Glial glutamate transporter and glutamine synthetase regulate GABAergic synaptic strength in the spinal dorsal horn

Journal of Neurochemistry

Volumn 121, Issue 4, 2012, Pages 526-536

  Jiang, Enshe ^a,b   Yan, Xisheng ^a   Weng, Han Rong ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b HENAN UNIVERSITY   (China)

Author keywords

Disinhibition; GABA; Glutamate transporters; Nociception; Pain; Synapses

Indexed keywords

4 AMINOBUTYRIC ACID; EXCITATORY AMINO ACID TRANSPORTER; GLIAL GLUTAMATE TRANSPORTER; GLT 1 PROTEIN; GLUTAMATE AMMONIA LIGASE; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; GLUTAMINE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL INTERACTION; CONTROLLED STUDY; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; GLIA CELL; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MINIATURE ENDPLATE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL; SYNAPSE; TISSUE SLICE;

ANIMALS; ASPARTIC ACID; ASTROCYTES; ELECTRIC STIMULATION; ELECTROPHYSIOLOGICAL PHENOMENA; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE-AMMONIA LIGASE; GLUTAMINE; KAINIC ACID; MALE; NEUROGLIA; PATCH-CLAMP TECHNIQUES; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

RATTUS;

EID: 84859772298     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07694.x     Document Type: Article

References (59)

