Glutamate transporter studies reveal the pruning of metabotropic glutamate receptors and absence of AMPA receptor desensitization at mature calyx of Held synapses

Journal of Neuroscience

Volumn 25, Issue 37, 2005, Pages 8482-8497

  Renden, Robert ^a   Taschenberger, Holger ^b   Puente, Nagore ^c,d   Rusakov, Dmitri A ^e   Duvoisin, Robert ^a   Wang, Lu Yang ^f,g   Lehre, Knut P ^c   Von Gersdorff, Henrique ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c UNIVERSITY OF OSLO   (Norway)

^d UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

^g UNIVERSITY OF TORONTO   (Canada)

Author keywords

DGG; AMPA and NMDA receptors; Auditory brainstem; Desensitization; Development; Diffusion modeling; Glutamate transporters; Group II mGluR; mGluR8; MNTB; TBOA

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; AMPA RECEPTOR; GAMMA DEXTRO GLUTAMYLGLYCINE; GLUTAMATE RECEPTOR; GLUTAMATE TRANSPORTER; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY BRAIN STEM IMPLANT; CALYX OF HELD SYNAPSE; CELL MATURATION; CONTROLLED STUDY; DESENSITIZATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; RECEPTOR DENSITY; RECEPTOR DOWN REGULATION; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; MICE; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES;

EID: 24944568133     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1848-05.2005     Document Type: Article

References (95)

