 |
||||
|
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, April 15, 1998, 18(8):2856-2870
A Reluctant Gating Mode of Glycine Receptor Channels Determines the Time Course of Inhibitory Miniature Synaptic Events in Zebrafish Hindbrain Neurons
Pascal Legendre Institut des Neurosciences, Université Pierre et Marie Curie, 75252 Paris Cedex 05, France
Miniature IPSCs (mIPSCs) recorded in the Mauthner (M)-cell of zebrafish larvae have a broad amplitude distribution that is attributable only partly to the functional heterogeneity of postsynaptic glycine receptors (GlyRs). The role of the kinetic properties of GlyRs in amplitude fluctuation was investigated using fast-flow application techniques on outside-out patches. Short applications of a saturating glycine concentration evoked outside-out currents with a biphasic deactivation phase as observed for mIPSCs, and they were consistent with a rapid clearance of glycine from the synaptic cleft. Patch currents declined slowly during continuous applications of 3 mM glycine, but the biphasic deactivation phase of mIPSCs cannot reflect a desensitization process because paired-pulse desensitization was not observed. The maximum open probability (Po) of GlyRs was close to 0.9 with 3 mM glycine. Analyses of the onset of outside-out currents evoked by 0.1 mM glycine are consistent with the presence of two equivalent binding sites with a Kd of O.3-O.4 mM. Activation and deactivation properties of GlyRs were better described with a kinetic model, including two binding states, a doubly liganded open state, and a reluctant gating mode leading to another open state. The 20-80% rise time of mIPSCs was independent of their amplitude and is identical to that of outside-out currents evoked by the applications of a saturating concentration of glycine (>1 mM). These results support the hypothesis that GlyR kinetics determines the time course of synaptic events at M-cell inhibitory synapses and that large mIPSC amplitude fluctuations are mainly of postsynaptic origin.
Key words: glycine receptors; reluctant gating mode; zebrafish larva; miniature inhibitory synaptic currents; Mauthner cell; glycinergic synapses; channel kinetics
Copyright © 1998 Society for Neuroscience 0270-6474/98/1882856-15$05.00/0
This article has been cited by other articles:
D. Rayes, M. J. De Rosa, S. M. Sine, and C. Bouzat
Number and Locations of Agonist Binding Sites Required to Activate Homomeric Cys-Loop Receptors
J. Neurosci., May 6, 2009; 29(18): 6022 - 6032.
[Abstract] [Full Text] [PDF]
S. A. Patten and D. W. Ali
AMPA receptors associated with zebrafish Mauthner cells switch subunits during development
J. Physiol., June 15, 2007; 581(3): 1043 - 1056.
[Abstract] [Full Text] [PDF]
D.-S. Wang, R. Buckinx, H. Lecorronc, J.-M. Mangin, J.-M. Rigo, and P. Legendre
Mechanisms for Picrotoxinin and Picrotin Blocks of {alpha}2 Homomeric Glycine Receptors
J. Biol. Chem., June 1, 2007; 282(22): 16016 - 16035.
[Abstract] [Full Text] [PDF]
M. L. Veruki, S. B. Gill, and E. Hartveit
Spontaneous IPSCs and glycine receptors with slow kinetics in wide-field amacrine cells in the mature rat retina
J. Physiol., May 15, 2007; 581(1): 203 - 219.
[Abstract] [Full Text] [PDF]
S. B. Gill, M. L. Veruki, and E. Hartveit
Functional properties of spontaneous IPSCs and glycine receptors in rod amacrine (AII) cells in the rat retina
J. Physiol., September 15, 2006; 575(3): 739 - 759.
[Abstract] [Full Text] [PDF]
E. D. Eggers and P. D. Lukasiewicz
Receptor and transmitter release properties set the time course of retinal inhibition.
