L., Li T., Shekar A., and McKinzie D.L. Effects of ethanol on startle responding in alcohol-preferring and -non-preferring rats. Pharmacol. Biochem. Behav. 67 (2000) 313-318
27. Jung S., Akabas M.H., and Harris R.A. Functional and structural analysis of the GABA-A receptor alpha-1 subunit during channel gating and alcohol modulation. J. Biol. Chem. 280 (2005) 308-316
28. Kalant H., LeBlanc A.E., Wilson A., and Homatidis S. Sensorimotor and physiological effects of various alcoholic beverages. Can. Med. Assoc. J. 112 (1975) 953-958
29. Koob G.F., Mendelson W.B., Schafer J., Wall T.L., Britton K.T., and Bloom F.E. Picrotoxinin receptor ligand blocks anti-punishment effects of alcohol. Alcohol 5 (1988) 437-443
30. Laurie D.J., Wisden W., and Seeburg P. The distribution of 13 GABA-A receptor subunit mRNAs in the rat brain. III Embryonic and postnatal development. J. Neurosci. 12 (1992) 4151-4172
31. Liang J., Cagetti E., Olsen R.W., and Spigelman I. Altered pharmacology of synaptic and extrasynaptic GABAA receptors on CA1 hippocampal neurons is consistent with subunit changes in a model of alcohol withdrawal and dependence. J. Pharmacol. Exp. Ther. 310 (2004) 1234-1245
32. Luddens H., and Korpi E.R. Biological functions of GABA-A/benzodiazepine receptor heterogeneity. J. Psychiatr. Res. 29 (1995) 77-94
33. A receptor α4 subunit expression-possible relevance to alcohol dependence. J. Neurochem. 68 (1997) 2485-2492
34. Mihalek R.M., Bowers B.J., Wehner J.M., Kralic J.E., VanDoren M.J., Morrow A.L., and Homanics G.E. GABA (A)-receptor delta subunit knockout mice have multiple defects in behavioral responses to ethanol. Alcohol. Clin. Exp. Res. 25 (2001) 1708-1718
35. Mihic S.J., and Harris R.A. Inhibition of rho-I receptor GABAergic currents by alcohols and volatile anesthetics. J. Pharmacol. Exp. Ther. 277 (1996) 411-416
36. Mihic S.J., Ye Q., Wick M.J., Koltchine V.V., Krasowski M.D., Finn S.E., Mascia M.O., Valenzuela C.F., Hanson K.K., Greenblatt E.P., et al. Sites of alcohol and volatile anaesthetic action on GABA (A) and glycine receptors. Nature 389 (1997) 385-389
37. Morrow A.L., Suzdak P., and Paul S.M. Benzodiazepine, barbiturate, ethanol and hypnotic steroid hormone modulation of GABA-mediated chloride ion transport in rat brain synaptoneurosomes. Adv. Biochem. Psychopharmacol. 45 (1988) 247-261
38. Moykkynen T., Korpi E.R., and Lovinger D.M. Ethanol inhibits alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor function in central neurons by stabilizing desensitization. J. Pharmacol. Exp. Ther. 306 (2003) 546-555
39. Nguyen S.A., Deleon C.P., Malcom R.J., and Middaugh L.D. Tiagabine reduces ethanol reward in C57BL/6 mice under acute and chronic administration regimens. Synapse 56 (2005) 135-146
40. Nyberg S., Wahlstrom G., Backstrom T., and Sundstrom-Poromaa I. Altered sensitivity to alcohol in the late luteal phase among patients with premenstrual dysphoric disorder. Psychoneuroendocrinology 29 (2004) 767-777
41. Nyberg S., Wahlstrom G., Backstrom T., and Sundstrom-Poromaa I. No difference in responsiveness to a low dose of alcohol between healthy women and men. Pharmacol. Biochem. Behav. 78 (2004) 603-610
42. Overstreet L.S., Jones M.V., and Westbrook G.L. Slow desensitization regulates the availability of synaptic GABA (A) receptors. J. Neurosci. 20 (2000) 7914-7921
43. Ponomarev I., and Crabbe J.C. Characterization of acute functional tolerance to the hypnotic effects of ethanol in mice. Alcohol. Clin. Exp. Res. 28 (2004) 991-997
44. Quertemont E., Green H.L., and Grant K.A. Brain ethanol concentrations and ethanol discrimination in rats: effects of dose and time. Psychopharmacology (Berl.) 168 (2003) 262-270
45. Roberto M., Madamba S.G., Moore S.D., Tallent M.K., and Siggins G.R. Ethanol increases GABAergic transmission at both pre- and post-synaptic sites in rat central amygdala neurons. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 2053-2058
46. Saxena N.C., Neelands T.R., and Macdonald R.L. Contrasting actions of lanthanum on different recombinant gamma-aminobutyric acid receptor isoforms expressed in L929 fibroblasts. Mol. Pharmacol. 51 (1997) 328-335
47. Serra M., Mostallino M.C., Talani G., Pisu M.G., Carta M., Mura M.L., Floris I., Maciocco E., Sanna E., and Biggio G. Social isolation-induced increase in alpha and delta subunit gene expression is associated with a greater efficacy of ethanol on steroidogenesis and GABA receptor function. J. Neurochem. 98 (2006) 122-133
48. Shannon E.E., Shelton K.L., Vivian J.A., Yount I., Morgan A.R., Homanics G.E., and Grant K.A. Discriminative stimulus effects of ethanol in mice lacking the gamma-aminobutyric acid type A receptor delta subunit. Alcohol. Clin. Exp. Res. 28 (2004) 906-913
