GABAA receptor subtypes: the ‘one glass of wine’ receptors

Olsen, Richard W.; Hanchar, Harry J.; Meera, Pratap; Wallner, Martin

doi:10.1016/j.alcohol.2007.04.006

Cited by 144Neuroscience and Neuropharmacology ResearchNicotinic Acetylcholine Receptors StudyReceptor Mechanisms and Signaling

GABAA receptor subtypes: the ‘one glass of wine’ receptors

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Olsen, Richard W., Hanchar, Harry J., Meera, Pratap, Wallner, Martin·2007·Alcohol

DOI 10.1016/j.alcohol.2007.04.006PMC PMC2852584

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Abstract

This review discusses evidence for and apparent controversy about, gamma-aminobutyric acid type A (GABAA) receptor (GABAAR) subtypes that mediate alcohol effects experienced during social drinking. GABAARs that contain the beta3 and delta subunits were shown to be enhanced by alcohol concentrations that mirror the concentration dependence of alcohol responses in humans. A mutation (alpha6R100Q) previously found in alcohol nontolerant rats in the cerebellar GABAAR alpha6 subunit is sufficient for increased alcohol-induced ataxia in rats homozygous for this mutation (alpha6-100QQ) and further increases alcohol sensitivity of tonic GABA currents (mediated by alpha6betadelta receptors) in cerebellar granule cells of alpha6-100QQ rats and in recombinant alpha6R100Qbeta3delta receptors. This provided the first direct evidence that these types of receptors mediate behavioral effects of ethanol. Furthermore, the behavioral alcohol antagonist Ro15-4513 specifically reverses ethanol enhancement on alpha4/6beta3delta receptors. Unexpectedly, native and recombinant alpha4/6beta3delta receptors bind the behavioral alcohol antagonist Ro15-4513 with high affinity and this binding is competitive with EtOH, suggesting a specific and mutually exclusive (competitive) ethanol/Ro15-4513 site, which explains the puzzling activity of Ro15-4513 as a behavioral alcohol antagonist. Our conclusion from these findings is that alcohol/Ro15-4513-sensitive GABAAR subtypes are important alcohol targets and that alcohol at relevant concentrations is more specific than previously thought. In this review, we discuss technical difficulties in expressing recombinant delta subunit-containing receptors in oocytes and mammalian cells that may have contributed to negative results and confusion. Not only because we have reproduced detailed positive results numerous times, and we and many others have built extensively on basic findings, but also because we explain and combine many previously puzzling results into a coherent and highly plausible paradigm on how alcohol exerts an important part of its action in the brain, we are confident about our findings and conclusions. However, many important open questions remain to be answered.

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Ethanol at high doses potentiates GABA-gated current in a mostly nonselective manner across GABAAR subunits.
“Another GABAAR-modulating drug of abuse, ethanol, at high doses potentiates GABA-gated current in a mostly nonselective manner in terms of the GABAAR subunits, with the exception of the α4/6β3δ GABAARs, which seem to be sensitive to low concentrations of ethanol as observed with social drinking [110].”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [110]
α4/6β3δ GABAARs are sensitive to low concentrations of ethanol as observed with social drinking.
“Another GABAAR-modulating drug of abuse, ethanol, at high doses potentiates GABA-gated current in a mostly nonselective manner in terms of the GABAAR subunits, with the exception of the α4/6β3δ GABAARs, which seem to be sensitive to low concentrations of ethanol as observed with social drinking [110].”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [110]
Ethanol modulation of high-sensitivity α4/6β3δ GABAARs may play an important role in the maintenance of ethanol self-administration.
“The ethanol modulation of these high-sensitivity receptors may play an important role in the maintenance of ethanol self-administration, as knockdown of α4GABAARs in the NAc shell (but not core) was sufficient to completely abolish self-administration of ethanol in rats [111, 112].”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [110]

