A reinforcing circuit action of extrasynaptic GABAA receptor modulators on cerebellar granule cell inhibition

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Santhakumar, Vijayalakshmi ^a,b   Meera, Pratap ^a   Karakossian, Movses H ^a   Otis, Thomas S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID A RECEPTOR DELTA; ALCOHOL; GABOXADOL; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; AMINO ACID RECEPTOR BLOCKING AGENT; GLUTAMATE RECEPTOR; GLUTAMIC ACID DERIVATIVE; ISOXAZOLE DERIVATIVE; PROTEIN SUBUNIT;

4 AMINOBUTYRIC ACID RELEASE; ADULT; ALLELE; ANIMAL CELL; ARTICLE; CEREBELLUM GRANULAR LAYER; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GABAERGIC SYSTEM; GOLGI COMPLEX; GRANULE CELL; HOMOZYGOSITY; KNOCKOUT MOUSE; MOUSE; NEUROMODULATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SPONTANEOUS EXCITATORY POSTSYNAPTIC CURRENT; SPONTANEOUS INHIBITORY POSTSYNAPTIC CURRENT; ACTION POTENTIAL; ANIMAL; C57BL MOUSE; CEREBELLUM; CHANNEL GATING; CYTOLOGY; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; METABOLISM; NERVE CELL; NERVE CELL INHIBITION; PROTEIN SUBUNIT; SPRAGUE DAWLEY RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

MUS; RATTUS;

ACTION POTENTIALS; ANIMALS; CEREBELLUM; ETHANOL; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA-A RECEPTOR AGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATES; INHIBITORY POSTSYNAPTIC POTENTIALS; ION CHANNEL GATING; ISOXAZOLES; MICE, INBRED C57BL; NEURAL INHIBITION; NEURONS; PROTEIN SUBUNITS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RECEPTORS, GLUTAMATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84894105979     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072976     Document Type: Article

References (70)

1. Brickley SG, Mody I (2012) Extrasynaptic GABA(A) receptors: their function in the CNS and implications for disease. Neuron 73: 23-34
2. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6: 215-229
3. Chadderton P, Margrie TW, Hausser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428: 856-860
4. Houston CM, McGee TP, Mackenzie G, Troyano-Cuturi K, Rodriguez PM, et al. (2012) Are extrasynaptic GABAA receptors important targets for sedative/ hypnotic drugs? The Journal of neuroscience : the official journal of the Society for Neuroscience 32: 3887-3897
5. Stell BM, Brickley SG, Tang CY, 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 U S A 100: 14439-14444
6. Mihalek RM, Banerjee PK, Korpi ER, Quinlan JJ, Firestone LL, et al. (1999) Attenuated sensitivity to neuroactive steroids in gamma-aminobutyrate type A receptor delta subunit knockout mice. Proc Natl Acad Sci U S A 96: 12905-12910
7. Chisari M, Eisenman LN, Covey DF, Mennerick S, Zorumski CF (2010) The sticky issue of neurosteroids and GABA(A) receptors. Trends in neurosciences 33: 299-306
8. Bai D, Zhu G, Pennefather P, Jackson MF, MacDonald JF, et al. (2001) Distinct functional and pharmacological properties of tonic and quantal inhibitory postsynaptic currents mediated by gamma-aminobutyric acid(A) receptors in hippocampal neurons. Molecular pharmacology 59: 814-824
9. Jia F, Yue M, Chandra D, Homanics GE, Goldstein PA, et al. (2008) Isoflurane is a potent modulator of extrasynaptic GABA(A) receptors in the thalamus. The Journal of pharmacology and experimental therapeutics 324: 1127-1135
10. Meera P, Wallner M, Otis TS (2011) Molecular basis for the high THIP/ gaboxadol sensitivity of extrasynaptic GABA(A) receptors. Journal of Neurophysiology 106: 2057-2064
11. 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. BrJPharmacol 136: 965-974
12. Drasbek KR, Hoestgaard-Jensen K, Jensen K (2007) Modulation of extrasynaptic THIP conductances by GABAA-receptor modulators in mouse neocortex. Journal of Neurophysiology 97: 2293-2300
