Context-dependent modulation of GABAAR-mediated tonic currents

Journal of Neuroscience

Volumn 36, Issue 2, 2016, Pages 607-621

  Patel, Bijal ^a   Bright, Damian P ^a   Mortensen, Martin ^a   Frølund, Bente ^b   Smart, Trevor G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

4 PIOL; Extrasynaptic GABA receptors; GABA; Partial agonist; Synaptic inhibition; Tonic inhibition

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 5-(4-PIPERIDYL)ISOXAZOL-3-OL; AMINO ACID RECEPTOR AFFECTING AGENT; GABAERGIC RECEPTOR AFFECTING AGENT; ISOXAZOLE DERIVATIVE; PIPERIDINE DERIVATIVE; PROTEIN SUBUNIT;

ANIMAL; BRAIN; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENETICS; HUMAN; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; MEMBRANE POTENTIAL; METABOLISM; NERVE CELL; NERVE CELL INHIBITION; NEWBORN; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PROTEIN SUBUNIT; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID AGENTS; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; HUMANS; IN VITRO TECHNIQUES; INHIBITORY POSTSYNAPTIC POTENTIALS; ISOXAZOLES; MEMBRANE POTENTIALS; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PIPERIDINES; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A;

EID: 84954342115     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2047-15.2016     Document Type: Article

References (72)