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International Union of Pharmacology. LXX. Subtypes of γ-Aminobutyric AcidA Receptors: Classification on the Basis of Subunit Composition, Pharmacology, and Function. Update
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GABAA receptors as molecular targets of general anesthetics: identification of binding sites provides clues to allosteric modulation
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Differential assembly diversifies GABAA receptor structures and signalling
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Extrasynaptic δ-containing GABA A receptors in the nucleus accumbens dorsomedial shell contribute to alcohol intake
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A study of subunit selectivity, mechanism and site of action of the delta selective compound 2 ( DS2 ) at human recombinant and rodent native GABAA receptors
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Physiology and pharmacology of alcohol: the imidazobenzodiazepine alcohol antagonist site on subtypes of GABAAreceptors as an opportunity for drug development?
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GABAA receptor subtypes and benzodiazepine use, misuse, and abuse
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Oxytocin prevents ethanol actions at δ subunit-containing GABA A receptors and attenuates ethanol-induced motor impairment in rats
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Neurosteroids and GABAergic signaling in health and disease
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The Glycine Receptor—A Functionally Important Primary Brain Target of Ethanol
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The Yin and Yang of GABAergic and Glutamatergic Synaptic Plasticity: Opposites in Balance by Crosstalking Mechanisms
Chapman, C. A., Nuwer, J. L., & Jacob, T. C. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.911020 · Cited by 62 · see citing works
Isoflurane Is a Potent Modulator of Extrasynaptic GABAA Receptors in the Thalamus
Jia, F., Yue, M. E., Chandra, D., Homanics, G. E., Goldstein, P. A., & Harrison, N. L. (2007) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.134569 · Cited by 61 · see citing works
Neurosteroid regulation of GABAA receptors: A role in catamenial epilepsy
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From Pleasure to Pain, and Back Again: The Intricate Relationship Between Alcohol and Nociception
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Ethanol induces stronger dopamine release in nucleus accumbens (shell) of alcohol-preferring (bibulous) than in alcohol-avoiding (abstainer) rats
Bustamante, D., Quintanilla, M. E., Tampier, L., González-Lira, V., Israel, Y., & Herrera‐Marschitz, M. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.06.069 · Cited by 55 · see citing works
Etomidate, propofol and the neurosteroid THDOC increase the GABA efficacy of recombinant α4β3δ and α4β3 GABAA receptors expressed in HEK cells
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GABRA2 markers moderate the subjective effects of alcohol
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Slow intracellular accumulation of GABAA receptor δ subunit is modulated by brain-derived neurotrophic factor
Joshi, S., & Kapur, J. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.08.008 · Cited by 48 · see citing works
Differential Effects of the Dual Orexin Receptor Antagonist Almorexant and the GABAA-α1 Receptor Modulator Zolpidem, Alone or Combined with Ethanol, on Motor Performance in the Rat
Steiner, M. A., Lecourt, H., Strasser, D. S., Roch, C., & Jenck, F. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.224 · Cited by 48 · see citing works
GABAA receptor-mediated neurotransmission: Not so simple after all
Knoflach, F., Hernandez, M., & Bertrand, D. (2016) · Biochemical Pharmacology · doi:10.1016/j.bcp.2016.03.014 · Cited by 48 · see citing works
Alteration of Ethanol Drinking in Mice via Modulation of the GABAA Receptor with Ganaxolone, Finasteride, and Gaboxadol
Ramaker, M. J., Ford, M. M., Fretwell, A. M., & Finn, D. A. (2011) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2011.01551.x · Cited by 43 · see citing works
Ethanol modulates mammalian circadian clock phase resetting through extrasynaptic gaba receptor activation
