Opposite actions of alcohol on tonic GABA A receptor currents mediated by nNOS and PKC activity

Nature Neuroscience

Volumn 16, Issue 12, 2013, Pages 1783-1793

  Kaplan, Joshua S ^a   Mohr, Claudia ^a   Rossi, David J ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ALCOHOL; FUROSEMIDE; N(G) METHYLARGININE; N(G) NITROARGININE; NEURONAL NITRIC OXIDE SYNTHASE; NICOTINE; PROTEIN KINASE C; TETRODOTOXIN;

4 AMINOBUTYRIC ACID RELEASE; ACTION POTENTIAL; ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; CEREBELLUM CORTEX; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE DELETION; GENETIC VARIABILITY; GENOTYPE; GOLGI COMPLEX; GRANULE CELL; MALE; MEMBRANE CURRENT; MOUSE; NONHUMAN; PHENOTYPE; POSTSYNAPTIC INHIBITION; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTUM YIELD; RAT; VOLTAGE CLAMP;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CEREBELLUM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; ETHANOL; FEMALE; GABA AGENTS; GABA ANTAGONISTS; GENE EXPRESSION REGULATION; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; PROTEIN KINASE C; RATS; RECEPTORS, GABA-A;

EID: 84888371946     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3559     Document Type: Article

References (51)

