Modulation of the glycine response by Ca2+‐permeable AMPA receptors in rat spinal neurones

1 In acutely isolated rat sacral dorsal commisural nucleus (SDCN) neurones, application of kainate (KA) reversibly potentiated glycine‐evoked Cl− currents (IGly) in a concentration‐dependent manner. 2 The cellular events underlying the interaction between non‐NMDA receptors and glycine receptors were studied by using nystatin‐perforated patch and cell‐attached single‐channel recording modes. 3 The action of KA was not accompanied by a shift in the reversal potential for IGly. In dose‐response curves, KA potentiated IGly without significantly changing glycine binding affinity. 4 GYKI 52466 blocked while NS‐102 had no effect on the KA‐induced potentiation of IGly. 5 The potentiation was reduced when KA was applied in a Ca2+‐free extracellular solution or in the presence of BAPTA AM, and was independent of the activation of voltage‐dependent Ca2+ channels. 6 Pretreatment with KN‐62, a selective Ca2+‐calmodulin‐dependent protein kinase II (CaMKII) inhibitor, abolished the action of KA. Inhibition of calcineurin converted the KA‐induced potentiation to a sustained one. 7 Single‐channel recordings revealed that KA decreased the mean closing time of glycine‐gated single‐channel activity, resulting in an increase in the probability of channel opening. 8 It is proposed that Ca2+ entry through AMPA receptors modulates the glycine receptor function via coactivation of CaMKII and calcineurin in SDCN neurones. This interaction may provide a new postsynaptic mechanism for control of inhibitory synaptic signalling and represent one of the important regulatory mechanisms of spinal nociception.

[1]  N. Burnashev,et al.  Facilitation of currents through rat Ca2+‐permeable AMPA receptor channels by activity‐dependent relief from polyamine block , 1998, The Journal of physiology.

[2]  Pankaj Sah,et al.  Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala , 1998, Nature.

[3]  P. Jonas,et al.  Corelease of two fast neurotransmitters at a central synapse. , 1998, Science.

[4]  Andreas Lüthi,et al.  Modulation of AMPA receptor unitary conductance by synaptic activity , 1998, Nature.

[5]  C. Mulle,et al.  Potentiation of GABAergic synaptic transmission by AMPA receptors in mouse cerebellar stellate cells: changes during development , 1998, The Journal of physiology.

[6]  N. Akaike,et al.  5‐HT potentiation of the GABAA response in the rat sacral dorsal commissural neurones , 1998, British journal of pharmacology.

[7]  K. Yung.  Localization of glutamate receptors in dorsal horn of rat spinal cord , 1998, Neuroreport.

[8]  Tian-Le Xu,et al.  Taurine-activated chloride currents in the rat sacral dorsal commissural neurons , 1998, Brain Research.

[9]  J. Kirsch,et al.  Glycine-receptor activation is required for receptor clustering in spinal neurons , 1998, Nature.

[10]  L. Satin,et al.  Effects of intracellular calcium on GABAA receptors in mouse cortical neurons , 1998, Pflügers Archiv.

[11]  H. Higashi,et al.  128 Electrophysiology and morphology of neurons in dorsal commissural nucleus of rat sacral spinal cord , 1997, Neuroscience Research.

[12]  J. Tapia,et al.  Differential intracellular regulation of cortical GABAA and spinal glycine receptors in cultured neurons , 1997, Brain Research.

[13]  G Tocco,et al.  Glycine-induced long-term potentiation is associated with structural and functional modifications of alpha-amino-3-hydroxyl-5-methyl-4-isoxazolepropionic acid receptors. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J G Chen,et al.  Low-Frequency Stimulation of Afferent Aδ-Fibers Induces Long-Term Depression at Primary Afferent Synapses with Substantia Gelatinosa Neurons in the Rat , 1997, The Journal of Neuroscience.

[15]  N. Akaike,et al.  Protein kinase C‐mediated enhancement of glycine response in rat sacral dorsal commissural neurones by serotonin. , 1996, The Journal of physiology.

[16]  A. Macdermott,et al.  Synaptic strengthening through activation of Ca2+ -permeable AMPA receptors , 1996, Nature.

[17]  M. Randić,et al.  alpha-subunit of CaM-KII increases glycine currents in acutely isolated rat spinal neurons. , 1996, Journal of neurophysiology.