49. Shen H., Gong Q.H., Yuan M., and Smith S.S. Short-term steroid treatment increases delta GABA-A receptor subunit expression in rat CA1 hippocampus: pharmacological and behavioral effects. Neuropharmacology 49 (2005) 573-586
50. Smith S.S., and Gong Q.H. Ethanol administration rapidly reverses alpha-4 GABA-A receptor subunit upregulation following steroid exposure. Neuropharmacology 47 (2004) 9-16
51. A receptor α4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature 392 (1998) 926-929
52. Smith S.S., Ruderman Y., Gong Q.H., and Gulinello M. Effects of a low dose of ethanol in an animal model of premenstrual anxiety. Alcohol 33 (2004) 41-49
53. Song M., and Messing R.O. Protein kinase C regulation of GABAA receptors. Cell. Mol. Life. Sci. 62 (2005) 119-127
54. Stell B.M., Brickley S.G., Tang C.Y., Farrant M., and Mody I. Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABA-A receptors. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 14439-14444
55. Stell B.M., and Mody I. Receptors with different affinities mediate phasic and tonic GABA (A) conductances in hippocampal neurons. J. Neurosci. 22 (2002) RC223
56. Sundstrom I., Andersson A., Nyberg S., Ashbrook D., Purdy R.H., and Backstrom T. Patients with premenstrual syndrome have a different sensitivity to a neuroactive steroid during the menstrual cycle compared to control subjects. Neuroendocrinology 67 (1998) 126-138
57. A receptors are a target for alcohol. Nat. Neurosci. 5 (2002) 721-722
58. Suzdak P.D., Glowa J., Crawley J.N., Schwartz R.D., Skolnick P., and Paul S.M. A selective imidazobenzodiazepine antagonist of ethanol in the rat. Science 234 (1986) 1243-1247
59. Suzdak P., and Paul S.M. Ethanol stimulates GABAn receptor-mediated Cl- ion flux in vitro: possible relationship to the anxiolytic and intoxicating actions of alcohol. Psychopharmacol. Bull. 23 (1987) 445-451
60. Suzdak P., Schwartz R.D., Skolnick P., and Paul S.M. Ethanol stimulates gamma-aminobutyric acid receptor-mediated chloride transport in rat brain synaptoneurosomes. Proc. Natl. Acad. Sci. U. S. A. 83 (1986) 4071-4075
61. Tampier L., and Quintanilla M.E. Effect of a dose of ethanol on acute tolerance and ethanol consumption in alcohol drinker (EChB) and non-drinker (UChA) rats. Addict. Biol. 7 (2002) 279-284
62. Ticku M.K., Lowrimore P., and Lehoullier P. Ethanol enhances GABA-induced 36 CI-influx in primary spinal cord cultured neurons. Brain Res. Bull 17 (1986) 123-136
63. Ueno S., Harris R.A., Messing R.O., Sanchez-Perez A.M., Hodge C.W., McMahon T., Wang D., Mehmert K.K., Kelley S.P., Haywood A., et al. Alcohol actions on GABA (A) receptors: from protein structure to mouse behavior. Alcohol. Clin. Exp. Res. 25 (2001) 76S-81S
64. Wallner M., Hanchar H.J., and Olsen R.W. Ethanol enhances alpha 4 beta 3 delta and alpha 6 beta 3 delta gamma-aminobutyric acid type A receptors at low concentrations known to affect humans. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15218-15223
65. Wallner M., Hanchar H.J., and Olsen R.W. Low dose ethanol actions on alpha4-beta3-delta GABA-A receptors are reversed by the behavioral alcohol antagonist Ro15-4513. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 8540-8545
66. Wan F.J., Berton F., Madamba S.G., Francesconi W., and Siggins G.R. Low ethanol concentrations enhance GABAergic inhibitory postsynaptic potentials in hippocampal pyramidal neurons only after block of GABA-B receptors. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 5049-5054
67. Wei W., Faria L.C., and Mody I. Low ethanol concentrations selectively augment the tonic inhibition mediated by delta subunit-containing GABA-A receptors in hippocampal neurons. J. Neurosci. 24 (2004) 8379-8382
68. Wei W., Zhang N., Peng Z., Houser C.R., and Mody I. Perisynaptic localization of delta subunit-containing GABA (A) receptors and their activation by GABA spillover in the mouse dentate gyrus. J. Neurosci. 23 (2003) 10650-10661
69. Wisden W., Laurie D.J., Monyer H., and Seeburg P. The distribution of 13 GABA-A receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J. Neurosci. 12 (1992) 1040-1062
70. Yamashita M., Marszalec W., Yeh J.Z., and Narahashi T. Effects of ethanol on tonic GABA current in cerebellar granule cells and mammalian cells recombinantly expressing GABA-A receptors. J. Pharmacol. Exp. Ther. 319 (2007) 431-438
71. Zhu W.J., Wang J.F., Corsi L., and Vicini S. Lanthanum-mediated modification of GABA-A receptor deactivation, desensitization, and inhibitory synaptic currents in rat cerebellar neurons. J. Physiol. 511 (1998) 647-661