1. Arriza J. L., Fairman W. A., Wadiche J. I., Murdoch G. H., Kavanaugh M. P. and Amara S. G. (1994) Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J. Neurosci. 14, 5559-5569. (Pubitemid 24279072)
2. Bak L. K., Schousboe A. and Waagepetersen H. S. (2006) The glutamate/ GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J. Neurochem. 98, 641-653. (Pubitemid 44051266)
3. Balakrishnan V., Kuo S. P., Roberts P. D. and Trussell L. O. (2009) Slow glycinergic transmission mediated by transmitter pooling. Nat. Neurosci. 12, 286-94.
4. Calcagnotto M. E., Paredes M. F. and Baraban S. C. (2002) Heterotopic neurons with altered inhibitory synaptic function in an animal model of malformation-associated epilepsy. J. Neurosci. 22, 7596-7605. (Pubitemid 35386361)
5. Chen Z., Muscoli C., Doyle T., Bryant L., Cuzzocrea S., Mollace V., Mastroianni R., Masini E. and Salvemini D. (2010) NMDA-receptor activation and nitroxidative regulation of the glutamatergic pathway during nociceptive processing. Pain 149, 100-106.
6. Coull J. A. M., Boudreau D., Bachand K., Prescott S. A., Nault F., Sik A., DeKoninck P. and DeKoninck Y. (2003) Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424, 938-942. (Pubitemid 37051684)
7. Danbolt N. C. (2001) Glutamate uptake. Prog. Neurobiol. 65, 1-105.
8. Foster T. C. and McNaughton B. L. (1991) Long-term enhancement of CA1 synaptic transmission is due to increased quantal size, not quantal content. Hippocampus 1, 79-91.
9. Fredj N. B. and Burrone J. (2009) A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat. Neurosci. 12, 751-758.
10. Fricke M. N., Jones-Davis D. M. and Mathews G. C. (2007) Glutamine uptake by System A transporters maintains neurotransmitter GABA synthesis and inhibitory synaptic transmission. J. Neurochem. 102, 1895-1904. (Pubitemid 47329253)
11. Hasegawa J., Obara T., Tanaka K. and Tachibana M. (2006) High-density presynaptic transporters are required for glutamate removal from the first visual synapse. Neuron 50, 63-74.
12. Hugel S. and Schlichter R. (2000) Presynaptic P2X receptors facilitate inhibitory GABAergic transmission between cultured rat spinal cord dorsal horn neurons. J. Neurosci. 20, 2121-2130. (Pubitemid 30230064)
13. Hunt R. F., Scheff S. W. and Smith B. N. (2011) Synaptic reorganization of inhibitory hilar interneuron circuitry after traumatic brain injury in mice. J. Neurosci. 31, 6880-6890.
14. Ingram R. A., Fitzgerald M. and Baccei M. L. (2008) Developmental changes in the fidelity and short-term plasticity of GABAergic synapses in the neonatal rat dorsal horn. J. Neurophysiol. 99, 3144-3150.
15. Juge N., Gray J. A., Omote H., Miyaji T., Inoue T., Hara C., Uneyama H., Edwards R. H., Nicoll R. A. and Moriyama Y. (2010) Metabolic control of vesicular glutamate transport and release. Neuron 68, 99-112.
16. Kam K. and Nicoll R. (2007) Excitatory synaptic transmission persists independently of the glutamate-glutamine cycle. J. Neurosci. 27, 9192-9200. (Pubitemid 47312054)
17. Kandel E., Schwartz J. and Jessell T. (2000) Principles of Neural Science, 4th edn. McGraw-Hill, New York.
18. Kawasaki Y., Zhang L., Cheng J. K. and Ji R. R. (2008) Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J. Neurosci. 28, 5189-5194.
19. Liang S. L., Carlson G. C. and Coulter D. A. (2006) Dynamic regulation of synaptic GABA release by the glutamate-glutamine cycle in hippocampal area CA1. J. Neurosci. 26, 8537-8548. (Pubitemid 44316183)
20. 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. (2005) Spinal glutamate uptake is critical for maintaining normal sensory transmission in rat spinal cord. Pain 115, 60-70.
21. Lipp P., Egger M. and Niggli E. (2002) Spatial characteristics of sarcoplasmic reticulum Ca2+ release events triggered by L-type Ca2+ current and Na+ current in guinea-pig cardiac myocytes. J. Physiol. 542, 383-393. (Pubitemid 35190301)
22. Malan T. P., Mata H. P. and Porreca F. (2002) Spinal GABA A and GABAB receptor pharmacology in a model of neuropathic pain. Anesthesiology 96, 1161-1167. (Pubitemid 34462578)
23. Manabe T., Wyllie D. J., Perkel D. J. and Nicoll R. A. (1993) Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J. Neurophysiol. 70, 1451-1459. (Pubitemid 23326382)
24. Mao J., Sung B., Ji R. R. and Lim G. (2002) Chronic morphine induces downregulation of spinal glutamate transporters: implications in morphine tolerance and abnormal pain sensitivity. J. Neurosci. 22, 8312-8323. (Pubitemid 35379137)
25. Marty V., Kuzmiski J. B., Baimoukhametova D. V. and Bains J. S. (2011) Short-term plasticity impacts information transfer at glutamate synapses onto parvocellular neuroendocrine cells in the paraventricular nucleus of the hypothalamus. J. Physiol. 589, 4259-4270.
26. Mathew S. S., Pozzo-Miller L. and Hablitz J. J. (2008) Kainate modulates presynaptic GABA release from two vesicle pools. J. Neurosci. 28, 725-731. (Pubitemid 351159023)
27. Mathews G. C. and Diamond J. S. (2003) Neuronal glutamate uptake Contributes to GABA synthesis and inhibitory synaptic strength. J. Neurosci. 23, 2040-2048. (Pubitemid 36368891)
28. Milligan E. D. and Watkins L. R. (2009) Pathological and protective roles of glia in chronic pain. Nat. Rev. Neurosci. 10, 23-36.
29. Moore K. A., Kohno T., Karchewski L. A., Scholz J., Baba H. and Woolf C. J. (2002) Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J. Neurosci. 22, 6724-6731. (Pubitemid 35386428)
30. Murthy V. N. and Stevens C. F. (1999) Reversal of synaptic vesicle docking at central synapses. Nat. Neurosci. 2, 503-507. (Pubitemid 30491229)
31. Muscoli C., Doyle T., Dagostino C., Bryant L., Chen Z., Watkins L. R., Ryerse J., Bieberich E., Neumman W. and Salvemini D. (2010) Counter-regulation of opioid analgesia by glial-derived bioactive sphingolipids. J. Neurosci. 30, 15400-15408.