1. Atack JR (2010) Preclinical and clinical pharmacology of the GABAA receptor α5 subtype-selective inverse agonist α5IA. Pharmacol Ther 125:11- 26. CrossRef Medline
2. Atack JR, Bayley PJ, Seabrook GR, Wafford KA, McKernan RM, Dawson GR (2006) L-655,708 enhances cognition in rats but is not proconvulsant at a dose selective for α5-containing GABAA receptors. Neuropharmacology 51:1023-1029. CrossRef Medline
3. Attwell D, Barbour B, Szatkowski M (1993) Nonvesicular release of neurotransmitter. Neuron 11:401- 407. CrossRef Medline
4. Axmacher N, Draguhn A (2004) Inhibition of GABA release by presynaptic ionotropic GABA receptors in hippocampal CA3. Neuroreport 15:329- 334. CrossRef Medline
5. Ballard TM, Knoflach F, Prinssen E, Borroni E, Vivian JA, Basile J, Gasser R, Moreau JL, Wettstein JG, Buettelmann B, Knust H, Thomas AW, Trube G, Hernandez MC (2009) RO4938581, a novel cognitive enhancer acting at GABAA α5 subunit-containing receptors. Psychopharmacology (Berl) 202:207-223. CrossRef Medline
6. Belelli D, Harrison NL, Maguire J, Macdonald RL, Walker MC, Cope DW (2009) Extrasynaptic GABAA receptors: form, pharmacology and function. J Neurosci 29:12757-12763. CrossRef Medline
7. Boddum K, Frølund B, Kristiansen U (2014) The GABAA antagonist DPP- 4-PIOL selectively antagonises tonic over phasic GABAergic currents in dentate gyrus granule cells. Neurochem Res 39:2078 -2084. CrossRef Medline
8. Borden LA (1996) GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem Int 29:335-356. CrossRef Medline
9. Borden LA, Murali Dhar TG, Smith KE, Weinshank RL, Branchek TA, Gluchowski C (1994) Tiagabine, SK&F 89976-A, CI-966, and NNC-711 are selective for the cloned GABA transporter GAT-1. Eur J Pharmacol 269:219 -224. CrossRef Medline
10. Braudeau J, Delatour B, Duchon A, Pereira PL, Dauphinot L, de Chaumont F, Olivo-Marin JC, Dodd RH, Hérault Y, PotierMC (2011) Specific targeting of the GABAA receptor α5 subtype by a selective inverse agonist restores cognitive deficits in Down syndrome mice. J Psychopharmacol 25:1030 -1042. CrossRef Medline
11. Brickley SG, Mody I (2012) Extrasynaptic GABAA receptors: their function in the CNS and implications for disease. Neuron 73:23-34. CrossRef Medline
12. Brickley SG, Cull-Candy SG, FarrantM (1999) Single-channel properties of synaptic and extrasynaptic GABAA receptors suggest differential targeting of receptor subtypes. J Neurosci 19:2960 -2973. Medline
13. Brickley SG, Revilla V, Cull-Candy SG, Wisden W, FarrantM (2001) Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409:88 -92. CrossRef Medline
14. Bright DP, Aller MI, Brickley SG (2007) Synaptic release generates a tonic GABAA receptor-mediated conductance that modulates burst precision in thalamic relay neurons. J Neurosci 27:2560 -2569. CrossRef Medline
15. Brown N, Kerby J, Bonnert TP, Whiting PJ, Wafford KA (2002) Pharmacological characterization of a novel cell line expressing human α4β3δ GABAA receptors. Br J Pharmacol 136:965-974. CrossRef Medline
16. Caraiscos VB, Elliott EM, You-Ten KE, Cheng VY, Belelli D, Newell JG, Jackson MF, Lambert JJ, Rosahl TW, Wafford KA, MacDonald JF, Orser BA (2004) Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunit-containing gamma-aminobutyric acid type A receptors. Proc Natl Acad Sci U S A 101:3662-3667. CrossRef Medline
17. Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST (2010) Re- ducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 468:305-309. CrossRef Medline
18. Cope DW, Hughes SW, Crunelli V (2005) GABAA receptor-mediated tonic inhibition in thalamic neurons. J Neurosci 25:11553-11563. CrossRef Medline
19. Cope DW, Di Giovanni G, Fyson SJ, Orbán G, Errington AC, Lorincz ML, Gould TM, Carter DA, Crunelli V (2009) Enhanced tonic GABAA inhibition in typical absence epilepsy. Nat Med 15:1392-1398. CrossRef Medline