13. Walsh JK, Mayleben D, Guico-Pabia C, Vandormael K, Martinez R, et al. (2008) Efficacy of the selective extrasynaptic GABA A agonist, gaboxadol, in a model of transient insomnia: a randomized, controlled clinical trial. Sleep medicine 9: 393-402
14. Santhakumar V, Wallner M, Otis TS (2007) Ethanol acts directly on extrasynaptic subtypes of GABAA receptors to increase tonic inhibition. Alcohol 41: 211-221
15. Carta M, Mameli M, Valenzuela CF (2004) Alcohol enhances GABAergic transmission to cerebellar granule cells via an increase in Golgi cell excitability. J Neurosci 24: 3746-3751
16. Glykys J, Peng Z, Chandra D, Homanics GE, Houser CR, et al. (2007) A new naturally occurring GABA(A) receptor subunit partnership with high sensitivity to ethanol. NatNeurosci 10: 40-48
17. Fleming RL, Wilson WA, Swartzwelder HS (2007) Magnitude and ethanol sensitivity of tonic GABAA receptor-mediated inhibition in dentate gyrus changes from adolescence to adulthood. JNeurophysiol 97: 3806-3811
18. Hanchar HJ, Dodson PD, Olsen RW, Otis TS, Wallner M (2005) Alcoholinduced motor impairment caused by increased extrasynaptic GABA(A) receptor activity. Nat Neurosci 8: 339-345
19. Xiao C, Zhou C, Li K, Ye JH (2007) Presynaptic GABAA receptors facilitate GABAergic transmission to dopaminergic neurons in the ventral tegmental area of young rats. The Journal of Physiology 580: 731-743
20. Botta P, de Souza FM, Sangrey T, De Schutter E, Valenzuela CF (2010) Alcohol excites cerebellar Golgi cells by inhibiting the Na+/K+ ATPase. Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology 35: 1984-1996
21. Botta P, Simoes de Souza FM, Sangrey T, De Schutter E, Valenzuela CF (2012) Excitation of rat cerebellar Golgi cells by ethanol: further characterization of the mechanism. Alcoholism, clinical and experimental research 36: 616-624
22. Tretter V, Hauer B, Nusser Z, Mihalek RM, Hoger H, et al. (2001) Targeted disruption of the GABA(A) receptor delta subunit gene leads to an up-regulation of gamma 2 subunit-containing receptors in cerebellar granule cells. The Journal of biological chemistry 276: 10532-10538
23. 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
24. 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
25. Santhakumar V, Hanchar HJ, Wallner M, Olsen RW, Otis TS (2006) Contributions of the GABAA receptor alpha6 subunit to phasic and tonic inhibition revealed by a naturally occurring polymorphism in the alpha6 gene. JNeurosci 26: 3357-3364
26. Smith SL, Otis TS (2003) Persistent changes in spontaneous firing of Purkinje neurons triggered by the nitric oxide signaling cascade. J Neurosci 23: 367-372
27. Karakossian MH, Otis TS (2004) Excitation of cerebellar interneurons by Group I metabotropic glutamate receptors. J Neurophysiol
28. Gupta A, Elgammal FS, Proddutur A, Shah S, Santhakumar V (2012) Decrease in Tonic Inhibition Contributes to Increase in Dentate Semilunar Granule Cell. Journal of Neuroscience 32: 2523-2537
29. Yu J, Proddutur A, Elgammal FS, Ito T, Santhakumar V (2013) Status epilepticus enhances tonic GABA currents and depolarizes GABA reversal potential in dentate fast-spiking basket cells. J Neurophysiol
30. Santhakumar V, Jones RT, Mody I (2010) Developmental regulation and neuroprotective effects of striatal tonic GABAA currents. Neuroscience 167: 644-655
31. Dieudonne S (1998) Submillisecond kinetics and low efficacy of parallel fibre-Golgi cell synaptic currents in the rat cerebellum. The Journal of Physiology 510 ( Pt 3): 845-866
32. Palay SL, Chan-Palay V (1982) The Cerebellum : new vistas. Berlin ; New York: Springer-Verlag. xvii, 637 p. p
33. Hull C, Regehr WG (2012) Identification of an inhibitory circuit that regulates cerebellar Golgi cell activity. Neuron 73: 149-158
