Glial glutamate transporter 1 regulates the spatial and temporal coding of glutamatergic synaptic transmission in spinal lamina II neurons

Neuroscience

Volumn 149, Issue 4, 2007, Pages 898-907

  Weng, H R ^a   Chen, J H ^a   Pan, Z Z ^a   Nie, H ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

astrocyte; cyclothiazide; excitatory amino acid transporter; gamma d glutamyl glycine; nociception; pain

Indexed keywords

DIHYDROKAINIC ACID; VESICULAR GLUTAMATE TRANSPORTER 1;

ARTICLE; DESENSITIZATION; ENZYME INHIBITION; EXCITATORY POSTSYNAPTIC POTENTIAL; GLIA CELL; KINETICS; MALE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SUBSTANTIA GELATINOSA; SYNAPSE;

ANIMALS; BENZOTHIADIAZINES; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID TRANSPORTER 2; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; KAINIC ACID; MALE; NEURONS; OLIGOPEPTIDES; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SYNAPTIC TRANSMISSION;

EID: 36249003803     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.07.063     Document Type: Article

References (68)

1. Ackley M.A., Governo R.J., Cass C.E., Young J.D., Baldwin S.A., and King A.E. Control of glutamatergic neurotransmission in the rat spinal dorsal horn by the nucleoside transporter ENT1. J Physiol 548 (2003) 507-517
2. Anderson C.M., Bridges R.J., Chamberlin A.R., Shimamoto K., Yasuda-Kamatani Y., and Swanson R.A. Differing effects of substrate and non-substrate transport inhibitors on glutamate uptake reversal. J Neurochem 79 (2001) 1207-1216
3. Anderson C.M., and Swanson R.A. Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32 (2000) 1-14
4. Arriza J.L., Fairman W.A., Wadiche J.I., Murdoch G.H., Kavanaugh M.P., and Amara S.G. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J Neurosci 14 (1994) 5559-5569
5. Bellingham M.C., Lim R., and Walmsley B. Developmental changes in EPSC quantal size and quantal content at a central glutamatergic synapse in rat. J Physiol 511 (1998) 861-869
6. Binns B.C., Huang Y., Goettl V.M., Hackshaw K.V., and Stephens Jr. R.L. Glutamate uptake is attenuated in spinal deep dorsal and ventral horn in the rat spinal nerve ligation model. Brain Res 1041 (2005) 38-47
7. Bird G.C., Asghar A.U., Ackley M.A., and King A.E. Modulation of primary afferent-mediated neurotransmission and Fos expression by glutamate uptake inhibition in rat spinal neurones in vitro. Neuropharmacology 41 (2001) 582-591
8. Breukel A.I., Besselsen E., Lopes da Silva F.H., and Ghijsen W.E. A presynaptic N-methyl-D-aspartate autoreceptor in rat hippocampus modulating amino acid release from a cytoplasmic pool. Eur J Neurosci 10 (1998) 106-114
9. Campbell S.L., and Hablitz J.J. Glutamate transporters regulate excitability in local networks in rat neocortex. Neuroscience 127 (2004) 625-635
10. Clements J.D. Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci 19 (1996) 163-171
11. Danbolt N.C. Glutamate uptake. Prog Neurobiol 65 (2001) 1-105
12. Edmonds B., Gibb A.J., and Colquhoun D. Mechanisms of activation of glutamate receptors and the time course of excitatory synaptic currents. Annu Rev Physiol 57 (1995) 495-519
13. Foster K.A., Crowley J.J., and Regehr W.G. The influence of multivesicular release and postsynaptic receptor saturation on transmission at granule cell to Purkinje cell synapses. J Neurosci 25 (2005) 11655-11665
14. Furue H., Katafuchi T., and Yoshimura M. Sensory processing and functional reorganization of sensory transmission under pathological conditions in the spinal dorsal horn. Neurosci Res 48 (2004) 361-368
15. Furuta A., Rothstein J.D., and Martin L.J. Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17 (1997) 8363-8375
16. Gegelashvili G., Robinson M.B., Trotti D., and Rauen T. Regulation of glutamate transporters in health and disease. Prog Brain Res 132 (2001) 267-286
17. Gerber G., Zhong J., Youn D.-H., and Randic M. Group II and group III metabotropic glutamate receptor agonists depress synaptic transmission in the rat spinal cord dorsal horn. Neuroscience 100 (2000) 393-406
18. Haugeto O., Ullensvang K., Levy L.M., Chaudhry F.A., Honore T., Nielsen M., Lehre K.P., and Danbolt N.C. Brain glutamate transporter proteins form homomultimers. J Biol Chem 271 (1996) 27715-27722
