Protein kinase C regulates tonic GABAA receptor-mediated inhibition in the hippocampus and thalamus

European Journal of Neuroscience

Volumn 38, Issue 10, 2013, Pages 3408-3423

  Bright, Damian P ^a   Smart, Trevor G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

GABAA receptor; Mouse; PKC; Tonic inhibition

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; ALPHA4BETA2DELTA GABA A RECEPTOR; ISOPROTEIN; PROTEIN KINASE C; RECOMBINANT PROTEIN; SERINE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DENTATE GYRUS; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GRANULE CELL; HIPPOCAMPUS; HUMAN; HUMAN CELL; MALE; MEDIAL GENICULATE BODY; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; ROOM TEMPERATURE; THALAMUS;

GABAA RECEPTOR; MOUSE; PKC; TONIC INHIBITION;

ANIMALS; ENZYME ACTIVATION; GAMMA-AMINOBUTYRIC ACID; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MICE; NEURAL INHIBITION; ORGAN CULTURE TECHNIQUES; PROTEIN KINASE C; RECEPTORS, GABA-A; THALAMUS;

EID: 84887815481     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12352     Document Type: Article

References (59)

1. Abramian, A.M., Comenencia-Ortiz, E., Vithlani, M., Tretter, E.V., Sieghart, W., Davies, P.A. & Moss, S.J. (2010) Protein kinase C phosphorylation regulates membrane insertion of GABAA receptor subtypes that mediate tonic inhibition. J. Biol. Chem., 285, 41795-41805.
2. Ashby, M.C., Ibaraki, K. & Henley, J.M. (2004) It's green outside: tracking cell surface proteins with pH-sensitive GFP. Trends Neurosci., 27, 257-261.
3. Belelli, D., Peden, D.R., Rosahl, T.W., Wafford, K.A. & Lambert, J.J. (2005) Extrasynaptic GABAA receptors of thalamocortical neurons: a molecular target for hypnotics. J. Neurosci., 25, 11513-11520.
4. Brandon, N.J., Delmas, P., Kittler, J.T., McDonald, B.J., Sieghart, W., Brown, D.A., Smart, T.G. & 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.
5. Brandon, N.J., Jovanovic, J.N., Colledge, M., Kittler, J.T., Brandon, J.M., Scott, J.D. & 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 beta subunits. Mol. Cell. Neurosci., 22, 87-97.
6. Brickley, S.G. & Mody, I. (2012) Extrasynaptic GABA(A) receptors: their function in the CNS and implications for disease. Neuron, 73, 23-34.
7. Brickley, S.G., Cull-Candy, S.G. & Farrant, M. (1996) Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. J. Physiol., 497(Pt 3), 753-759.
8. Bright, D.P. & Brickley, S.G. (2008) Acting locally but sensing globally: impact of GABAergic synaptic plasticity on phasic and tonic inhibition in the thalamus. J. Physiol., 586, 5091-5099.
9. Bright, D.P., Aller, M.I. & Brickley, S.G. (2007) Synaptic release generates a tonic GABA(A) receptor-mediated conductance that modulates burst precision in thalamic relay neurons. J. Neurosci., 27, 2560-2569.
10. Bright, D.P., Renzi, M., Bartram, J., McGee, T.P., MacKenzie, G., Hosie, A.M., Farrant, M. & Brickley, S.G. (2011) Profound desensitization by ambient GABA limits activation of delta-containing GABAA receptors during spillover. J. Neurosci., 31, 753-763.
11. Chadderton, P., Margrie, T.W. & Hausser, M. (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature, 428, 856-860.
12. Cherubini, E. (2012) Phasic GABAA-mediated inhibition. In Noebels, J.L., Avoli, M., Rogawski, M.A., Olsen, R.W. & Delgado-Escueta, A.V. (Eds), Jasper's Basic Mechanisms of the Epilepsies. US National Center for Biotechnology Information, Bethesda, MD.
13. Comenencia-Ortiz, E.J., Abramian, A.M., Deeb, T.Z., Davies, P.A. & Moss, S.J. (2010) Role of protein kinase C phosphorylation in neurosteroid modulation of extrasynaptic GABA(A) receptors. 2010 Neuroscience Meeting Planner. Program No. 239.2/E47. 2010. Society for Neuroscience, 2010.
14. Cope, D.W., Hughes, S.W. & Crunelli, V. (2005) GABAA receptor-mediated tonic inhibition in thalamic neurons. J. Neurosci., 25, 11553-11563.
15. Cope, D.W., Di, G.G., Fyson, S.J., Orban, G., Errington, A.C., Lorincz, M.L., Gould, T.M., Carter, D.A. & Crunelli, V. (2009) Enhanced tonic GABAA inhibition in typical absence epilepsy. Nat. Med., 15, 1392-1398.
