Ethanol activation of protein kinase A regulates GABA A receptor subunit expression in the cerebral cortex and contributes to ethanol-induced hypnosis

Frontiers in Neuroscience

Volumn , Issue APR, 2012, Pages

  Kumar, Sandeep ^a   Ren, Qinglu ^a   Beckley, Jonathon H ^a   O'Buckley, Todd K ^a   Gigante, Eduardo D ^b   Santerre, Jessica L ^b   Werner, David F ^a,b   Morrow, A Leslie ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b BINGHAMTON UNIVERSITY   (United States)

Author keywords

Ethanol; GABA A receptors; Loss of righting reflex; PKA; PKC

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; ALCOHOL; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IIALPHA; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IIBETA; ISOENZYME; MUSCIMOL; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PROTEIN KINASE C; PROTEIN KINASE C BETA; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; PROTEIN KINASE C GAMMA; SODIUM CHLORIDE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN SYNAPTOSOME; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HYPNOSIS; MALE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RIGHTING REFLEX; WESTERN BLOTTING;

EID: 84862218306     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2012.00044     Document Type: Article

References (53)

1. Angelotti, T. P., Uhler, M. D., and Macdonald, R. L. (1993). Enhancement of recombinant gamma-aminobutyric acid type A receptor currents by chronic activation of cAMP-dependent protein kinase. Mol. Pharmacol. 44, 1202-1210.
2. Bogdanov, Y., Michels, G., Armstrong-Gold, C., Haydon, P. G., Lindstrom, J., Pangalos, M., and Moss, S. J. (2006). Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBOJ. 25,4381-4389.
3. Brandon, N. J., Delmas, P., Kittler, J. T., McDonald, B. J., Sieghart, W., Brown, D. A., Smart, T. G., and Moss, S. J. (2000). GABAA receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J. Biol. Chem. 275, 38856-38862.
4. Brandon, N. J., Jovanovic, J. N., Colledge, M., Kittler, J. T., Brandon, J. M., Scott, J. D., and Moss, S. J. (2003). A-kinase anchoring protein 79/150 facilitates the phosphorylation of GABA(A) receptors by cAMP-dependent protein kinase via selective interaction with receptor betasubunits. Mol. Cell. Neurosci. 22, 87-97.
5. Cagetti, E., Liang, J., Spigelman, I., and Olsen, R. W. (2003). Withdrawal from chronic intermittent ethanol treatment changes subunit composition, reduces synaptic function, and decreases behavioral responses to positive allosteric modulators of GABAA receptors. Mol. Pharmacol. 63, 53-64.
6. Criswell, H. E., Ming, Z., Kelm, M. K., and Breese, G. R. (2008). Brain regional differences in the effect of ethanol on GABA release from presynaptic terminals. J. Pharmacol. Exp. Ther. 326, 596-603.
7. Devaud, L. L., Fritschy, J. M., Sieghart, W., and Morrow, A. L. (1997). Bidirectional alterations of GABA(A) receptor subunit peptide levels in rat cortex during chronic ethanol consumption and withdrawal. J. Neu-rochem. 69, 126-130.
8. Diamond, I., and Gordon, A. S. (1997). Cellular and molecular neuroscience of alcoholism. Physiol. Rev. 77,1-20.
9. Dohrman, D. P., Chen, H. M., Gordon, A. S., and Diamond, I. (2002). Ethanol-induced translocation of protein kinase A occurs in two phases: control by different molecular mechanisms. Alcohol. Clin. Exp. Res. 26, 407-415.
10. Dohrman, D. P., Diamond, I., and Gordon, A. S. (1996). Ethanol causes translocation of cAMP-dependent protein kinase catalytic subunit to the nucleus. Proc. Natl. Acad. Sci. U.S.A. 93, 10217-10221.
11. El Yacoubi, M., Ledent, C., Par-mentier, M., Daoust, M., Cos-tentin, J., and Vaugeois, J. (2001). Absence of the adenosine A(2A) receptor or its chronic blockade decrease ethanol withdrawal-induced seizures in mice. Neu-ropharmacology 40, 424-432.
12. Ferrani-Kile, K., Randall, P. K., and Leslie, S. W. (2003). Acute ethanol affects phosphorylation state of the NMDA receptor complex: implication of tyrosine phosphatases and protein kinase A. Brain Res. Mol. Brain Res. 115,78-86.
13. Freund, R. K., and Palmer, M. R. (1997). Beta adrenergic sensitiza-tion of gamma-aminobutyric acid receptors to ethanol involves a cyclic AMP/protein kinase A second-messenger mechanism. J. Pharmacol. Exp. Ther. 280, 1192-1200.
