Neurosteroids Shift Partial Agonist Activation of GABAA Receptor Channels from Low- to High-Efficacy Gating Patterns

Journal of Neuroscience

Volumn 23, Issue 34, 2003, Pages 10934-10943

  Bianchi, Matt T ^a   Macdonald, Robert L ^b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

Desensitization; GABAA receptor; Modal gating; Neurosteroid; Taurine; alanine; subunit

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ALANINE; ISOPROTEIN; NEUROSTEROID; PROTEIN SUBUNIT; TAURINE;

ALLOSTERISM; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; DESENSITIZATION; EMBRYO; GABAERGIC TRANSMISSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SYNAPSE;

EID: 0345491872     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-34-10934.2003     Document Type: Article

References (71)

1. A receptors characterized by fluorescence resonance energy transfer-derived measurements of membrane potential. J Biol Chem 276:38934-38939.
2. A receptor subunits: analysis of transient single-cell expression utilizing a fluorescent substrate/marker gene technique. J Neurosci 13:1418-1428.
3. Bai D, Zhu G, Pennefather P, Jackson MF, MacDonald JF, Orser BA (2001) Distinct functional and pharmacological properties of tonic and quantal inhibitory postsynaptic currents mediated by gamma-aminobutyric acid(A) receptors in hippocampal neurons. Mol Pharmacol 59:814-824.
4. A receptor γ2L subunit produces an apparent decrease in desensitization by stabilizing open states without altering desensitized states. Neuropharmacology 41:737-744.
5. Bianchi MT, Haas KF, Macdonald RL (2002) alpha1 and alpha6 subunits specify distinct desensitization, deactivation and neurosteroid modulation of GABA(A) receptors containing the delta subunit. Neuropharmacology 43:492-502.
6. A receptors. J Physiol (Lond) 497:753-759.
7. Brickley SG, Revilla V, Cull-Candy SG, Wisden W, Farrant M (2001) Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409:88-92.
8. Brown N, Kerby J, Bonnert TP, Whiting PJ, Wafford KA (2002) Pharmacological characterization of a novel cell line expressing human alpha(4)beta(3)delta GABA(A) receptors. Br J Pharmacol 136:965-974.
9. A IPSCs during development in rat hippocampal or cerebellar slices. J Physiol (Lond) 521:437-449.
10. Delcour AH, Tsien RW (1993) Altered prevalence of gating modes in neurotransmitter inhibition of N-type calcium channels. Science 259:980-984.
11. Ebert B, Thompson SA, Saounatsou K, McKernan R, Krogsgaard-Larsen P, Wafford KA (1997) Differences in agonist/antagonist binding affinity and receptor transduction using recombinant human gamma-aminobutyric acid type A receptors. Mol Pharmacol 52:1150-1156.
12. Fancsik A, Linn DM, Tasker JG (2000) Neurosteroid modulation of GABA IPSCs is phosphorylation dependent. J Neurosci 20:3067-3075.
13. Filatov GN, White MW (1995) The role of conserved leucines in the M2 domain of the acetylcholine receptor in channel gating. Mol Pharmacol 48:379-384.
14. A receptors containing γ2 or δ subtypes expressed with α1 and β3 subtypes in L929 cells. J Physiol (Lond) 505:283-297.
15. A receptors in transfected L929 cells isolated by immunomagnetic bead separation. Neuropharmacology 36:63-73.
16. A receptor currents in mouse fibroblasts. J Physiol (Lond) 514:27-45.
17. A receptors by the non-steroidal anti-inflammatory agent, mefenamic acid. Eur J Neurosci 11:2897-2905.
18. Hamann M, Rossi DJ, Attwell D (2002) Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33:625-633.
19. Harrison NL, Vicini S, Barker JL (1987) A steroid anesthetic prolongs inhibitory postsynaptic currents in cultured rat hippocampal neurons. J Neurosci 7:604-609.
20. Herlitze S, Zhong H, Scheuer T, Catterall WA (2001) Allosteric modulation of Ca2+ channels by G proteins, voltage-dependent facilitation, protein kinase C, and Ca(v)beta subunits. Proc Natl Acad Sci USA 98:4699-4704.