19. Huang H., and Bordey A. Glial glutamate transporters limit spillover activation of presynaptic NMDA receptors and influence synaptic inhibition of Purkinje neurons. J Neurosci 24 (2004) 5659-5669
20. Isaacson J.S., and Nicoll R.A. 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 (1993) 2187-2191
21. Iserhot C., Gebhardt C., Schmitz D., and Heinemann U. Glutamate transporters and metabotropic receptors regulate excitatory neurotransmission in the medial entorhinal cortex of the rat. Brain Res 1027 (2004) 151-160
22. Jahr C.E. Drooling and stuttering, or do synapses whisper?. Trends Neurosci 26 (2003) 7-9
23. Ji R.R., and Strichartz G. Cell signaling and the genesis of neuropathic pain. Sci STKE 2004 (2004) reE14
24. Jonas P. The time course of signaling at central glutamatergic synapses. News Physiol Sci 15 (2000) 83-89
25. Kerchner G.A., Wilding T.J., Huettner J.E., and Zhuo M. Kainate receptor subunits underlying presynaptic regulation of transmitter release in the dorsal horn. J Neurosci 22 (2002) 8010-8017
26. Kerr F.W. Pain. A central inhibitory balance theory. Mayo Clin Proc 50 (1975) 685-690
27. Kojima S., Nakamura T., Nidaira T., Nakamura K., Ooashi N., Ito E., Watase K., Tanaka K., Wada K., Kudo Y., and Miyakawa H. Optical detection of synaptically induced glutamate transport in hippocampal slices. J Neurosci 19 (1999) 2580-2588
28. Kumazawa T., and Perl E.R. Primate cutaneous receptors with unmyelinated (C) fibres and their projection to the substantia gelatinosa. J Physiol 73 (1977) 287-304
29. Kumazawa T., and Perl E.R. Excitation of marginal and substantia gelatinosa neurons in the primate spinal cord: indications of their place in dorsal horn functional organization. J Comp Neurol 177 (1978) 417-434
30. Lee C.J., Labrakakis C., Joseph D.J., and MacDermott A.B. Functional similarities and differences of AMPA and kainate receptors expressed by cultured rat sensory neurons. Neuroscience 129 (2004) 35-48
31. Lehre K.P., and Danbolt N.C. The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 18 (1998) 8751-8757
32. Levenson J., Weeber E., Selcher J.C., Kategaya L.S., Sweatt J.D., and Eskin A. Long-term potentiation and contextual fear conditioning increase neuronal glutamate uptake. Nat Neurosci 5 (2002) 155-161
33. +-dependent glutamate uptake. J Neurosci 18 (1998) 9620-9628
34. Liaw W.J., Stephens Jr. R.L., Binns B.C., Chu Y., Sepkuty J.P., Johns R.A., Rothstein J.D., and Tao Y.X. Spinal glutamate uptake is critical for maintaining normal sensory transmission in rat spinal cord. Pain 115 (2005) 60-70
35. Liu G., Choi S., and Tsien R.W. Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron 22 (1999) 395-409
36. Maki R., Robinson M.B., and Dichter M.A. The glutamate uptake inhibitor L-trans-pyrrolidine-2,4-dicarboxylate depresses excitatory synaptic transmission via a presynaptic mechanism in cultured hippocampal neurons. J Neurosci 14 (1994) 6754-6762
37. Marcaggi P., and Attwell D. Role of glial amino acid transporters in synaptic transmission and brain energetics. Glia 47 (2004) 217-225
38. Mennerick S., and Zorumski C.F. Presynaptic influence on the time course of fast excitatory synaptic currents in cultured hippocampal cells. J Neurosci 15 (1995) 3178-3192
39. Molander C., Xu Q., and Grant G. The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J Comp Neurol 230 (1984) 133-141
40. Mugnaini E., Dino M.R., and Jaarsma D. The unipolar brush cells of the mammalian cerebellum and cochlear nucleus: cytology and microcircuitry. Prog Brain Res 114 (1997) 131-150
41. Nakatsuka T., Tsuzuki K., Ling J.X., Sonobe H., and Gu J.G. Distinct roles of P2X receptors in modulating glutamate release at different primary sensory synapses in rat spinal cord. J Neurophysiol 89 (2003) 3243-3252
42. Neugebauer V. Metabotropic glutamate receptors: important modulators of nociception and pain behavior. Pain 98 (2002) 1-8
43. Niederberger E., Schmidtko A., Coste O., Marian C., Ehnert C., and Geisslinger G. The glutamate transporter GLAST is involved in spinal nociceptive processing. Biochem Biophys Res Commun 346 (2006) 393-399
