Electrographic seizures are significantly reduced by in vivo inhibition of neuronal uptake of extracellular glutamine in rat hippocampus

Epilepsy Research

Volumn 107, Issue 1-2, 2013, Pages 20-36

  Kanamori, Keiko ^a   Ross, Brian D ^a  

^a HUNTINGTON MEDICAL RESEARCH INSTITUTES   (United States)

Author keywords

2 (Methylamino)isobutyrate; EAAT; ECF; Epileptic seizure; Extracellular glutamine; GABA; GLN; GLU; KA; Kainate; MeAIB; Neuronal uptake; Rat hippocampus; SNAT; TAU

Indexed keywords

2 METHYL 2 METHYLAMINOPROPIONIC ACID; 4 AMINOBUTYRIC ACID; AMINO ACID TRANSPORTER; GLUTAMINE; GLYCINE; KAINIC ACID; SODIUM COUPLED NEUTRAL AMINO ACID TRANSPORTER 1; SODIUM COUPLED NEUTRAL AMINO ACID TRANSPORTER 2; TAURINE; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG TARGETING; ELECTROENCEPHALOGRAPHY; EPILEPTIC DISCHARGE; EXTRACELLULAR FLUID; EXTRACELLULAR SPACE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; IN VIVO STUDY; MALE; MICRODIALYSIS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; STEADY STATE; TEMPORAL LOBE EPILEPSY;

2-(METHYLAMINO)ISOBUTYRATE; EAAT; ECF; EPILEPTIC SEIZURE; EXCITATORY AMINO ACID TRANSPORTER; EXTRACELLULAR FLUID; EXTRACELLULAR GLUTAMINE; GABA; GLN; GLU; GLUTAMATE; GLUTAMINE; KA; KAINATE; KAINIC ACID; MEAIB; NEURONAL UPTAKE; RAT HIPPOCAMPUS; SNAT; SODIUM-COUPLED NEUTRAL AMINO ACID TRANSPORTER; TAU; TAURINE; Γ-AMINOBUTYRIC ACID;

AMINO ACID TRANSPORT SYSTEM A; AMINO ACID TRANSPORT SYSTEMS; AMINOISOBUTYRIC ACIDS; ANIMALS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLUTAMINE; HIPPOCAMPUS; KAINIC ACID; MALE; MICRODIALYSIS; NEURONS; RATS; RATS, WISTAR; SEIZURES;

EID: 84886946983     PISSN: 09201211     EISSN: 18726844     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2013.08.007     Document Type: Article

References (68)