1. Awatramani GB, Turecek R, Trussell LO (2004) Inhibitory control at a synaptic relay. J Neurosci 24:2643-2647.
2. Barnes-Davies M, Forsythe ID (1995) Pre- and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices. J Physiol (Lond) 488:387-406.
3. Bean BP (1989) Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature 340:153-156.
4. Bergles DE, Diamond JS, Jahr CE (1999) Clearance of glutamate inside the synapse and beyond. Curr Opin Neurobiol 9:293-298.
5. Billups B, Graham B, Wong A, Forsythe ID (2005) Unmasking group III metabotropic glutamate autoreceptor function at excitatory synapses. J Physiol (Lond) 565:885-896.
6. Blatchley BJ, Cooper WA, Coleman JR (1987) Development of auditory brainstem response to tone pip stimuli in the rat. Brain Res Dev Brain Res 32:75-84.
7. Borst JG, Sakmann B (1996) Calcium influx and transmitter release in a fast CNS synapse. Nature 383:431-434.
8. Borst JG, Sakmann B (1998) Facilitation of presynaptic calcium currents in the rat brainstem. J Physiol (Lond) 513:149-155.
9. Brasnjo G, Otis TS (2001) Neuronal glutamate transporters control activation of postsynaptic metabotropic glutamate receptors and influence cerebellar long-term depression. Neuron 31:607-616.
10. Breakwell NA, Huang L-Q, Rowan MJ, Anwyl R (1997) DCG-IV inhibits synaptic transmission by activation of NMDA receptors in area CA1 of rat hippocampus. Eur J Pharmacol 322:173-178.
11. Brenowitz S, Trussell LO (2001) Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus. J Neurosci 21:9487-9498.
12. Cartmell J, Schoepp DD (2000) Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 75:889-907.
13. Chen CY, Ling E, Horowitz JM, Bonham AC (2002) Synaptic transmission in nucleus tractus solitarius is depressed by Group II and III but not Group I presynaptic metabotropic glutamate receptors in rats. J Physiol (Lond) 538:773-786.
14. Chuhma N, Ohmori H (1998) Postnatal development of phase-locked high-fidelity synaptic transmission in the medial nucleus of the trapezoid body of the rat. J Neurosci 18:512-520.
15. Dehnes Y, Chaudhry FA, Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC (1998) The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J Neurosci 18:3606-3619.
16. Diamond JS (2005) Deriving the glutamate clearance time course from transporter currents in CA1 hippocampal astrocytes: transmitter uptake gets faster during development. J Neurosci 25:2906-2916.
17. DiGregorio DA, Nusser Z, Silver RA (2002) Spillover of glutamate onto synaptic AMPA receptors enhances fast transmission at a cerebellar synapse. Neuron 35:521-533.
18. Duvoisin RM, Zhang C, Ramonell K (1995) A novel metabotropic glutamate receptor expressed in the retina and olfactory bulb. J Neurosci 15:3075-3083.
19. Elezgarai I, Benitez R, Mateos JM, Lazaro E, Osorio A, Azkue JJ, Bilbao A, Lingenhoehl K, Van Der Putten H, Hampson DR, Kuhn R, Knopfel T, Grandes P (1999) Developmental expression of the group III metabotropic glutamate receptor mGluR4a in the medial nucleus of the trapezoid body of the rat. J Comp Neurol 411:431-440.
20. Elezgarai I, Bilbao A, Mateos JM, Azkue JJ, Benitez R, Osorio A, Diez J, Puente N, Donate-Oliver F, Grandes P (2001) Group II metabotropic glutamate receptors are differentially expressed in the medial nucleus of the trapezoid body in the developing and adult rat. Neuroscience 104:487-498.
21. Gillis KD (1995) Techniques for membrane capacitance measurements. In: Single channel recording (Sakmann B, Neher E, eds), pp 155-198. New York: Plenum.
22. Guinan Jr JJ, Li RY (1990) Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat. Hear Res 49:321-334.
23. Haugeto O, Ullensvang K, Levy LM, Chaudhry FA, Honore T, Nielsen M, Lehre KP, Danbolt NC (1996) Brain glutamate transporter proteins form homomultimers. J Biol Chem 271:27715-27722.
24. Hefft S, Kraushaar U, Geiger JR, Jonas P (2002) Presynaptic short-term depression is maintained during regulation of transmitter release at a GABAergic synapse in rat hippocampus. J Physiol (Lond) 539:201-208.
25. Hestrin S, Sah P, Nicoll RA (1990) Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5:247-253.
26. Howson PA, Jane DE (2003) Actions of LY341495 on metabotropic glutamate receptor-mediated responses in the neonatal rat spinal cord. Br J Pharmacol 139:147-155.
27. Huang YH, Bergles DE (2004) Glutamate transporters bring competition to the synapse. Curr Opin Neurobiol 14:346-352.
28. B receptor-mediated modulation of presynaptic currents and excitatory transmission at a fast central synapse. J Neurophysiol 80:1571-1576.
29. Isaacson JS, Nicoll RA (1993) The uptake inhibitor L-trans-PDC enhances responses to glutamate but fails to alter the kinetics of excitatory synaptic currents in the hippocampus. J Neurophysiol 70:2187-2191.
30. Isaacson JS, Walmsley B (1996) Amplitude and time course of spontaneous and evoked excitatory postsynaptic currents in bushy cells of the anteroventral cochlear nucleus. J Neurophysiol 76:1566-1571.
31. Iwasaki S, Takahashi T (2001) Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem. J Physiol (Lond) 534:861-871.