J. Neurosci., September 13, 2006; 26(37): 9413 - 9425.
[Abstract] [Full Text] [PDF]
E. Hartveit and M. L. Veruki
Studying properties of neurotransmitter receptors by non-stationary noise analysis of spontaneous synaptic currents
J. Physiol., August 1, 2006; 574(3): 751 - 785.
[Abstract] [Full Text] [PDF]
D.-S. Wang, J.-M. Mangin, G. Moonen, J.-M. Rigo, and P. Legendre
Mechanisms for Picrotoxin Block of {alpha}2 Homomeric Glycine Receptors
J. Biol. Chem., February 17, 2006; 281(7): 3841 - 3855.
[Abstract] [Full Text] [PDF]
A. K Magnusson, C. Kapfer, B. Grothe, and U. Koch
Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset
J. Physiol., October 15, 2005; 568(2): 497 - 512.
[Abstract] [Full Text] [PDF]
N. Lozovaya, N. Yatsenko, A. Beketov, T. Tsintsadze, and N. Burnashev
Glycine Receptors in CNS Neurons as a Target for Nonretrograde Action of Cannabinoids
J. Neurosci., August 17, 2005; 25(33): 7499 - 7506.
[Abstract] [Full Text] [PDF]
V. Burzomato, M. Beato, P. J. Groot-Kormelink, D. Colquhoun, and L. G. Sivilotti
Single-Channel Behavior of Heteromeric {alpha}1{beta} Glycine Receptors: An Attempt to Detect a Conformational Change before the Channel Opens
J. Neurosci., December 1, 2004; 24(48): 10924 - 10940.
[Abstract] [Full Text] [PDF]
J. W. Lynch
Molecular Structure and Function of the Glycine Receptor Chloride Channel
Physiol Rev, October 1, 2004; 84(4): 1051 - 1095.
[Abstract] [Full Text] [PDF]
E. D. Eggers and A. J. Berger
Mechanisms for the Modulation of Native Glycine Receptor Channels by Ethanol
J Neurophysiol, June 1, 2004; 91(6): 2685 - 2695.
[Abstract] [Full Text] [PDF]
G. B. Awatramani, R. Turecek, and L. O. Trussell
Inhibitory Control at a Synaptic Relay
J. Neurosci., March 17, 2004; 24(11): 2643 - 2647.
[Abstract] [Full Text] [PDF]
M. Beato, P. J. Groot-Kormelink, D. Colquhoun, and L. G. Sivilotti
The Activation Mechanism of {alpha}1 Homomeric Glycine Receptors
J. Neurosci., January 28, 2004; 24(4): 895 - 906.
[Abstract] [Full Text] [PDF]
J.-M. Rigo, C. I. Badiu, and P. Legendre
Heterogeneity of postsynaptic receptor occupancy fluctuations among glycinergic inhibitory synapses in the zebrafish hindbrain
J. Physiol., December 15, 2003; 553(3): 819 - 832.
[Abstract] [Full Text] [PDF]
J M Mangin, M Baloul, L Prado de Carvalho, B Rogister, J M Rigo, and P Legendre
Kinetic properties of the {alpha}2 homo-oligomeric glycine receptor impairs a proper synaptic functioning
J. Physiol., December 1, 2003; 553(2): 369 - 386.
[Abstract] [Full Text] [PDF]
L. L. Thio, A. Shanmugam, K. Isenberg, and K. Yamada
Benzodiazepines Block {alpha}2-Containing Inhibitory Glycine Receptors in Embryonic Mouse Hippocampal Neurons
J Neurophysiol, July 1, 2003; 90(1): 89 - 99.
[Abstract] [Full Text] [PDF]
T. M Lewis, P. R Schofield, and A. M L McClellan
Kinetic determinants of agonist action at the recombinant human glycine receptor
J. Physiol., June 1, 2003; 549(2): 361 - 374.
[Abstract] [Full Text] [PDF]
L. J Gentet and J. D Clements
Binding site stoichiometry and the effects of phosphorylation on human {alpha}1 homomeric glycine receptors
J. Physiol., October 1, 2002; 544(1): 97 - 106.
[Abstract] [Full Text] [PDF]
P. Legendre, E. Muller, C. I. Badiu, J. Meier, C. Vannier, and A. Triller
Desensitization of Homomeric alpha 1 Glycine Receptor Increases with Receptor Density
Mol. Pharmacol., October 1, 2002; 62(4): 817 - 827.