34. Korpi ER, Kleingoor C, Kettenmann H, Seeburg PH (1993) Benzodiazepineinduced motor impairment linked to point mutation in cerebellar GABAA receptor. Nature 361: 356-359
35. Saba L, Porcella A, Congeddu E, Colombo G, Peis M, et al. (2001) The R100Q mutation of the GABA(A) alpha(6) receptor subunit may contribute to voluntary aversion to ethanol in the sNP rat line. Brain Res Mol Brain Res 87: 263-270
36. Carr LG, Spence JP, Peter Eriksson CJ, Lumeng L, Li TK (2003) AA and ANA rats exhibit the R100Q mutation in the GABAA receptor alpha 6 subunit. Alcohol 31: 93-97
37. Brickley SG, Farrant M, Swanson GT, Cull-Candy SG (2001) CNQX increases GABA-mediated synaptic transmission in the cerebellum by an AMPA/kainate receptor-independent mechanism. Neuropharmacology 41: 730-736
38. McBain CJ, Eaton JV, Brown T, Dingledine R (1992) CNQX increases spontaneous inhibitory input to CA3 pyramidal neurones in neonatal rat hippocampal slices. Brain Res 592: 255-260
39. Menuz K, Stroud RM, Nicoll RA, Hays FA (2007) TARP auxiliary subunits switch AMPA receptor antagonists into partial agonists. Science 318: 815-817
40. Sundstrom-Poromaa I, Smith DH, Gong QH, Sabado TN, Li X, et al. (2002) Hormonally regulated alpha(4)beta(2)delta GABA(A) receptors are a target for alcohol. Nature neuroscience 5: 721-722
41. Wallner M, Hanchar HJ, Olsen RW (2006) Low-dose alcohol actions on alpha4beta3delta GABAA receptors are reversed by the behavioral alcohol antagonist Ro15-4513. Proceedings of the National Academy of Sciences of the United States of America 103: 8540-8545
42. Wallner M, Hanchar HJ, Olsen RW (2003) Ethanol enhances alpha 4 beta 3 delta and alpha 6 beta 3 delta gamma-aminobutyric acid type A receptors at low concentrations known to affect humans. Proc Natl Acad Sci U S A 100: 15218-15223
43. Hanchar HJ, Chutsrinopkun P, Meera P, Supavilai P, Sieghart W, et al. (2006) Ethanol potently and competitively inhibits binding of the alcohol antagonist Ro15-4513 to alpha4/6beta3delta GABAA receptors. Proceedings of the National Academy of Sciences of the United States of America 103: 8546-8551
44. Otis TS (2008) Comments on "Ethanol sensitivity of GABAergic currents in cerebellar granule neurons is not increased by a single amino acid change (R100Q) in the alpha6 GABA(A) receptor subunit". The Journal of pharmacology and experimental therapeutics 324: 399-400; author reply 401-393
45. Botta P, Mameli M, Floyd KL, Radcliffe RA, Valenzuela CF (2007) Ethanol sensitivity of GABAergic currents in cerebellar granule neurons is not increased by a single amino acid change (R100Q) in the alpha6 GABAA receptor subunit. The Journal of pharmacology and experimental therapeutics 323: 684-691
46. Krogsgaard-Larsen P, Johnston GA, Lodge D, Curtis DR (1977) A new class of GABA agonist. Nature 268: 53-55
47. Wall MJ, Usowicz MM (1997) Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. The European journal of neuroscience 9: 533-548
48. Eccles JC, Llinas R, Sasaki K (1966) The inhibitory interneurones within the cerebellar cortex. Experimental brain research Experimentelle Hirnforschung Experimentation cerebrale 1: 1-16
49. Brickley SG, Cull-Candy SG, 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
50. 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
51. Zhang W, Linden DJ (2012) Calcium influx measured at single presynaptic boutons of cerebellar granule cell ascending axons and parallel fibers. Cerebellum 11: 121-131
52. Stell BM (2011) Biphasic action of axonal GABA-A receptors on presynaptic calcium influx. Journal of Neurophysiology 105: 2931-2936
53. Stell BM, Rostaing P, Triller A, Marty A (2007) Activation of presynaptic GABA(A) receptors induces glutamate release from parallel fiber synapses. The Journal of neuroscience : the official journal of the Society for Neuroscience 27: 9022-9031