32. Joshi I, Wang LY (2002) Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem. J Physiol (Lond) 540:861-873.
33. Joshi I, Shokralla S, Titis P, Wang LY (2004) The role of AMPA receptor gating in the development of high-fidelity neurotransmission at the calyx of Held synapse. J Neurosci 24:183-196.
34. Kajikawa Y, Saitoh N, Takahashi T (2001) GTP-binding protein beta gamma subunits mediate presynaptic calcium current inhibition by GABA(B) receptor. Proc Natl Acad Sci USA 98:8054-8058.
35. Kandler K, Friauf E (1993) Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol 328:161-184.
36. Kimura M, Saitoh N, Takahashi T (2003) Adenosine A(1) receptor-mediated presynaptic inhibition at the calyx of Held of immature rats. J Physiol (Lond) 553:415-426.
37. Kingston AE, Ornstein PL, Wright RA, Johnson BG, Mayne NG, Burnett JP, Belagaje R, Wu S, Schoepp DD (1998) LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37:1-12.
38. Kinney GA, Overstreet LS, Slater NT (1997) Prolonged physiological entrapment of glutamate in the synaptic cleft of cerebellar unipolar brush cells. J Neurophysiol 78:1320-1333.
39. Kinoshita A, Ohishi H, Neki A, Nomura S, Shigemoto R, Takada M, Nakanishi S, Mizuno N (1996) Presynaptic localization of a metabotropic glutamate receptor, mGluR8, in the rhinencephalic areas: a light and electron microscope study in the rat. Neurosci Lett 207:61-64.
40. Kinoshita A, Shigemoto R, Ohishi H, van der Putten H, Mizuno N (1998) Immunohistochemical localization of metabotropic glutamate receptors, mGluR7a and mGluR7b, in the central nervous system of the adult rat and mouse: a light and electron microscopic study. J Comp Neurol 393:332-352.
41. Koike-Tani M, Saitoh N, Takahashi T (2005) Mechanisms underlying developmental speeding in AMPA-EPSC decay time at the calyx of Held. J Neurosci 25:199-207.
42. Kugler P, Schleyer V (2004) Developmental expression of glutamate transporters and glutamate dehydrogenase in astrocytes of the postnatal rat hippocampus. Hippocampus 14:975-985.
43. 2+ currents by endocannabinoids released via postsynaptic mGluR activation at a calyx synapse. J Neurosci 24:5955-5965.
44. Leão RM, von Gersdorff H (2002) Noradrenaline increases high-frequency firing at the calyx of Held synapse during development by inhibiting glutamate release. J Neurophysiol 87:2297-2306.
45. + channels: locus, development, and recovery from inactivation at a high-fidelity synapse. J Neurosci 25:3724-3738.
46. Lehre KP, Danbolt NC (1998) The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 18:8751-8757.
47. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC (1995) Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J Neurosci 15:1835-1853.
48. Losonczy A, Somogyi P, Nusser Z (2003) Reduction of excitatory postsynaptic responses by persistently active metabotropic glutamate receptors in the hippocampus. J Neurophysiol 89:1910-1919.
49. Mateos JM, Elezgarai I, Benitez R, Osorio A, Bilbao A, Azkue JJ, Kuhn R, Knopfel T, Grandes P (1999) Clustering of the group III metabotropic glutamate receptor 4a at parallel fiber synaptic terminals in the rat cerebellar molecular layer. Neurosci Res 35:71-74.
50. Oertel D (1999) The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61:496-519.
51. Oliet SH, Piet R, Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292:923-926.
52. Otis TS, Wu YC, Trussell LO (1996a) Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J Neurosci 16:1634-1644.
53. Otis T, Zhang S, Trussell LO (1996b) Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J Neurosci 16:7496-7504.
54. Overstreet LS, Kinney GA, Liu YB, Billups D, Slater NT (1999) Glutamate transporters contribute to the time course of synaptic transmission in cerebellar granule cells. J Neurosci 19:9663-9673.
55. Palhalmi J, Paulsen O, Freund TF, Hajos N (2004) Distinct properties of carbachol- and DHPG-induced network oscillations in hippocampal slices. Neuropharmacology 47:381-389.
56. Palmer MJ, Taschenberger H, Hull C, Tremere L, von Gersdorff H (2003) Synaptic activation of presynaptic glutamate transporter currents in nerve terminals. J Neurosci 23:4831-4841.
57. Rossi DJ, Alford S, Mugnaini E, Slater NT (1995) Properties of transmission at a giant glutamatergic synapse in cerebellum: the mossy fiber-unipolar brush cell synapse. J Neurophysiol 74:24-42.
58. 2+ depletion. Biophys J 81:1947-1959.
59. Rusakov DA, Kullmann DM (1998) A tortuous and viscous route to understanding diffusion in the brain. Trends Neurosci 21:469-470.
60. Rusakov DA, Lehre KP (2002) Perisynaptic asymmetry of glia: new insights into glutamate signalling. Trends Neurosci 25:492-494.
61. Sakaba T, Neher E (2003) Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature 424:775-778.
62. Sarantis M, Ballerini L, Miller B, Silver RA, Edwards M, Attwell D (1993) Glutamate uptake from the synaptic cleft does not shape the decay of the non-NMDA component of the synaptic current. Neuron 11:541-549.