McElroy, B., Zakaria, A., Glass, J. D., & Prosser, R. A. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.08.020 · Cited by 42 · see citing works
Sex differences in acoustic startle responses and seizure thresholds between ethanol-withdrawn male and female rats
Reilly, W., Koirala, B., & Devaud, L. L. (2009) · Alcohol and Alcoholism · doi:10.1093/alcalc/agp049 · Cited by 40 · see citing works
Plasticity of GABAA Receptors after Ethanol Pre-Exposure in Cultured Hippocampal Neurons
Shen, Y., Lindemeyer, A. K., Spigelman, I., Sieghart, W., Olsen, R. W., & Liang, J. (2010) · Molecular Pharmacology · doi:10.1124/mol.110.068650 · Cited by 40 · see citing works
The α5-Containing GABAA Receptors—a Brief Summary
Mohamad, F. H., & Has, A. T. C. (2019) · Journal of Molecular Neuroscience · doi:10.1007/s12031-018-1246-4 · Cited by 38 · see citing works
Deleterious Effects of a Low Amount of Ethanol on LTP-Like Plasticity in Human Cortex
Lücke, C., Heidegger, T., Röhner, M., Toennes, S. W., Kriváneková, L., Müller‐Dahlhaus, F., & Ziemann, U. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.350 · Cited by 36 · see citing works
Loop 2 Structure in Glycine and GABAA Receptors Plays a Key Role in Determining Ethanol Sensitivity
Perkins, D. I., Trudell, J. R., Crawford, D. K., Asatryan, L., Alkana, R. L., & Davies, D. L. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.023598 · Cited by 35 · see citing works
Dihydromyricetin Prevents Fetal Alcohol Exposure-Induced Behavioral and Physiological Deficits: The Roles of GABAA Receptors in Adolescence
Liang, J., Shen, Y., Shao, X. M., Scott, M., Ly, E., Wong, S. C., Nguyen, A. T., Tan, K., Kwon, O. J., Olsen, R. W., et al. (2014) · Neurochemical Research · doi:10.1007/s11064-014-1291-5 · Cited by 35 · see citing works
Alpha4 subunit‐containing GABA<sub>A</sub>receptors in the accumbens shell contribute to the reinforcing effects of alcohol
Rewal, M., Donahue, R., Gill, T. M., Nie, H., Ron, D., & Janak, P. H. (2012) · Addiction Biology · doi:10.1111/j.1369-1600.2011.00333.x · Cited by 34 · see citing works
Ethanol Sensitivity of GABAergic Currents in Cerebellar Granule Neurons Is Not Increased by a Single Amino Acid Change (R100Q) in the α6 GABAA Receptor Subunit
Botta, P., Mameli, M., Floyd, K. L., Radcliffe, R. A., & Valenzuela, C. F. (2007) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.127894 · Cited by 33 · see citing works
GABAA receptors in the posterior, but not anterior, ventral tegmental area mediate Ro15-4513-induced attenuation of binge-like ethanol consumption in C57BL/6J female mice
Melón, L. C., & Boehm, S. L. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.02.014 · Cited by 32 · see citing works
Selective Changes of GABAA Channel Subunit mRNAs in the Hippocampus and Orbitofrontal Cortex but not in Prefrontal Cortex of Human Alcoholics
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Low-dose alcohol actions on α4β3δ GABA A receptors are reversed by the behavioral alcohol antagonist Ro15-4513
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Authors: Olsen, R. W., Hanchar, H. J., Meera, P., & Wallner, M.
Affiliations: University of California, Los Angeles (US)
Corresponding author: Wallner, Martin
ORCID: Meera, Pratap
Wallner, Martin
Venue: Alcohol
Publisher: Elsevier BV
Published: 2007-05
Volume: 41
Issue: 3
Pages: 201-209
ISSN: 0741-8329 (ISSN-L)
DOI: 10.1016/j.alcohol.2007.04.006
PMC: PMC2852584
OpenAlex: W1978493649
Cited by: 142
References: 125
Citations by year: 2024: 4 · 2023: 6 · 2022: 5 · 2021: 5 · 2020: 2 · 2019: 9 · 2018: 11 · 2017: 7 · 2016: 8 · 2015: 7 · 2014: 16 · 2013: 6 · 2012: 15
FWCI: 0.96
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Alcohol (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Alcohol Abuse and Alcoholism (F31AA015460, AA 015460, AA07680, R37AA007680, R01AA007680)
National Institute of Neurological Disorders and Stroke (NS-35985, P01NS035985)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
Keywords: GABAA receptor subtypes, alcohol effects, social drinking, alpha6 subunit, cerebellar granule cells, Ro 15-4513, alcohol sensitivity
MeSH terms: Ethanol, Animals, Azides, Benzodiazepines, Central Nervous System Depressants, Humans, Receptors, GABA-A, Wine

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GABAA receptor subtypes: the ‘one glass of wine’ receptors

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