[Abstract] [Full Text] [PDF]
M. Beato, P. J. Groot-Kormelink, D. Colquhoun, and L. G. Sivilotti
Openings of the Rat Recombinant {alpha}1 Homomeric Glycine Receptor as a Function of the Number of Agonist Molecules Bound
J. Gen. Physiol., April 29, 2002; 119(5): 443 - 466.
[Abstract] [Full Text] [PDF]
V. B Caraiscos, S J. Mihic, J. F MacDonald, and B. A Orser
Tyrosine kinases enhance the function of glycine receptors in rat hippocampal neurons and human {alpha}1{beta} glycine receptors
J. Physiol., March 1, 2002; 539(2): 495 - 502.
[Abstract] [Full Text] [PDF]
P. Drapeau, R. R. Buss, D. W. Ali, P. Legendre, and R. L. Rotundo
Limits to the Development of Fast Neuromuscular Transmission in Zebrafish
J Neurophysiol, December 1, 2001; 86(6): 2951 - 2956.
[Abstract] [Full Text] [PDF]
D. D. S. Jan, B. David-Watine, H. Korn, and P. Bregestovski
Activation of human {alpha}1 and {alpha}2 homomeric glycine receptors by taurine and GABA
J. Physiol., September 15, 2001; 535(3): 741 - 755.
[Abstract] [Full Text] [PDF]
D. D Mott, K. Erreger, T. G Banke, and S. F Traynelis
Open probability of homomeric murine 5-HT3A serotonin receptors depends on subunit occupancy
J. Physiol., September 1, 2001; 535(2): 427 - 443.
[Abstract] [Full Text] [PDF]
H. Suwa, L. Saint-Amant, A. Triller, P. Drapeau, and P. Legendre
High-Affinity Zinc Potentiation of Inhibitory Postsynaptic Glycinergic Currents in the Zebrafish Hindbrain
J Neurophysiol, February 1, 2001; 85(2): 912 - 925.
[Abstract] [Full Text] [PDF]
D. W. Ali, P. Drapeau, and P. Legendre
Development of Spontaneous Glycinergic Currents in the Mauthner Neuron of the Zebrafish Embryo
J Neurophysiol, October 1, 2000; 84(4): 1726 - 1736.
[Abstract] [Full Text] [PDF]
M. I. Banks and R. A. Pearce
Kinetic Differences between Synaptic and Extrasynaptic GABAA Receptors in CA1 Pyramidal Cells
J. Neurosci., February 1, 2000; 20(3): 937 - 948.
[Abstract] [Full Text] [PDF]
P. Legendre, D. W. Ali, and P. Drapeau
Recovery from Open Channel Block by Acetylcholine during Neuromuscular Transmission in Zebrafish
J. Neurosci., January 1, 2000; 20(1): 140 - 148.
[Abstract] [Full Text] [PDF]
P. Legendre
Voltage Dependence of the Glycine Receptor-Channel Kinetics in the Zebrafish Hindbrain
J Neurophysiol, November 1, 1999; 82(5): 2120 - 2129.
[Abstract] [Full Text] [PDF]
J. H. Singer and A. J. Berger
Contribution of Single-Channel Properties to the Time Course and Amplitude Variance of Quantal Glycine Currents Recorded in Rat Motoneurons
J Neurophysiol, April 1, 1999; 81(4): 1608 - 1616.
[Abstract] [Full Text] [PDF]
J. H. Singer, E. M. Talley, D. A. Bayliss, and A. J. Berger
Development of Glycinergic Synaptic Transmission to Rat Brain Stem Motoneurons
J Neurophysiol, November 1, 1998; 80(5): 2608 - 2620.
[Abstract] [Full Text] [PDF]
M. Beato, P. J. Groot-Kormelink, D. Colquhoun, and L. G. Sivilotti
Openings of the Rat Recombinant {alpha}1 Homomeric Glycine Receptor as a Function of the Number of Agonist Molecules Bound
J. Gen. Physiol., April 29, 2002; 119(5): 443 - 466.
[Abstract] [Full Text] [PDF]
V. B. Caraiscos, S. J. Mihic, J. F. MacDonald, and B. A. Orser
Tyrosine kinases enhance the function of glycine receptors in rat hippocampal neurons and human {alpha}1{beta} glycine receptors
J. Physiol., January 25, 2002; (2002) 200101350.
[Abstract] [PDF]
|
|
|
|
 |
|