63. Satzler K, Sohl LF, Bollmann JH, Borst JG, Frotscher M, Sakmann B, Lubke JH (2002) Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci 22:10567-10579.
64. Saugstad JA, Kinzie JM, Shinohara MM, Segerson TP, Westbrook GL (1997) Cloning and expression of rat metabotropic glutamate receptor 8 reveals a distinct pharmacological profile. Mol Pharmacol 51:119-125.
65. Scanziani M (2002) Competing on the edge. Trends Neurosci 25:282-283.
66. Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA (1997) Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385:630-634.
67. Scheuss V, Schneggenburger R, Neher E (2002) Separation of presynaptic and postsynaptic contributions to depression by covariance analysis of successive EPSCs at the calyx of Held synapse. J Neurosci 22:728-739.
68. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23:399-409.
69. Schneggenburger R, Sakaba T, Neher E (2002) Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25:206-212.
70. Schoepp DD, Jane DE, Monn JA (1999) Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38:1431-1476.
71. Selkirk JV, Naeve GS, Foster AC (2003) Blockade of excitatory amino acid transporters in the rat hippocampus results in enhanced activation of group I and group III metabotropic glutamate receptors. Neuropharmacology 45:885-894.
72. Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, Yumoto N, Nakajima T (1998) DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol Pharmacol 53:195-201.
73. Shimamoto K, Sakai R, Takaoka K, Yumoto N, Nakajima T, Amara SG, Shigeri Y (2004) Characterization of novel L-threo-beta-benzyloxy-aspartate derivatives, potent blockers of the glutamate transporters. Mol Pharmacol 65:1008-1015.
74. Silver RA, Cull-Candy SG, Takahashi T (1996) Non-NMDA glutamate receptor occupancy and open probability at a rat cerebellar synapse with single and multiple release sites. J Physiol (Lond) 494:231-250.
75. Sun JY, Wu LG (2001) Fast kinetics of exocytosis revealed by simultaneous measurements of presynaptic capacitance and postsynaptic currents at a central synapse. Neuron 30:171-182.
76. Takahashi T, Forsythe ID, Tsujimoto T, Barnes-Davies M, Onodera K (1996) Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 274:594-597.
77. B receptor. J Neurosci 18:3138-3146.
78. Takayasu Y, Iino M, Ozawa S (2004) Roles of glutamate transporters in shaping excitatory synaptic currents in cerebellar Purkinje cells. Eur J Neurosci 19:1285-1295.
79. Taschenberger H, von Gersdorff H (2000) Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20:9162-9173.
80. Taschenberger H, von Gersdorff H (2001) Mechanisms of EPSC reduction after glutamate uptake blockade at the calyx of Held synapse. Soc Neurosci Abstr 27:607.18.
81. Taschenberger H, Leão RM, Rowland KC, Spirou GA, von Gersdorff H (2002) Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36:1127-1143.
82. Thomas NK, Wright RA, Howson PA, Kingston AE, Schoepp DD, Jane DE (2001) (S)-3,4-DCPG, a potent and selective mGlu8a receptor agonist, activates metabotropic glutamate receptors on primary afferent terminals in the neonatal rat spinal cord. Neuropharmacology 40:311-318.
83. Trussell LO, Zhang S, Raman IM (1993) Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10:1185-1196.
84. Turecek R, Trussell LO (2000) Control of synaptic depression by glutamate transporters. J Neurosci 20:2054-2063.
85. Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC (1997) Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur J Neurosci 9:1646-1655.
86. von Gersdorff H, Borst JG (2002) Short-term plasticity at the calyx of Held. Nat Rev Neurosci 3:53-64.
87. von Gersdorff H, Schneggenburger R, Weis S, Neher E (1997) Presynaptic depression at a calyx synapse: the small contribution of metabotropic glutamate receptors. J Neurosci 17:8137-8146.
88. Wada E, Shigemoto R, Kinoshita A, Ohishi H, Mizuno N (1998) Metabotropic glutamate receptor subtypes in axon terminals of projection fibers from the main and accessory olfactory bulbs: a light and electron microscopic immunohistochemical study in the rat. J Comp Neurol 393:493-504.
89. Wadiche JI, Jahr CE (2001) Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32:301-313.
90. Watabe AM, Carlisle HJ, O'Dell TJ (2002) Postsynaptic induction and presynaptic expression of group 1 mGluR-dependent LTD in the hippocampal CA1 region. J Neurophysiol 87:1395-1403.
91. Wong AY, Graham BP, Billups B, Forsythe ID (2003) Distinguishing between presynaptic and postsynaptic mechanisms of short-term depression during action potential trains. J Neurosci 23:4868-4877.
92. Wu SH, Kelly JB (1993) Response of neurons in the lateral superior olive and medial nucleus of the trapezoid body to repetitive stimulation: intracellular and extracellular recordings from mouse brain slice. Hear Res 68:189-201.
93. Xu J, Wu LG (2005) The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 46:633-645.
94. Yamashita T, Hige T, Takahashi T (2005) Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 307:124-127.
95. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.