16. Coulter, D.A. & Carlson, G.C. (2007) Functional regulation of the dentate gyrus by GABA-mediated inhibition. Prog. Brain Res., 163, 235-243.
17. Damgaard, T., Plath, N., Neill, J.C. & Hansen, S.L. (2011) Extrasynaptic GABAA receptor activation reverses recognition memory deficits in an animal model of schizophrenia. Psychopharmacology, 214, 403-413.
18. Duguid, I., Branco, T., London, M., Chadderton, P. & Hausser, M. (2012) Tonic inhibition enhances fidelity of sensory information transmission in the cerebellar cortex. J. Neurosci., 32, 11132-11143.
19. Farrant, M. & Nusser, Z. (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci., 6, 215-229.
20. Glykys, J. & Mody, I. (2007) Activation of GABAA receptors: views from outside the synaptic cleft. Neuron, 56, 763-770.
21. Heinemann, U., Beck, H., Dreier, J.P., Ficker, E., Stabel, J. & Zhang, C.L. (1992) The dentate gyrus as a regulated gate for the propagation of epileptiform activity. Epilepsy Res. Suppl., 7, 273-280.
22. Herd, M.B., Haythornthwaite, A.R., Rosahl, T.W., Wafford, K.A., Homanics, G.E., Lambert, J.J. & Belelli, D. (2008) The expression of GABAA beta subunit isoforms in synaptic and extrasynaptic receptor populations of mouse dentate gyrus granule cells. J. Physiol., 586, 989-1004.
23. Holdefer, R.N., Norton, T.T. & Godwin, D.W. (1989) Effects of bicuculline on signal detectability in lateral geniculate nucleus relay cells. Brain Res., 488, 341-347.
24. Houston, C.M., Lee, H.H., Hosie, A.M., Moss, S.J. & Smart, T.G. (2007) Identification of the sites for CaMK-II-dependent phosphorylation of GABA(A) receptors. J. Biol. Chem., 282, 17855-17865.
25. Hubel, D.H. & Wiesel, T.N. (1961) Integrative action in the cat's lateral geniculate body. J. Physiol., 155, 385-398.
26. Jia, F., Yue, M., Chandra, D., Keramidas, A., Goldstein, P.A., Homanics, G.E. & Harrison, N.L. (2008) Taurine is a potent activator of extrasynaptic GABA(A) receptors in the thalamus. J. Neurosci., 28, 106-115.
27. Jones, M.V. & Westbrook, G.L. (1997) Shaping of IPSCs by endogenous calcineurin activity. J. Neurosci., 17, 7626-7633.
28. Kittler, J.T. & Moss, S.J. (2003) Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr. Opin. Neurobiol., 13, 341-347.
29. Krishek, B.J., Xie, X., Blackstone, C., Huganir, R.L., Moss, S.J. & Smart, T.G. (1994) Regulation of GABAA receptor function by protein kinase C phosphorylation. Neuron, 12, 1081-1095.
30. Lin, Y.F., Browning, M.D., Dudek, E.M. & Macdonald, R.L. (1994) Protein kinase C enhances recombinant bovine alpha 1 beta 1 gamma 2L GABAA receptor whole-cell currents expressed in L929 fibroblasts. Neuron, 13, 1421-1431.
31. Luscher, B., Fuchs, T. & Kilpatrick, C.L. (2011) GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron, 70, 385-409.
32. Machu, T.K., Dillon, G.H., Huang, R., Lovinger, D.M. & Leidenheimer, N.J. (2006) Temperature: an important experimental variable in studying PKC modulation of ligand-gated ion channels. Brain Res., 1086, 1-8.
33. Maguire, J.L., Stell, B.M., Rafizadeh, M. & Mody, I. (2005) Ovarian cycle-linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat. Neurosci., 8, 797-804.
34. McDonald, B.J., Amato, A., Connolly, C.N., Benke, D., Moss, S.J. & Smart, T.G. (1998) Adjacent phosphorylation sites on GABAA receptor beta subunits determine regulation by cAMP-dependent protein kinase. Nat. Neurosci., 1, 23-28.
35. Merali, Z., Du, L., Hrdina, P., Palkovits, M., Faludi, G., Poulter, M.O. & Anisman, H. (2004) Dysregulation in the suicide brain: mRNA expression of corticotropin-releasing hormone receptors and GABA(A) receptor subunits in frontal cortical brain region. J. Neurosci., 24, 1478-1485.
36. Mitchell, S.J. & Silver, R.A. (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron, 38, 433-445.
37. Mortensen, M., Ebert, B., Wafford, K. & Smart, T.G. (2010) Distinct activities of GABA agonists at synaptic- and extrasynaptic-type GABAA receptors. J. Physiol., 588, 1251-1268.