32. Nie H. and Weng H. R. (2009) Glutamate Transporters Prevent Excessive Activation of NMDA Receptors and Extrasynaptic Glutamate Spillover in the Spinal Dorsal Horn. J. Neurophysiol. 101, 2041-2051.
33. Nie H. and Weng H. R. (2010) Impaired glial glutamate uptake induces extrasynaptic glutamate spillover in the spinal sensory synapses of neuropathic rats. J. Neurophysiol. 103, 2570-2580.
34. Nie H., Zhang H. and Weng H. R. (2010) Minocycline prevents impaired glial glutamate uptake in the spinal sensory synapses of neuropathic rats. Neuroscience 170, 901-912.
35. Ortinski P. I., Dong J., Mungenast A., Yue C., Takano H., Watson D. J., Haydon P. G. and Coulter D. A. (2011) Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat. Neurosci. 13, 584-591.
36. Overstreet L. S., Kinney G. A., Liu Y. B., Billups D. and Slater N. T. (1999) Glutamate transporters contribute to the time course of synaptic transmission in cerebellar granule cells. J. Neurosci. 19, 9663-9673. (Pubitemid 30228117)
37. Palmer M. J., Taschenberger H., Hull C., Tremere L. and von Gersdorff H. (2003) Synaptic activation of presynaptic glutamate transporter currents in nerve terminals. J. Neurosci. 23, 4831-4841. (Pubitemid 36793209)
38. Ren K. and Dubner R. (2010) Interactions between the immune and nervous systems in pain. Nat. Med. 16, 1267-1276.
39. Rothstein J. D., Dykes-Hoberg M., Pardo C. A. et al. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16, 675-686. (Pubitemid 26103145)
40. Schikorski T. and Stevens C. F. (2001) Morphological correlates of functionally defined synaptic vesicle populations. Nat. Neurosci. 4, 391-395. (Pubitemid 32260115)
41. Scholz J., Broom D. C., Youn D. H., Mills C. D., Kohno T., Suter M. R., Moore K. A., Decosterd I., Coggeshall R. E. and Woolf C. J. (2005) Blocking caspase activity prevents transsynaptic neuronal apoptosis and the loss of inhibition in lamina II of the dorsal horn after peripheral nerve injury. J. Neurosci. 25, 7317-7323. (Pubitemid 41129803)
42. Sellinger O. Z. (1967) Inactivation of cerebral glutamine synthetase by DL-methionine-DL-sulfoximine. Biochim. Biophys. Acta 132, 514-516.
43. Shimamoto K., Sakai R., Takaoka K., Yumoto N., Nakajima T., Amara S. G. and Shigeri Y. (2004) Characterization of novel L-threo-beta-benzyloxyaspartate derivatives, potent blockers of the glutamate transporters. Mol. Pharmacol. 65, 1008-1015. (Pubitemid 38420507)
44. Stiller C. O., Cui J. G., O'Connor W. T., Brodin E., Meyerson B. A. and Linderoth B. (1996) Release of y-aminobutyric acid in the dorsal horn and suppression of tactile alloydynia by spinal cord stimulation in mononeuropathic rats. Neurosurgery 39, 367-374.
45. Sung B., Lim G. and Mao J. (2003) Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats. J. Neurosci. 23, 2899-2910. (Pubitemid 36418626)
46. Tanaka K., Watase K., Manabe T. et al. (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276, 1699-1702. (Pubitemid 27421977)
47. Tong G. and Jahr C. E. (1994) Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13, 1195-1203. (Pubitemid 24372137)
48. Weng H. R., Aravindan N., Cata J. P., Chen J. H., Shaw A. D. and Dougherty P. M. (2005) Spinal glial glutamate transporters downregulate in rats with taxol-induced hyperalgesia. Neurosci. Lett. 386, 18-22. (Pubitemid 41019636)
49. Weng H. R., Chen J. H. and Cata J. P. (2006) Inhibition of glutamate uptake in the spinal cord induces hyperalgesia and increased responses of spinal dorsal horn neurons to peripheral afferent stimulation. Neuroscience 138, 1351-1360. (Pubitemid 43363551)
50. Weng H. R., Chen J. H., Pan Z. Z. and Nie H. (2007) Glial glutamate transporter 1 regulates the spatial and temporal coding of glutamatergic synaptic transmission in spinal lamina II neurons. Neuroscience 149, 898-907. (Pubitemid 350122884)
51. Winkler B. S., Kapousta-Bruneau N., Arnold M. J. and Green D. G. (1999) Effects of inhibiting glutamine synthetase and blocking glutamate uptake on b-wave generation in the isolated rat retina. Vis. Neurosci. 16, 345-353. (Pubitemid 29188127)
52. Xin W. J., Weng H. R. and Dougherty P. M. (2009) Plasticity in expression of the glutamate transporters GLT-1 and GLAST in spinal dorsal horn glial cells following partial sciatic nerve ligation. Mol. Pain 5, 15.
53. Xu H., Wu L. J., Wang H., Zhang X., Vadakkan K. I., Kim S. S., Steenland H. W. and Zhuo M. (2008) Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J. Neurosci. 28, 7445-7453.
54. Yaksh T. L. (1989) Behavioral and autonomic correlates of the tactile evoked allodynia produced by a spinal glycine inhibition:effects of modulatory receptor systems and excitatory amino acid antagonists. Pain 37, 111-123.
55. Yang K., Fujita T. and Kumamoto E. (2004) Adenosine inhibits GABAergic and glycinergic transmission in adult rat substantia gelatinosa neurons. J. Neurophysiol. 92, 2867-2877. (Pubitemid 40340498)
56. Yang C. P., Cherng C. H., Wu C. T., Huang H. Y., Tao P. L. and Wong C. S. (2011) Intrathecal ultra-low dose naloxone enhances the antinociceptive effect of morphine by enhancing the reuptake of excitatory amino acids from the synaptic cleft in the spinal cord of partial sciatic nerve-transected rats. Anesth. Analg. 113, 1490-500.
57. Yoshimura M. and Jessell T. M. (1989) Primary afferent-evoked synaptic responses and slow potential generation in rat substantia gelatinosa neurons in vitro. J. Neurophysiol. 62, 96-108. (Pubitemid 19180544)
58. Zhou Q., Petersen C. C. and Nicoll R. A. (2000) Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurones. J. Physiol. 525, 195-206. (Pubitemid 30311946)
59. Zucker R. S. (1989) Short-term synaptic plasticity. Annu. Rev. Neurosci. 12, 13-31.