14. Fritschy, J. M., and Mohler, H. (1995). GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J. Comp. Neu-rol. 359, 154-194.
15. Glantz, S. B., Amat, J. A., and Rubin, C. S. (1992). cAMP signaling in neurons: patterns of neuronal expression and intracellular localization for a novel protein, AKAP 150, that anchors the regulatory sub-unit of cAMP-dependent protein kinase II beta. Mol. Biol. Cell 3, 1215-1228.
16. Grey, C. L., and Chang, J. P. (2011). Differential Involvement of PKC and PKA in ghrelin-induced growth hormone and gonadotrophin release from goldfish (Carassius auratus) pituitary cells. J. Neuroendocrinol. 12,1273-1287.
17. Ives, J. H., Drewery, D. L., and Thompson, C. L. (2002). Differential cell surface expression of GABAA receptor alpha1, alpha6, beta2 and beta3 subunits in cultured mouse cerebel-lar granule cells influence of cAMP-activated signalling. J. Neurochem. 80,317-327.
18. Kano, M., and Konnerth, A. (1992). Potentiation of GABA-mediated currents by cAMP-dependent protein kinase. Neuroreport 3, 563-566.
19. Kapur, J., and Macdonald, R. L. (1996). Cyclic AMP-dependent protein kinase enhances hippocampal dentate granule cell GABAA receptor currents. J. Neurophysiol. 76, 2626-2634.
20. Kelm, M. K., Criswell, H. E., and Breese, G. R. (2008). The role of protein kinase A in the ethanol-induced increase in spontaneous GABA release onto cerebellar Purk-inje neurons. J. Neurophysiol. 100, 3417-3428.
21. Kim, K. S., Kim, H., Baek, I. S., Lee, K. W., and Han, P. L. (2010). Mice lacking adenylyl cyclase type 5 (AC5) show increased ethanol consumption and reduced ethanol sensitivity. Psychopharmacology (Berl.) 215, 391-398.
22. Kralic, J. E., O'Buckley, T. K., Khisti, R. T., Hodge, C. W., Homanics, G. E., and Morrow, A. L. (2002). GABA(A) receptor alpha-1 sub-unit deletion alters receptor subtype assembly, pharmacological and behavioral responses to benzodi-azepines and zolpidem. Neurophar-macology 43, 685-694.
23. Kumar, S., Lane, B. M., and Morrow, A. L. (2006). Differential effects of systemic ethanol administration on protein kinase Cepsilon, gamma, and beta isoform expression, membrane translocation, and target phosphorylation: reversal by chronic ethanol exposure. J. Pharmacol. Exp. Ther. 319, 1366-1375.
24. Kumar, S., Porcu, P., Werner, D. F., Matthews, D. B., Diaz-Granados, J. L., Helfand, R. S., and Morrow, A. L. (2009). The role of GABA(A) receptors in the acute and chronic effects of ethanol: a decade of progress. Psychopharmacology (Berl.) 205, 529-564.
25. Kumar, S., Suryanarayanan, A., Boyd, K. N., Comerford, C. E., Lai, M. A., Ren, Q., and Morrow, A. L. (2010). Ethanol reduces GABAA alpha1 sub-unit receptor surface expression by a protein kinase Cgamma-dependent mechanism in cultured cerebral cortical neurons. Mol. Pharmacol. 77, 793-803.
26. Lai, C. C., Kuo, T. I., and Lin, H. H. (2007). The role of protein kinase A in acute ethanol-induced neu-robehavioral actions in rats. Anesth. Analg. 105, 89-96.
27. Lau, G. C., Saha, S., Faris, R., and Russek, S. J. (2004). Up-regulation of NMDAR1 subunit gene expression in cortical neurons via a PKA-dependent pathway. J. Neurochem. 88, 564-575.
28. Leidenheimer, N. J., Machu, T. K., Endo, S., Olsen, R. W., Harris, R. A., and Browning, M. D. (1991). Cyclic AMP-dependent protein kinase decreases gamma-aminobutyric acidA receptor-mediated 36Cl-uptake by brain microsacs. J. Neurochem. 57, 722-725.
29. Liang, J., Suryanarayanan, A., Abriam, A., Snyder, B., Olsen, R. W., and Spigelman, I. (2007). Mechanisms of reversible GABAA receptor plasticity after ethanol intoxication. J. Neurosci. 27, 12367-12377.
30. Maas, J. W Jr., Vogt, S. K., Chan, G. C., Pineda, V. V., Storm, D. R., and Muglia, L. J. (2005). Calcium-stimulated adenylyl cyclases are critical modulators of neuronal ethanol sensitivity. J. Neurosci. 25, 4118-4126.
31. McKnight, G. S. (1991). Cyclic AMP second messenger systems. Curr. Opin. Cell Biol. 3,213-217.
32. Messing, R. O., Petersen, P. J., and Henrich, C. J. (1991). Chronic ethanol exposure increases levels of protein kinase C delta and epsilon and protein kinase C-mediated phosphorylation in cultured neural cells. J. Biol. Chem. 266, 23428-23432.