38. Moss, S.J. & Smart, T.G. (1996) Modulation of amino acid-gated ion channels by protein phosphorylation. Int. Rev. Neurobiol., 39, 1-52.
39. Moss, S.J., Gorrie, G.H., Amato, A. & Smart, T.G. (1995) Modulation of GABAA receptors by tyrosine phosphorylation. Nature, 377, 344-348.
40. Mtchedlishvili, Z. & Kapur, J. (2006) High-affinity, slowly desensitizing GABAA receptors mediate tonic inhibition in hippocampal dentate granule cells. Mol. Pharmacol., 69, 564-575.
41. Naylor, D.E., Liu, H. & Wasterlain, C.G. (2005) Trafficking of GABA(A) receptors, loss of inhibition, and a mechanism for pharmacoresistance in status epilepticus. J. Neurosci., 25, 7724-7733.
42. Nusser, Z. & Mody, I. (2002) Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J. Neurophysiol., 87, 2624-2628.
43. Nusser, Z., Sieghart, W. & 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.
44. Olmos-Serrano, J.L., Paluszkiewicz, S.M., Martin, B.S., Kaufmann, W.E., Corbin, J.G. & Huntsman, M.M. (2010) Defective GABAergic neurotransmission and pharmacological rescue of neuronal hyperexcitability in the amygdala in a mouse model of fragile X syndrome. J. Neurosci., 30, 9929-9938.
45. Pavlov, I., Savtchenko, L.P., Kullmann, D.M., Semyanov, A. & Walker, M.C. (2009) Outwardly rectifying tonically active GABAA receptors in pyramidal cells modulate neuronal offset, not gain. J. Neurosci., 29, 15341-15350.
46. Peden, D.R., Petitjean, C.M., Herd, M.B., Durakoglugil, M.S., Rosahl, T.W., Wafford, K., Homanics, G.E., Belelli, D., Fritschy, J.M. & Lambert, J.J. (2008) Developmental maturation of synaptic and extrasynaptic GABAA receptors in mouse thalamic ventrobasal neurones. J. Physiol., 586, 965-987.
47. Pirker, S., Schwarzer, C., Wieselthaler, A., Sieghart, W. & Sperk, G. (2000) GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience, 101, 815-850.
48. Poisbeau, P., Cheney, M.C., Browning, M.D. & Mody, I. (1999) Modulation of synaptic GABAA receptor function by PKA and PKC in adult hippocampal neurons. J. Neurosci., 19, 674-683.
49. Saliba, R.S., Kretschmannova, K. & Moss, S.J. (2012) Activity-dependent phosphorylation of GABA(A) receptors regulates receptor insertion and tonic current. EMBO J., 31, 2937-2951.
50. Scimemi, A., Semyanov, A., Sperk, G., Kullmann, D.M. & Walker, M.C. (2005) Multiple and plastic receptors mediate tonic GABAA receptor currents in the hippocampus. J. Neurosci., 25, 10016-10024.
51. Sillito, A.M. & Kemp, J.A. (1983) The influence of GABAergic inhibitory processes on the receptive field structure of X and Y cells in cat dorsal lateral geniculate nucleus (dLGN). Brain Res., 277, 63-77.
52. Song, I., Savtchenko, L. & Semyanov, A. (2011) Tonic excitation or inhibition is set by GABA(A) conductance in hippocampal interneurons. Nat. Commun., 2, 376.
53. Stell, B.M., Brickley, S.G., Tang, C.Y., Farrant, M. & Mody, I. (2003) 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.
54. Sur, C., Farrar, S.J., Kerby, J., Whiting, P.J., Atack, J.R. & McKernan, R.M. (1999) Preferential coassembly of alpha4 and delta subunits of the gamma-aminobutyric acidA receptor in rat thalamus. Mol. Pharmacol., 56, 110-115.
55. Vithlani, M., Terunuma, M. & Moss, S.J. (2011) The dynamic modulation of GABA(A) receptor trafficking and its role in regulating the plasticity of inhibitory synapses. Physiol. Rev., 91, 1009-1022.
56. Wang, X., Wei, Y., Vaingankar, V., Wang, Q., Koepsell, K., Sommer, F.T. & Hirsch, J.A. (2007) Feedforward excitation and inhibition evoke dual modes of firing in the cat's visual thalamus during naturalistic viewing. Neuron, 55, 465-478.
57. Wang, X., Sommer, F.T. & Hirsch, J.A. (2011) Inhibitory circuits for visual processing in thalamus. Curr. Opin. Neurobiol., 21, 726-733.
58. Wu-Zhang, A.X. & Newton, A.C. (2013) Protein kinase C pharmacology: refining the toolbox. Biochem. J., 452, 195-209.
59. Zhan, R.Z. & Nadler, J.V. (2009) Enhanced tonic GABA current in normotopic and hilar ectopic dentate granule cells after pilocarpine-induced status epilepticus. J. Neurophysiol., 102, 670-681.