54. Pugh JR, Jahr CE (2011) Axonal GABAA receptors increase cerebellar granule cell excitability and synaptic activity. The Journal of neuroscience : the official journal of the Society for Neuroscience 31: 565-574
55. Dellal SS, Luo R, Otis TS (2012) GABAA receptors increase excitability and conduction velocity of cerebellar parallel fiber axons. Journal of Neurophysiology 107: 2958-2970
56. Bright DP, Renzi M, Bartram J, McGee TP, MacKenzie G, et al. (2011) Profound desensitization by ambient GABA limits activation of delta-containing GABAA receptors during spillover. The Journal of neuroscience : the official journal of the Society for Neuroscience 31: 753-763
57. Moriguchi S, Zhao X, Marszalec W, Yeh JZ, Narahashi T (2007) Effects of ethanol on excitatory and inhibitory synaptic transmission in rat cortical neurons. Alcoholism, clinical and experimental research 31: 89-99
58. Ziskind-Conhaim L, Gao BX, Hinckley C (2003) Ethanol dual modulatory actions on spontaneous postsynaptic currents in spinal motoneurons. Journal of Neurophysiology 89: 806-813
59. Valenzuela CF, Bhave S, Hoffman P, Harris RA (1998) Acute effects of ethanol on pharmacologically isolated kainate receptors in cerebellar granule neurons: comparison with NMDA and AMPA receptors. Journal of neurochemistry 71: 1777-1780
60. Schmid G, Bonanno G, Raiteri L, Sarviharju M, Korpi ER, et al. (1999) Enhanced benzodiazepine and ethanol actions on cerebellar GABA(A) receptors mediating glutamate release in an alcohol-sensitive rat line. Neuropharmacology 38: 1273-1279
61. Botta P, Radcliffe RA, Carta M, Mameli M, Daly E, et al. (2007) Modulation of GABAA receptors in cerebellar granule neurons by ethanol: a review of genetic and electrophysiological studies. Alcohol 41: 187-199
62. Jia F, Pignataro L, Harrison NL (2007) GABAA receptors in the thalamus: alpha4 subunit expression and alcohol sensitivity. Alcohol 41: 177-185
63. Wei W, Faria LC, Mody I (2004) Low ethanol concentrations selectively augment the tonic inhibition mediated by delta subunit-containing GABAA receptors in hippocampal neurons. J Neurosci 24: 8379-8382
64. Liang J, Zhang N, Cagetti E, Houser CR, Olsen RW, et al. (2006) Chronic intermittent ethanol-induced switch of ethanol actions from extrasynaptic to synaptic hippocampal GABAA receptors. The Journal of neuroscience : the official journal of the Society for Neuroscience 26: 1749-1758
65. Borghese CM, Storustovu S, Ebert B, Herd MB, Belelli D, et al. (2006) The delta subunit of gamma-aminobutyric acid type A receptors does not confer sensitivity to low concentrations of ethanol. The Journal of pharmacology and experimental therapeutics 316: 1360-1368
66. Franks NP (2008) General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nature reviews Neuroscience 9: 370-386
67. Bieda MC, MacIver MB (2004) Major role for tonic GABAA conductances in anesthetic suppression of intrinsic neuronal excitability. Journal of Neurophysiology 92: 1658-1667
68. Caraiscos VB, Newell JG, You-Ten KE, Elliott EM, Rosahl TW, et al. (2004) Selective enhancement of tonic GABAergic inhibition in murine hippocampal neurons by low concentrations of the volatile anesthetic isoflurane. The Journal of neuroscience : the official journal of the Society for Neuroscience 24: 8454-8458
69. Korpi ER, Luddens H, Seeburg PH (1992) GABAA antagonists reveal binding sites for [35S]TBPS in cerebellar granular cell layer. Eur J Pharmacol 211: 427-428
70. Korpi ER, Makela R, Romeo E, Guidotti A, Uusi-Oukari M, et al. (2001) Increased behavioral neurosteroid sensitivity in a rat line selectively bred for high alcohol sensitivity. Eur J Pharmacol 421: 31-38