21. Hess P, Lansman JB, Tsien RW (1984) Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature 311:538-544.
22. Huxtable RJ (1989) Taurine in the central nervous system and the mammalian actions of taurine. Prog Neurobiol 32:471-533.
23. Khakh BS, Proctor WR, Dunwiddie TV, Labarca C, Lester HA (1999) Allosteric control of gating and kinetics at P2X(4) receptor channels. J Neurosci 19:7289-7299.
24. A receptor partial agonist, 4-PIOL. Neuropharmacology 35:1181-1191.
25. Krogsgaard-Larsen P, Falch E, Schousboe A, Curtis DR, Lodge D (1980) Piperidine-4-sulphonic acid, a new specific GABA agonist. J Neurochem 34:756-759.
26. Krogsgaard-Larsen P, Snowman A, Lummis SC, Olsen RW (1981) Characterization of the binding of the GABA agonist [3H]piperidine-4-sulphonic acid to bovine brain synaptic membranes. J Neurochem 37:401-409.
27. Labarca C, Nowak MW, Zhang H, Tang L, Deshpande P, Lester HA (1995) Channel gating governed symmetrically by conserved leucine residues in the M2 domain of nicotinic receptors. Nature 376:514-516.
28. A receptor function. Trends Pharmacol Sci 16:295-303.
29. A receptors to neurosteroids. J Neurochem 57:1818-1821.
30. A receptor in frog pituitary melanotrophs. J Physiol (Lond) 504:387-400.
31. Lees G, Edwards MD (1998) Modulation of recombination human gamma-aminobutyric acidA receptors by isoflurane: influence of the delta subunit. Anesthesiology 88:206-217.
32. Leidenheimer NJ, Chapell R (1997) Effects of PKC activation and receptor desensitization on neurosteroid modulation of GABA(A) receptors. Brain Res Mol Brain Res 52:173-181.
33. Lerma J, Herranz AS, Herreras O, Abraira V, Martin DR (1986) In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res 384:145-155.
34. Low K, Crestani F, Keist R, Benke D, Brunig I, Benson JA, Fritschy JM, Rulicke T, Bluethmann H, Mohler H, Rudolph U (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290:131-134.
35. A receptor channels. Annu Rev Neurosci 17:569-602.
36. Maksay G, Thompson SA, Wafford KA (2000) Allosteric modulators affect the efficacy of partial agonists for recombinant GABA(A) receptors. Br J Pharmacol 129:1794-1800.
37. Marrion NV (1993) Selective reduction of one mode of M-channel gating by muscarine in sympathetic neurons. Neuron 11:77-84.
38. Marrion NV (1996) Calcineurin regulates M channel modal gating in sympathetic neurons. Neuron 16:163-173.
39. McKernan RM, Rosahl TW, Reynolds DS, Sur C, Wafford KA, Atack JR, Farrar S, Myers J, Cook G, Ferris P, Garrett L, Bristow L, Marshall G, Macaulay A, Brown N, Howell O, Moore KW, Carling RW, Street LJ, Castro JL, et al. (2000) Sedative but not anxiolytic properties of benzodiazepines are mediated by the GABA(A) receptor alpha1 subtype. Nat Neurosci 3:587-592.
40. A receptors. Brain Res Brain Res Rev 29:196-217.
41. Mellon SH, Griffin LD (2002) Neurosteroids: biochemistry and clinical significance. Trends Endocrinol Metab 13:35-43.
42. Mihalek RM, Banerjee PK, Korpi ER, Quinlan JJ, Firestone LL, Mi ZP, Lagenaur C, Tretter V, Sieghart W, Anagnostaras G, Sage JR, Fanselow MS, Guidotti A, Spigelman I, Li Z, DeLorey TM, Olsen RW, Homanics GE (1999) Attenuated sensitivity to neuroactive steroids in γ-aminobutyrate type A receptor delta subunit knock-out mice. Proc Natl Acad Sci USA 96:12905-12910.
43. Milone M, Wang HL, Ohno K, Prince R, Fukudome T, Shen XM, Brengman JM, Griggs RC, Sine SM, Engel AG (1998) Mode switching kinetics produced by a naturally occurring mutation in the cytoplasmic loop of the human acetylcholine receptor epsilon subunit. Neuron 20:575-588.
44. A receptor of mouse spinal neurones in culture. Exp Physiology 75:199-209.
45. Naranjo D, Brehm P (1993) Modal shifts in acetylcholine receptor channel gating confer subunit-dependent desensitization. Science 260:1811-1814.
46. A receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 18:1693-1703.