1. + transport by the neural glutamine transporter ATA1. Pflüg. Arch.-Eur. J. Physiol. 2001, 443(1):92-101.
2. Andersen P., Bliss T.V.P., Skrede K.K. Unit analysis of hippocampal polulation spikes. Exp. Brain Res. 1971, 13(2):208-221.
3. Bacci A., Sancini G., Verderio C., Armano S., Pravettoni E., Fesce R., Franceschetti S., Matteoli M. Block of glutamate-glutamine cycle between astrocytes and neurons inhibits epileptiform activity in hippocampus. J. Neurophysiol. 2002, 88(5):2302-2310.
4. Bradford H.F. Glutamate, GABA and epilepsy. Prog. Neurobiol. 1995, 47(6):477-511.
5. Bragin A., Azizyan A., Almajano J., Wilson C.L., Engel J. Analysis of chronic seizure onsets after intrahippocampal kainic acid injection in freely moving rats. Epilepsia 2005, 46(10):1592-1598.
6. Bragin A., Engel J., Staba R.J. High-frequency oscillations in epileptic brain. Curr. Opin. Neurol. 2010, 23(2):151-156.
7. Bragin A., Engel J., Wilson C.L., Vizentin E., Mathern G.W. Electrophysiologic analysis of a chronic seizure model after unilateral hippocampal KA injection. Epilepsia 1999, 40(9):1210-1221.
8. Bröer S., Brookes N. Transfer of glutamine between astrocytes and neurons. J. Neurochem. 2001, 77(3):705-719.
9. Brown M.N., Mathews G.C. Activity- and age-dependent modulation of GABAergic neurotransmission by system A-mediated glutamine uptake. J. Neurochem. 2010, 114:909-920.
10. Bruhn T., Cobo M., Berg M., Diemer N.H. Limbic seizure-induced changes in extracellular amino acid levels in the hippocampal formation: a microdialysis study of freely moving rats. Acta Neurol. Scand. 1992, 86(5):455-461.
11. Cavus I., Kasoff W.S., Cassaday M.P., Jacob R., Gueorguieva R., Sherwin R.S., Krystal J.H., Abi-Saab W.M., Spencer D.D. Extracellular metabolites in the cortex and hippocampus of epileptic patients. Ann. Neurol. 2005, 57(2):226-235.
12. Cavus I., Pan J.W., Hetherington H.P., Abi-Saab W., Zaveri H.P., Vives K.P., Krystal J.H., Spencer S.S., Spencer D.D. Decreased hippocampal volume on MRI is associated with increased extracellular glutamate in epilepsy patients. Epilepsia 2008, 49(8):1358-1366.
13. Chaudhry F.A., Reimer R.J., Edwards R.H. The glutamine commute: take the N line and transfer to the A. J. Cell Biol. 2002, 157:349-355.
14. Chaudhry F.A., Reimer R.J., Krizaj D., Barber D., Storm-Mathisen J., Copenhagen D.R., Edwards R.H. Molecular analysis of system N suggests novel physiological roles in nitrogen metabolism and synaptic transmission. Cell 1999, 99(7):769-780.
15. Christensen H.N. Role of amino acid transport and countertransport in nutrition and metabolism. Physiol. Rev. 1990, 70:43-77.
16. Christensen H.N., Cullen A.M. Effects of non-metabolizable analogs on the distribution of amino acids in the rat. Biochim. Biophys. Acta 1968, 150:237-252.
17. Christensen H.N., Oxender D.L., Liang M., Vatz K.A. The use of N-methylation to direct the route of mediated transport of amino acids. J. Biol. Chem. 1965, 240:3609-3616.
18. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 2001, 65(1):1-105.
19. During M.J., Spencer D.D. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 1993, 341(8861):1607-1610.
20. Eid T., Behar K., Dhaher R., Bumanglag A.V., Lee T.W. Roles of glutamine synthetase inhibition in epilepsy. Neurochem. Res. 2012, 37:2339-2350.
21. Eid T., Ghosh A., Wang Y., Beckstrom H., Zaveri H.P., Lee T.S.W., Lai J.C.K., Malthankar-Phatak G.H., de Laneroll N.C. Recurrent seizures and brain pathology after inhibition of glutamine synthetase in the hippoccampus in rats. Brain 2008, 131(Pt 8):2061L 2070.
22. Eid T., Thomas M.J., Spencer D.D., Rundén-Pran E., Lai J.C.K., Malthanker G.V., Kim J.H., Danbolt N.C., Ottersen O.P., de Lanerolle N.C. Loss of glutamine synthetase in the human epileptogenic hippocampus: possible mechanism for raised extracellular glutamate in medial temporal lobe epilepsy. Lancet 2004, 363(9402):28-37.