20. DeBiasi S, Vitellaro-Zuccarello L, Brecha NC (1998) Immunoreactivity for the GABA transporter-1 and GABA transporter-3 is restricted to astrocytes in the rat thalamus: a light and electron-microscopic immunolocalization. Neuroscience 83:815- 828. CrossRef Medline
21. deGroote L, Linthorst AC (2007) Exposure to novelty and forced swimming evoke stressor-dependent changes in extracellular GABA in the rat hippocampus. Neuroscience 148:794-805. CrossRef Medline
22. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors. Nat Rev Neurosci 6:215-229. CrossRef Medline
23. Fritschy JM, Benke D, Mertens S, Oertel WH, Bachi T, Möhler H (1992) Five subtypes of type A gamma-aminobutyric acid receptors identified in neurons by double and triple immunofluorescence staining with subunitspecific antibodies. Proc Natl Acad Sci U S A 89:6726-6730. CrossRef Medline
24. Frølund B, Kristiansen U, Brehm L, Hansen AB, Krogsgaard-Larsen P, Falch E (1995) Partial GABAA receptor agonists: synthesis and in vitro pharmacology of a series of nonannulated analogs of 4,5,6,7- tetrahydroisoxazolo[4,5-c]pyridin-3-ol. J Med Chem 38:3287-3296. CrossRef Medline
25. Gielen MC, Lumb MJ, Smart TG (2012) Benzodiazepines modulate GABAA receptors by regulating the preactivation step after GABA binding. J Neurosci 32:5707-5715. CrossRef Medline
26. Glaeser BS, HareTA (1975) Measurement ofGABAin human cerebrospinal fluid. Biochem Med 12:274 -282. CrossRef Medline
27. Glykys J, Peng Z, Chandra D, Homanics GE, Houser CR, Mody I (2007) A new naturally occurring GABAA receptor subunit partnership with high sensitivity to ethanol. Nat Neurosci 10:40-48. CrossRef Medline
28. Glykys J, Mann EO, Mody I (2008) Which GABAA receptor subunits are necessary for tonic inhibition in the hippocampus? J Neurosci 28:1421- 1426. CrossRef Medline
29. Hoestgaard-Jensen K, Dalby NO, Wolinsky TD, Murphey C, Jones KA, Rottländer M, Frederiksen K, Watson WP, Jensen K, Ebert B (2010) Pharmacological characterization of a novel positive modulator at α4β3δ-containing extrasynaptic GABAA receptors. Neuropharmacology 58:702-711. CrossRef Medline
30. Hoestgaard-Jensen K, O'Connor RM, Dalby NO, Simonsen C, Finger BC, Golubeva A, Hammer H, Bergmann ML, Kristiansen U, Krogsgaard- Larsen P, Bräuner-Osborne H, Ebert B, Frølund B, Cryan JF, Jensen AA (2013) The orthosteric GABAA receptor ligand thio-4-PIOL displays distinctly different functional properties at synaptic and extrasynaptic receptors. Br J Pharmacol 170:919 -932. CrossRef Medline
31. Houston CM, Smart TG (2006) CaMK-II modulation of GABAA receptors expressed in HEK293, NG108-15 and rat cerebellar granule neurons. Eur J Neurosci 24:2504 -2514. CrossRef Medline
32. Houston CM, McGee TP, Mackenzie G, Troyano-Cuturi K, Rodriguez PM, Kutsarova E, Diamanti E, Hosie AM, Franks NP, Brickley SG (2012) Are extrasynaptic GABAA receptors important targets for sedative/hypnotic drugs? J Neurosci 32:3887-3897. CrossRef Medline
33. Jensen ML, Wafford KA, Brown AR, Belelli D, Lambert JJ, Mirza NR (2013) A study of subunit selectivity, mechanism and site of action of the δ selective compound 2 (DS2) at human recombinant and rodent native GABAA receptors. Br J Pharmacol 168:1118 -1132. CrossRef Medline
34. Jo S, Yarishkin O, Hwang YJ, Chun YE, Park M, Woo DH, Bae JY, Kim T, Lee J, Chun H, Park HJ, Lee da Y, Hong J, Kim HY, Oh SJ, Park SJ, Lee H, Yoon BE, Kim Y, Jeong Y, et al. (2014) GABA from reactive astrocytes impairs memory in mouse models of Alzheimer's disease. Nat Med 20: 886-896. CrossRef Medline
35. Jones A, Korpi ER, McKernan RM, Pelz R, Nusser Z, Mäkelä R, Mellor JR, Pollard S, Bahn S, Stephenson FA, Randall AD, Sieghart W, Somogyi P, Smith AJ, WisdenW (1997) Ligand-gated ion channel subunit partnerships: GABAA receptor α6 subunit gene inactivation inhibits δ subunit expression. J Neurosci 17:1350 -1362. Medline