47. A receptor complex: structure and function In: Glutamate and GABA receptors and transporters: structure, function, and pharmacology, Sec 9 (Egebjerg J, Schousboe A, Krogsgaard-Larsen P, eds), pp 203-235. London: Taylor and Francis.
48. O'Shea SM, Wong LC, Harrison NL (2000) Propofol increases agonist efficacy at the GABA(A) receptor. Brain Res 852:344-348.
49. Paul SM, Purdy RH (1992) Neuroactive steroids. FASEB J 6:2311-2322.
50. A receptor. Neuron 4:759-765.
51. Rossi DJ, Hamann M (1998) Spillover-mediated transmission at inhibitory synapses promoted by high affinity alpha6 subunit GABA(A) receptors and glomerular geometry. Neuron 20:783-795.
52. Rudolph U, Crestani F, Benke D, Brunig I, Benson JA, Fritschy JM, Martin JR, Bluethmann H, Mohler H (1999) Benzodiazepine actions mediated by specific gamma-aminobutyric acid(A) receptor subtypes. Nature 401:796-800.
53. Sakai Y, Okamoto K, Kimura H (1985) Pharmacological evidence for taurine as an inhibitory neurotransmitter in the cerebellum. Prog Clin Biol Res 179:313-319.
54. Schonherr R, Mannuzzu L, Isacoff E, Heinemann S (2002) Conformational switch between slow and fast gating modes. Allosteric regulation of voltage sensor mobility in the EAG K(+) channel. Neuron 35:935.
55. A receptors. Trends Pharmacol 18:425-429.
56. Steinbach JH, Akk G (2001) Modulation of GABA(A) receptor channel gating by pentobarbital. J Physiol (Lond) 537:715-733.
57. Stell BM, Mody I (2002) Receptors with different affinities mediate phasic and tonic GABA(A) conductances in hippocampal neurons. J Neurosci 22:RC223.
58. Stevenson A, Wingrove PB, Whiting PJ, Wafford KA (1995) beta-Carboline gamma-aminobutyric acidA receptor inverse agonists modulate gamma-aminobutyric acid via the loreclezole binding site as well as the benzodiazepine site. Mol Pharmacol 48:965-969.
59. Thompson SA, Arden SA, Marshall G, Wingrove PB, Whiting PJ, Wafford KA (1999) Residues in transmembrane domains I and II determine gamma-aminobutyric acid type A receptor subtype-selective antagonism by furosemide. Mol Pharmacol 55:993-999.
60. Thompson SA, Wingrove PB, Connelly L, Whiting PJ, Wafford KA (2002) Tracazolate reveals a novel type of allosteric interaction with recombinant gamma-aminobutyric acid(A) receptors. Mol Pharmacol 61:861-869.
61. A receptor single-channel kinetic properties of mouse spinal cord neurons in culture. J Physiol (Lond) 456:215-245.
62. A receptor channels. Neurosci Lett 96:89-95.
63. Wang HL, Ohno K, Milone M, Brengman JM, Evoli A, Batocchi AP, Middleton LT, Christodoulou K, Engel AG, Sine SM (2000) Fundamental gating mechanism of nicotinic receptor channel revealed by mutation causing a congenital myasthenic syndrome. J Gen Physiol 116:449-462.
64. Wingrove PB, Wafford KA, Bain C, Whiting PJ (1994) The modulatory action of loreclezole at the gamma-aminobutyric acid type A receptor is determined by a single amino acid in the beta 2 and beta 3 subunit. Proc Natl Acad Sci USA 91:4569-4573.
65. A receptors containing the 8 subunit. J Neurosci 22:1541-1549.
66. Wu Y, Wang W, Richerson GB (2003) Vigabatrin induces tonic inhibition via GABA transporter reversal without increasing vesicular GABA release. J Neurophysiol 89:2021-2034.
67. Yue DT, Herzig S, Marban E (1990) Beta-adrenergic stimulation of calcium channels occurs by potentiation of high-activity gating modes. Proc Natl Acad Sci USA 87:753-757.
68. Zhong H, Li B, Scheuer T, Catterall WA (2001) Control of gating mode by a single amino acid residue in transmembrane segment IS3 of the N-type Ca2+ channel. Proc Natl Acad Sci USA 98:4705-4709.
69. Zhou JY, Potts JF, Trimmer JS, Agnew WS, Sigworth FJ (1991) Multiple gating modes and the effect of modulating factors on the microI sodium channel. Neuron 7:775-785.
70. A channel deactivation by altering kinetics of desensitized states. J Neurosci 17:4022-4031.
71. A receptors. J Neurosci 16:6648-6656.