[18]  P. Legendre,et al.  Effects of nocodazole and taxol on glycine evoked currents on rat spinal cord neurones in culture , 1995, Neuroreport.

[19]  D. Storm,et al.  Ca2+ Inhibition of Type III Adenylyl Cyclase in Vivo(*) , 1995, The Journal of Biological Chemistry.

[20]  P. A. Goldstein,et al.  Variable distributions of Ca(2+)-permeable and Ca(2+)-impermeable AMPA receptors on embryonic rat dorsal horn neurons. , 1995, Journal of neurophysiology.

[21]  George G. Lunt,et al.  Evolutionary history of the ligand-gated ion-channel superfamily of receptors , 1995, Trends in Neurosciences.

[22]  R. Wong,et al.  Suppression of GABAA receptor responses by NMDA application in hippocampal neurones acutely isolated from the adult guinea‐pig. , 1995, The Journal of physiology.

[23]  R. Nicoll,et al.  A role for protein kinases and phosphatases in the Ca2+-induced enhancement of hippocampal AMPA receptor-mediated synaptic responses , 1994, Neuron.

[24]  K. Ren,et al.  A comparative study of the calcium-binding proteins calbindin-D28K, calretinin, calmodulin and parvalbumin in the rat spinal cord , 1994, Brain Research Reviews.

[25]  J. Lerma,et al.  Modulation of inhibitory glycine receptors by phosphorylation by protein kinase C and cAMP-dependent protein kinase. , 1994, The Journal of biological chemistry.

[26]  M. Randić,et al.  Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  F. Eusebi,et al.  Inhibition of GABA and glycine responses by glutamate in rat hippocampal neurons , 1993, Brain Research.

[28]  L. Vyklický,et al.  Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  D. Langosch,et al.  The 93 kDa protein gephyrin and tubulin associated with the inhibitory glycine receptor are phosphorylated by an endogenous protein kinase , 1992, FEBS letters.

[30]  T. Jessell,et al.  Amino acid‐mediated EPSPs at primary afferent synapses with substantia gelatinosa neurones in the rat spinal cord. , 1990, The Journal of physiology.

[31]  A. Takai,et al.  Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. , 1988, The Biochemical journal.

[32]  I. Forsythe,et al.  The dependence of motoneurone membrane potential on extracellular ion concentrations studied in isolated rat spinal cord. , 1988, The Journal of physiology.

[33]  B. Pomeranz,et al.  Electroacupuncture suppresses a nociceptive reflex: naltrexone prevents but does not reverse this effect , 1988, Brain Research.

[34]  B. Sakmann,et al.  Mechanism of anion permeation through channels gated by glycine and gamma‐aminobutyric acid in mouse cultured spinal neurones. , 1987, The Journal of physiology.

[35]  T. Yakushiji,et al.  Intracellular calcium ions decrease the affinity of the GABA receptor , 1986, Nature.

[36]  P. Greengard,et al.  Regional distribution of calcium- and cyclic adenosine 3':5'- monophosphate-regulated protein phosphorylation systems in mammalian brain. II. Soluble systems , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  P. Greengard,et al.  Regional distribution of calcium- and cyclic adenosine 3':5'- monophosphate-regulated protein phosphorylation systems in mammalian brain. I. Particulate systems , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  P. Wall,et al.  Pain mechanisms: a new theory. , 1965, Science.

[39]  Richard F. Thompson,et al.  Glycine-induced long-term potentiation is associated with structural and functional modifications of a-amino-3-hydroxyl-5- methyl-4-isoxazolepropionic acid receptors (hippocampusyplasticityycalpainyglutamateyspectrin) , 1997 .

[40]  H. Schulman,et al.  The multifunctional calcium/calmodulin-dependent protein kinase: from form to function. , 1995, Annual review of physiology.

[41]  S. Nishi,et al.  Primary afferent‐evoked glycine‐ and GABA‐mediated IPSPs in substantia gelatinosa neurones in the rat spinal cord in vitro. , 1995, The Journal of physiology.

[42]  A. Larson,et al.  Antinociceptive effects of intrathecal taurine and calcium in the mouse. , 1992, Life sciences.

[43]  A. Stelzer,et al.  Intracellular regulation of GABAA-receptor function. , 1992, Ion channels.