36. Jones MV, Westbrook GL (1995) Desensitized states prolong GABAA channel responses to brief agonist pulses. Neuron 15:181-191. CrossRef Medline
37. Kasugai Y, Swinny JD, Roberts JD, Dalezios Y, Fukazawa Y, Sieghart W, Shigemoto R, Somogyi P (2010) Quantitative localisation of synaptic and extrasynaptic GABAA receptor subunits on hippocampal pyramidal cells by freeze-fracture replica immunolabelling. Eur J Neurosci 32:1868- 1888. CrossRef Medline
38. Kristiansen U, Lambert JD, Falch E, Krogsgaard-Larsen P (1991) Electrophysiological studies of the GABAA receptor ligand, 4-PIOL, on cultured hippocampal neurones. Br J Pharmacol 104:85-90. CrossRef Medline
39. Kristiansen U, Barker JL, Serafini R (1995) The low efficacy gammaaminobutyric acid typeAagonist 5-(4-piperidyl)isoxazol-3-ol opens brief Cl- channels in embryonic rat olfactory bulb neurons. Mol Pharmacol 48:268 -279. Medline
40. Krogsgaard-Larsen P, Frølund B, Liljefors T (2002) Specific GABAA agonists and partial agonists. Chem Rec 2:419-430. CrossRef
41. Lerma J, Herranz AS, Herreras O, Abraira V, Martín del Río R (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. CrossRef Medline
42. Liang J, Cagetti E, Olsen RW, Spigelman I (2004) Altered pharmacology of synaptic and extrasynaptic GABAA receptors on CA1 hippocampal neurons is consistent with subunit changes in a model of alcohol withdrawal and dependence. J Pharmacol Exp Ther 310:1234 -1245. CrossRef
43. Li P, Akk G (2015) Synaptic-type α1β2γ2L GABAA receptors produce large persistent currents in the presence of ambient GABA and anesthetic drugs. Mol Pharmacol 87:776 -781. CrossRef Medline
44. Maconochie DJ, Zempel JM, Steinbach JH (1994) How quickly can GABAA receptors open? Neuron 12:61-71. CrossRef Medline
45. Mangan PS, Sun C, Carpenter M, Goodkin HP, Sieghart W, Kapur J (2005) Cultured hippocampal pyramidal neurons express two kinds of GABAA receptors. Mol Pharmacol 67:775-788. CrossRef Medline
46. Mann EO, Mody I (2010) Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons. Nat Neurosci 13:205-212. CrossRef Medline
47. Martínez-Cué C, Martínez P, Rueda N, Vidal R, García S, Vidal V, Corrales A, Montero JA, Pazosá, Flórez J, Gasser R, Thomas AW, Honer M, Knoflach F, Trejo JL, Wettstein JG, Hernández MC (2013) Reducing GABAA α5 receptor-mediated inhibition rescues functional and neuromorphological deficits in a mouse model of down syndrome. J Neurosci 33:3953- 3966. CrossRef Medline
48. Mortensen M, Smart TG (2006) Extrasynaptic αβ subunit GABAA receptors on rat hippocampal pyramidal neurons. J Physiol 577:841- 856. CrossRef Medline
49. Mortensen M, Smart TG (2007) Single-channel recording of ligand-gated ion channels. Nat Protoc 2:2826 -2841. CrossRef Medline
50. Mortensen M, Frølund B, Jørgensen AT, Liljefors T, Krogsgaard-Larsen P, Ebert B (2002) Activity of novel 4-PIOL analogues at human α1β2γ2S GABAA receptors- correlation with hydrophobicity. Eur J Pharmacol 451: 125-132. CrossRef Medline
51. Mortensen M, Kristiansen U, Ebert B, Frølund B, Krogsgaard-Larsen P, Smart TG (2004) Activation of single heteromeric GABAA receptor ion channels by full and partial agonists. J Physiol 557:389-413. CrossRef Medline
52. Mortensen M, Ebert B, Wafford K, Smart TG (2010) Distinct activities of GABA agonists at synaptic- and extrasynaptic-type GABAA receptors. J Physiol 588:1251-1268. CrossRef Medline
53. Mortensen M, Patel B, SmartTG (2011) GABApotency atGABAA receptors found in synaptic and extrasynaptic zones. Front Cell Neurosci 6:1. CrossRef Medline