44. Niederberger E., Schmidtko A., Rothstein J.D., Geisslinger G., and Tegeder I. Modulation of spinal nociceptive processing through the glutamate transporter GLT-1. Neuroscience 116 (2003) 81-87
45. Oleskevich S., and Walmsley B. Phosphorylation regulates spontaneous and evoked transmitter release at a giant terminal in the rat auditory brainstem. J Physiol 526 Pt 2 (2000) 349-357
46. Overstreet L.S., Kinney G.A., Liu Y.B., Billups D., and Slater N.T. Glutamate transporters contribute to the time course of synaptic transmission in cerebellar granule cells. J Neurosci 19 (1999) 9663-9673
47. Palay S.L., and Chan-Palay V. Cerebellar cortex: Cytology and organization (1974), Springer, Berlin
48. Rexed B. The cytoarchitectonic organization of the spinal cord in the cat. J Comp Neurol 96 (1952) 415-466
49. Rossi D.J., Alford S., Mugnaini E., and Slater N.T. Properties of transmission at a giant glutamatergic synapse in cerebellum: the mossy fiber-unipolar brush cell synapse. J Neurophysiol 74 (1995) 24-42
50. Seal R.P., and Amara S.G. Excitatory amino acid transporters: a family in flux. Annu Rev Pharmacol Toxicol 39 (1999) 431-456
51. Shen Y., Hansel C., and Linden D.J. Glutamate release during LTD at cerebellar climbing fiber-Purkinje cell synapses. Nat Neurosci 5 (2002) 725-726
52. Shimamoto K., Sakai R., Takaoka K., Yumoto N., Nakajima T., Amara S.G., and Shigeri Y. Characterization of novel L-threo-beta-benzyloxyaspartate derivatives, potent blockers of the glutamate transporters. Mol Pharmacol 65 (2004) 1008-1015
53. Sims K.D., and Robinson M.B. Expression patterns and regulation of glutamate transporters in the developing and adult nervous system. Crit Rev Neurobiol 13 (1999) 169-197
54. Spacek J. Three-dimensional analysis of dendritic spines. III. Glial sheath. Anat Embryol 171 (1985) 245-252
55. Sung B., Lim G., and Mao J. Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats. J Neurosci 23 (2003) 2899-2910
56. Takayasu Y., Iino M., and Ozawa S. Roles of glutamate transporters in shaping excitatory synaptic currents in cerebellar Purkinje cells. Eur J Neurosci 19 (2004) 1285-1295
57. Thomson L.M., Zeng J., and Terman G.W. Differential effect of glutamate transporter inhibition on EPSCs in the morphine naive and morphine tolerant neonatal spinal cord slice. Neurosci Lett 407 (2006) 64-69
58. Trussell L. Control of time course of glutamatergic synaptic currents. Prog Brain Res 116 (1998) 59-69
59. Trussell L.O., Thio L.L., Zorumski C.F., and Fischbach G.D. Rapid desensitization of glutamate receptors in vertebrate central neurons. Proc Natl Acad Sci U S A 85 (1988) 2834-2838
60. Ventura R., and Harris K.M. Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19 (1999) 6897-6906
61. Vera-Portocarrero L.P., Mills C.D., Ye Z., Fullwood S.D., McAdoo D.J., Hulsebosch C.E., and Westlund K.N. Rapid changes in expression of glutamate transporters after spinal cord injury. Brain Res 927 (2002) 104-110
62. 2+ transients in the presence of cyclothiazide in the rat substantia gelatinosa neurons. Cell Calcium 35 (2004) 461-469
63. Wadiche J.I., and Jahr C.E. Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32 (2001) 301-313
64. Weng H.R., Aravindan N., Cata J.P., Chen J.H., Shaw A.D., and Dougherty P.M. Spinal glial glutamate transporters downregulate in rats with taxol-induced hyperalgesia. Neurosci Lett 386 (2005) 18-22
65. Weng H.R., Chen J.H., and Cata J.P. Inhibition of glutamate uptake in the spinal cord induces hyperalgesia and increased responses of spinal dorsal horn neurons to peripheral afferent stimulation. Neuroscience 138 (2006) 1351-1360
66. Wu L.J., Zhao M.G., Toyoda H., Ko S., and Zhuo M. Kainate receptor-mediated synaptic transmission in the adult anterior cingulate cortex. J Neurophysiol 94 (2005) 1805-1813
67. Yoshimura M., and Nishi S. Blind patch-clamp recordings from substantia gelatinosa neurons in adult rat spinal cord slices: pharmacological properties of synaptic currents. Neuroscience 53 (1993) 519-526
68. Zahn P.K., and Brennan T.J. Intrathecal metabotropic glutamate receptor antagonists do not decrease mechanical hyperalgesia in a rat model of postoperative pain. Anesth Analg 87 (1998) 1354-1359