1. Harwood, H. Updating estimates of the economic costs of alcohol abuse in the United States: Estimates, update methods and data. National Institute on Alcohol Abuse and Alcoholism, http://pubs.niaaa.nih.gov/publications/economic- 2000/ (2000
2. Hill, S.Y. Neural plasticity, human genetics, and risk for alcohol dependence. Int. Rev. Neurobiol. 91, 53-94 (2010
3. Prescott, C.A. & Kendler, K.S. Genetic and environmental contributions to alcohol abuse and dependence in a population-based sample of male twins. Am. J. Psychiatry 156, 34-40 (1999
4. Herting, M.M., Fair, D. & Nagel, B.J. Altered fronto-cerebellar connectivity in alcohol-naive youth with a family history of alcoholism. Neuroimage 54, 2582-2589 (2011
5. Schuckit, M.A., Tsuang, J.W., Anthenelli, R.M., Tipp, J.E. & Nurnberger, J.I. Jr. Alcohol challenges in young men from alcoholic pedigrees and control families: A report from the COGA project. J. Stud. Alcohol 57, 368-377 (1996
6. Schuckit, M.A., Smith, T.L., Kalmijn, J. & Danko, G.P. A cross-generational comparison of alcohol challenges at about age 20 in 40 father-offspring pairs. Alcohol. Clin. Exp. Res. 29, 1921-1927 (2005
7. Yoneyama, N., Crabbe, J.C., Ford, M.M., Murillo, A. & Finn, D.A. Voluntary ethanol consumption in 22 inbred mouse strains. Alcohol 42, 149-160 (2008
8. Gallaher, E.J., Jones, G.E., Belknap, J.K. & Crabbe, J.C. Identification of genetic markers for initial sensitivity and rapid tolerance to ethanol-induced ataxia using quantitative trait locus analysis in BXD recombinant inbred mice. J. Pharmacol. Exp. Ther. 277, 604-612 (1996
9. Bell, R.L., et al. Responsivity and development of tolerance to the motor impairing effects of moderate doses of ethanol in alcohol-preferring (P) and-nonpreferring (NP) rat lines. Alcohol. Clin. Exp. Res. 25, 644-650 (2001
10. Malila, A. Intoxicating effects of three aliphatic alcohols and barbital on two rat strains genetically selected for their ethanol intake. Pharmacol. Biochem. Behav. 8, 197-201 (1978
11. McClearn, G.E., Deitrich, R.A. & Erwin, V.G. Development of Animal Models as Pharmacogentic Tools, Research Monograph No. 6 (National Institute of Alcohol Abuse and Alcoholism, Washington DC, 1981
12. Al-Rejaie, S. & Dar, M.S. Antagonism of ethanol ataxia by intracerebellar nicotine: Possible modulation by mouse cerebellar nitric oxide and cGMP. Brain Res. Bull. 69, 187-196 (2006
13. Duguid, I., Branco, T., London, M., Chadderton, P. & Hausser, M. Tonic inhibition enhances fidelity of sensory information transmission in the cerebellar cortex. J. Neurosci. 32, 11132-11143 (2012
14. Hamann, M., Rossi, D.J. & Attwell, D. Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33, 625-633 (2002
15. Brickley, S.G., Revilla, V., Cull-Candy, S.G., Wisden, W. & Farrant, M. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409, 88-92 (2001
16. Meera, P., Wallner, M. & Otis, T.S. Molecular basis for the high THIP/gaboxadol sensitivity of extrasynaptic GABAA receptors. J. Neurophysiol. 106, 2057-2064 (2011
17. Rossi, D.J., Hamann, M. & Attwell, D. Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J. Physiol. (Lond.) 548, 97-110 (2003
18. Stell, B.M., Brickley, S.G., Tang, C.Y., Farrant, M. & Mody, I. Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors. Proc. Natl. Acad. Sci. USA 100, 14439-14444 (2003
19. Carta, M., Mameli, M. & Valenzuela, C.F. Alcohol enhances GABAergic transmission to cerebellar granule cells via an increase in Golgi cell excitability. J. Neurosci. 24, 3746-3751 (2004
20. Hanchar, H.J., Dodson, P.D., Olsen, R.W., Otis, T.S. & Wallner, M. Alcohol-induced motor impairment caused by increased extrasynaptic GABA(A) receptor activity. Nat. Neurosci. 8, 339-345 (2005
21. Botta, P. et al. Modulation of GABAA receptors in cerebellar granule neurons by ethanol: A review of genetic and electrophysiological studies. Alcohol 41, 187-199 (2007
22. Melchior, C.L. & Myers, R.D. Genetic differences in ethanol drinking of the rat following injection of 6-OHDA, 5,6-DHT or 5,7-DHT into the cerebral ventricles. Pharmacol. Biochem. Behav. 5, 63-72 (1976
23. Korpi, E.R., Kuner, T., Seeburg, P.H. & Luddens, H. Selective antagonist for the cerebellar granule cell-specific gamma-Aminobutyric acid type A receptor. Mol. Pharmacol. 47, 283-289 (1995
24. Saxena, N.C. & Macdonald, R.L. Properties of putative cerebellar gamma-Aminobutyric acid A receptor isoforms. Mol. Pharmacol. 49, 567-579 (1996
25. De Schutter, E. & Bower, J.M. An active membrane model of the cerebellar Purkinje cell II. Simulation of synaptic responses. J. Neurophysiol. 71, 401-419 (1994
26. Ford, M.M. et al. The influence of selection for ethanol withdrawal severity on traits associated with ethanol self-Administration and reinforcement. Alcohol. Clin. Exp. Res. 35, 326-337 (2011