54. Nani F, Bright DP, Revilla-Sanchez R, Tretter V, Moss SJ, Smart TG (2013) Tyrosine phosphorylation of GABAA receptor γ2-subunit regulates tonic and phasic inhibition in the thalamus. J Neurosci 33:12718 -12727. CrossRef Medline
55. Navarro JF, Burón E, Martín-López M (2002) Anxiogenic-like activity of L-655,708, a selective ligand for the benzodiazepine site of GABAA receptors which contain the α5 subunit, in the elevated plus-maze test. Prog Neuropsychopharmacol Biol Psychiatry 26:1389 -1392. CrossRef Medline
56. Nusser Z, Sieghart W, Somogyi P (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 18:1693-1703. Medline
57. Pritchett DB, Sontheimer H, Shivers BD, Ymer S, Kettenmann H, Schofield PR, Seeburg PH (1989) Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology. Nature 338:582-585. CrossRef Medline
58. Richerson GB, Wu Y (2003) Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J Neurophysiol 90:1363- 1374. CrossRef
59. Medline Rudolph U, MöhlerH (2014) GABAA receptor subtypes: therapeutic potential in Down syndrome, affective disorders, schizophrenia, and autism. Annu Rev Pharmacol Toxicol 54:483-507. CrossRef Medline
60. SmartTG (2015) GABAA receptors. In: Handbook of ion channels (Zheng J, Trudeau MC, eds), pp 345-359. Boca Raton, FL: CRC.
61. Soltesz I, Roberts JD, Takagi H, Richards JG, Mohler H, Somogyi P (1990) Synaptic and nonsynaptic localization of benzodiazepine/GABAA receptor/ Cl- channel complex using monoclonal antibodies in the dorsal lateral geniculate nucleus of the cat. Eur J Neurosci 2:414-429. CrossRef Medline
62. Somogyi P, Fritschy JM, Benke D, Roberts JD, Sieghart W (1996) The γ2 subunit of the GABAA receptor is concentrated in synaptic junctions containing the α1 and β2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacology 35:1425-1444. CrossRef Medline
63. Stórustovu SI, Ebert B (2006) Pharmacological characterization of agonists at δ-containing GABAA receptors: functional selectivity for extrasynaptic receptors is dependent on the absence of γ2. J Pharmacol Exp Ther 316: 1351-1359. CrossRef Medline
64. Thomas P, Mortensen M, Hosie AM, SmartTG (2005) Dynamic mobility of functional GABAA receptors at inhibitory synapses. Nat Neurosci 8:889- 897. CrossRef Medline
65. Ueno S, Bracamontes J, Zorumski C, Weiss DS, Steinbach JH (1997) Bicuculline and gabazine are allosteric inhibitors of channel opening of the GABAA receptor. J Neurosci 17:625- 634. Medline
66. Wafford KA, van Niel MB, Ma QP, Horridge E, Herd MB, Peden DR, Belelli D, Lambert JJ (2009) Novel compounds selectively enhance δ subunit containing GABAA receptors and increase tonic currents in thalamus. Neuropharmacology 56:182-189. CrossRef Medline
67. Whissell PD, Lecker I, Wang DS, Yu J, Orser BA (2015) Altered expression of δ GABAA receptors in health and disease. Neuropharmacology 88:24- 35. CrossRef Medline
68. Wlodarczyk AI, Sylantyev S, Herd MB, Kersanté F, Lambert JJ, Rusakov DA, Linthorst AC, Semyanov A, Belelli D, Pavlov I, Walker MC (2013) GABA-independent GABAA receptor openings maintain tonic currents. J Neurosci 33:3905-3914. CrossRef Medline
69. Wooltorton JR, Moss SJ, Smart TG (1997) Pharmacological and physiological characterization of murine homomeric β3 GABAA receptors. Eur J Neurosci 9:2225-2235. CrossRef Medline
70. Wu Y, Wang W, Díez-Sampedro A, Richerson GB (2007) Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56:851- 865. CrossRef Medline
71. Wu Z, Guo Z, Gearing M, Chen G (2014) Tonic inhibition in dentate gyrus impairs long-term potentiation and memory in an Alzheimer's disease model. Nat Commun 5:4159. CrossRef Medline
72. Ye Z, McGee TP, Houston CM, Brickley SG (2013) The contribution of δ subunit-containing GABAA receptors to phasic and tonic conductance changes in cerebellum, thalamus and neocortex. Front Neural Circuits 7:203. CrossRef Medline