33. Moss, S. J., Doherty, C. A., and Huganir, R. L. (1992a). Identification of the cAMP-dependent protein kinase and protein kinase C phosphoryla-tion sites within the major intra-cellular domains of the beta 1, gamma 2S, and gamma 2L sub-units of the gamma-aminobutyric acid type A receptor. J. Biol. Chem. 267, 14470-14476.
34. Moss, S. J., Smart, T. G., Blackstone, C. D., and Huganir, R. L. (1992b). Functional modulation of GABAA receptors by cAMP-dependent protein phosphorylation. Science 257, 661-665.
35. Naassila, M., Ledent, C., and Daoust, M. (2002). Low ethanol sensitivity and increased ethanol consumption in mice lacking adenosine A2A receptors. J. Neurosci. 22, 10487-10493.
36. Nusser, Z., Sieghart, W., and Mody, I. (1999). Differential regulation of synaptic GABAA receptors by cAMP-dependent protein kinase in mouse cerebellar and olfactory bulb neurones. J. Physiol. 521(Pt 2), 421-435.
37. Olsen, R. W., and Sieghart, W. (2009). GABA A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 56, 141-148.
38. Pandey, S. C., Roy, A., and Zhang, H. (2003). The decreased phosphorylation of cyclic adenosine monophos-phate (cAMP) response element binding (CREB) protein in the central amygdala acts as a molecular substrate for anxiety related to ethanol withdrawal in rats. Alcohol. Clin. Exp. Res. 27, 396-409.
39. Park, S. K., Sedore, S. A., Cronmiller, C., and Hirsh, J. (2000). Type II cAMP-dependent protein kinase-deficient Drosophila are viable but show developmental, circadian, and drug response phenotypes. J. Biol. Chem. 275,20588-20596.
40. Paxinos, G., and Watson, C. H. (2007). The Rat Brain in Stereotaxic Coordinates, 6th Edn. London: Elsevier.
41. Poisbeau, P., Cheney, M. C., Browning, M. D., and Mody, I. (1999). Modulation of synaptic GABAA receptor function by PKA and PKC in adult hippocampal neurons. J. Neurosci. 19,674-683.
42. Robello, M., Amico, C., and Cupello, A. (1993). Regulation of GABAA receptor in cerebellar granule cells in culture: differential involvement of kinase activities. Neuroscience 53, 131-138.
43. Saywell, S. A., and Feldman, J. L. (2004). Dynamic interactions of excitatory and inhibitory inputs in hypoglossal motoneurones: respiratory phasing and modulation by PKA. J. Physiol. 554, 879-889.
44. Shew, T., Yip, S.,andSastry, B. R. (2000). Mechanisms involved in tetanus-induced potentiation of fast IPSCs in rat hippocampal CA1 neurons. J. Neurophysiol. 83, 3388-3401.
45. Tang, X., Hernandez, C. C., and Mac-donald, R. L. (2010). Modulation of spontaneous and GABA-evoked tonic alpha4beta3delta and alpha4beta3gamma2L GABAA receptor currents by protein kinase A.J. Neurophysiol. 103, 1007-1019.
46. Tehrani, M. H., Hablitz, J. J., and Barnes, E. M. Jr. (1989). cAMP increases the rate of GABAA receptor desen-sitization in chick cortical neurons. Synapse 4, 126-131.
47. Thiele, T. E., Willis, B., Stadler, J., Reynolds, J. G., Bernstein, I. L., and McKnight, G. S. (2000). High ethanol consumption and low sensitivity to ethanol-induced sedation in protein kinase A-mutant mice. J. Neurosci. 20, RC75.
48. Thomas, P., Mortensen, M., Hosie, A. M., and Smart, T. G. (2005). Dynamic mobility of functional GABAA receptors at inhibitory synapses. Nat. Neurosci. 8, 889-897.
49. Vaello, M. L., Ruiz-Gomez, A., Lerma, J., and Mayor, F. Jr. (1994). Modulation of inhibitory glycine receptors by phosphorylation by protein kinase C and cAMP-dependent protein kinase. J. Biol. Chem. 269, 2002-2008.
50. Wand, G., Levine, M., Zweifel, L., Schwindinger, W., and Abel, T. (2001). The cAMP-protein kinase A signal transduction pathway modulates ethanol consumption and sedative effects of ethanol. J. Neurosci. 21, 5297-5303.
51. Werner, D. F., Kumar, S., Criswell, H. E., Suryanarayanan, A., Alex Fet-zer, J., Comerford, C. E., and Leslie Morrow, A. (2011). PKCgamma is required for ethanol-induced increases in GABA(A) receptor alpha4 subunit expression in cultured cerebral cortical neurons. J. Neurochem. 116, 554-563.
52. White, G., Li, C., and Ishac, E. (1992). 1,9-Dideoxyforskolin does not mimic all cAMP and protein kinase A independent effects of forskolin on GABA activated ion currents in adult rat sensory neurons. Brain Res. 586, 157-161.
53. Yang, X., Oswald, L., and Wand, G. (2003). The cyclic AMP/protein kinase A signal transduction pathway modulates tolerance to sedative and hypothermic effects of ethanol. Alcohol. Clin. Exp. Res. 27, 1220-1225.