27. Porcu, P. et al. Differential effects of ethanol on serum GABAergic 3alpha,5alpha/3alpha,5beta neuroactive steroids in mice, rats, cynomolgus monkeys, and humans. Alcohol. Clin. Exp. Res. 34, 432-442 (2010
28. Botta, P., Simoes de Souza, F.M., Sangrey, T., De Schutter, E. & Valenzuela, C.F. Excitation of rat cerebellar Golgi cells by ethanol: Further characterization of the mechanism. Alcohol. Clin. Exp. Res. 36, 616-624 (2012
29. Fataccioli, V., Gentil, M., Nordmann, R. & Rouach, H. Inactivation of cerebellar nitric oxide synthase by ethanol in vitro. Alcohol Alcohol. 32, 683-691 (1997
30. Wall, M.J. Endogenous nitric oxide modulates GABAergic transmission to granule cells in adult rat cerebellum. Eur. J. Neurosci. 18, 869-878 (2003
31. Harris, R.A. et al. Mutant mice lacking the gamma isoform of protein kinase C show decreased behavioral actions of ethanol and altered function of gamma-Aminobutyrate type A receptors. Proc. Natl. Acad. Sci. USA 92, 3658-3662 (1995
32. Naik, M.U. et al. Distribution of protein kinase Mzeta and the complete protein kinase C isoform family in rat brain. J. Comp. Neurol. 426, 243-258 (2000
33. Fidler, T.L. et al. Intragastric self-infusion of ethanol in high-And low-drinking mouse genotypes after passive ethanol exposure. Genes Brain Behav. 10, 264-275 (2011
34. McCool, B.A. & Chappell, A.M. Using monosodium glutamate to initiate ethanol self-Administration in inbred mouse strains. Addict. Biol. 17, 121-131 (2012
35. Jia, F., Chandra, D., Homanics, G.E. & Harrison, N.L. Ethanol modulates synaptic and extrasynaptic GABAA receptors in the thalamus. J. Pharmacol. Exp. Ther. 326, 475-482 (2008
36. Liang, J. et al. Chronic intermittent ethanol-induced switch of ethanol actions from extrasynaptic to synaptic hippocampal GABAA receptors. J. Neurosci. 26, 1749-1758 (2006
37. Nie, Z., Madamba, S.G. & Siggins, G.R. Ethanol enhances gamma-Aminobutyric acid responses in a subpopulation of nucleus accumbens neurons: Role of metabotropic glutamate receptors. J. Pharmacol. Exp. Ther. 293, 654-661 (2000
38. Peris, J., Coleman-Hardee, M., Burry, J. & Pecins-Thompson, M. Selective changes in GABAergic transmission in substantia nigra and superior colliculus caused by ethanol and ethanol withdrawal. Alcohol. Clin. Exp. Res. 16, 311-319 (1992
39. Theile, J.W., Morikawa, H., Gonzales, R.A. & Morrisett, R.A. Role of 5-hydroxytryptamine2C receptors in Ca2+-dependent ethanol potentiation of GABA release onto ventral tegmental area dopamine neurons. J. Pharmacol. Exp. Ther. 329, 625-633 (2009
40. Criswell, H.E., Ming, Z., Kelm, M.K. & Breese, G.R. Brain regional differences in the effect of ethanol on GABA release from presynaptic terminals. J. Pharmacol. Exp. Ther. 326, 596-603 (2008
41. Kumar, S. et al. The role of GABA(A) receptors in the acute and chronic effects of ethanol: A decade of progress. Psychopharmacology (Berl.) 205, 529-564 (2009
42. Korpi, E.R. et al. Cerebellar granule cell-specific GABAA receptors attenuate benzodiazepine-induced ataxia: Evidence from alpha 6-subunit-deficient mice. Eur. J. Neurosci. 11, 233-240 (1999
43. Mihalek, R.M. et al. GABA(A)-receptor delta subunit knockout mice have multiple defects in behavioral responses to ethanol. Alcohol. Clin. Exp. Res. 25, 1708-1718 (2001
44. White, C.N. et al. Opposing effects of coupled and uncoupled NOS activity on the Na+-K+ pump in cardiac myocytes. Am. J. Physiol. Cell Physiol. 294, C572-C578 (2008
45. Salapatek, A.M., Wang, Y.F., Mao, Y.K., Mori, M. & Daniel, E.E. Myogenic NOS in canine lower esophageal sphincter: Enzyme activation, substrate recycling, and product actions. Am. J. Physiol. 274, C1145-C1157 (1998
46. Wang, W., Hebert, S.C. & Giebisch, G. Renal K+ channels: Structure and function. Annu. Rev. Physiol. 59, 413-436 (1997
47. Johnson, W.D., Howard, R.J., Trudell, J.R. & Harris, R.A. The TM2 6' position of GABA(A) receptors mediates alcohol inhibition. J. Pharmacol. Exp. Ther. 340, 445-456 (2012
48. Mihic, S.J. et al. Sites of alcohol and volatile anaesthetic action on GABA(A) and glycine receptors. Nature 389, 385-389 (1997
49. Ueno, S. et al. Tryptophan scanning mutagenesis in TM2 of the GABA(A) receptor alpha subunit: Effects on channel gating and regulation by ethanol. Br. J. Pharmacol. 131, 296-302 (2000
50. Yamashita, M., Marszalec, W., Yeh, J.Z. & Narahashi, T. Effects of ethanol on tonic GABA currents in cerebellar granule cells and mammalian cells recombinantly expressing GABA(A) receptors. J. Pharmacol. Exp. Ther. 319, 431-438 (2006
51. Kojima, H. et al. Detection and imaging of nitric oxide with novel fluorescent indicators: Diaminofluoresceins. Anal. Chem. 70, 2446-2453 (1998