23. Erecinska M., Silver I.A. Metabolism and role of glutamate in mammalian brain. Prog. Neurobiol. 1990, 35(4):245-296.
24. Estevez A.Y., O'Regan M.H., Song D.K., Phillis J.W. Effects of anion channel blockers on hyposmotically induced amino acid release from the in vivo rat cerebral cortex. Neurochem. Res. 1999, 24(3):447-452.
25. 13C-edited NMR spectroscopy. J. Cereb. Blood Flow Metab. 1990, 10(2):170-179.
26. González-González I.M., Cubelos B., Gimenéz C., Zafra F. Immunohistochemical localization of the amino acid transporter SNAT2 in the rat brain. Neuroscience 2005, 130(1):61-73.
27. Grewal S., Defamie N., Zhang X., De Gois S., Shawki A., Mackenzie B., Chen C., Varoqui H., Erickson J.D. SNAT2 amino acid transporter is regulated by amino acids of the SLC6 gamma-aminobutyric acid transporter subfamily in neocortical neurons and may play no role in delivering glutamine for glutamatergic transmission. J. Biol. Chem. 2009, 284(17):11224-11236.
28. Gullans S.R., Verbalis J.G. Control of brain volume during hyperosmolar and hypoosmolar conditions. Annu. Rev. Med. 1993, 44:289-301.
29. Hammer J., Alvestad S., Osen K.K., Skare O., Sonnewald U., Ottersen O.P. Expression of glutamine synthetase and glutamate dehydrogenase in the latent phase and chronic phase in the kainate model of temporal lobe epilepsy. Glia 2008, 56(8):856-868.
30. Hertz L. Functional interactions between neurons and astrocytes I. Turnover and metabolism of putative amino acid transmitters. Prog. Neurobiol. 1979, 13(3):277-323.
31. Jefferys J.G.R. Advances in understanding basic mechanisms of epilepsy and seizures. Seizure 2010, 19(10):638-646.
32. Jenstad M., Quazi A.Z., Zilberter M., Haglerod C., Berghuis P., Saddique N., Goiny M., Buntup D., Davenger S., Haug F.M., Barnes C.A., McNaughton B.L., Ottersen O.P., Storm-Mathisen J., Harkany T., Chaudhry F.A. System A transporter SAT2 mediates replenishment of dendritic glutamate pools controlling retrograde signaling by glutamate. Cereb. Cortex 2009, 19(5):1092-1106.
33. Junyent F., De Lemos L., Utrera J., Paco S., Aguado F., Camins A., Pallas M., Romero R., Auladell C. Content and traffic of taurine in hippocampal reactive astrocytes. Hippocampus 2011, 21(2):185-197.
34. 15N heteronuclear multiple-quantum coherence-transfer NMR in severely hyperammonemic rat. J. Neurochem. 1997, 68:1209-1220.
35. 15N coupling in mammalian brain. J. Magn. Reson. 2001, 153(2):193-202.
36. Kanamori K., Ross B.D. Quantitative determination of extracellular glutamine concentration in rat brain, and its elevation in vivo by system A transport inhibitor, α-(methylamino)isobutyrate. J. Neurochem. 2004, 90(1):203-210.
37. Kanamori K., Ross B.D. Suppression of glial glutamine release to the extracellular fluid studied in vivo by NMR and microdialysis in hyperammonemic rat brain. J. Neurochem. 2005, 94:74-85.
38. Kanamori K., Ross B.D. Kinetics of glial glutamine efflux and the mechanism of neuronal uptake studied in vivo in mildly hyperammonemic rat brain. J. Neurochem. 2006, 99(4):1103-1113.
39. Kanamori K., Ross B.D. Chronic electrographic seizure reduces glutamine and elevates glutamate in the extracellular fluid of rat brain. Brain Res. 2011, 1371:180-191.
40. 15N NMR. J. Neurochem. 1998, 70(3):1304-1315.
41. 13C-enrichment measurement of extracellular glutamate in rat brain. J. Neurosci. Methods 2002, 120(2):179-192.
42. Lehmann A., Hagberg H., Jacobson I., Hamberger A. Effects of status epilepticus on extracellular amino acids in the hippocampus. Brain Res. 1985, 359(1-2):147-151.
43. Löscher L., Fisher J.E., Nau H., Hönack D. Valproic acid in amygdala-kindled rats: alterations in anticonvulsant efficacy, adverse effects and drug and metabolite levels in various brain regions during chronic treatment. J. Pharmacol. Exp. Ther. 1989, 250:1067-1078.
44. Mackenzie B., Schäfer M.K., Erickson J.D., Hediger M.A., Weihe E., Varoqui H. Functional properties and cellular distribution of the system A glutamine transporter SNAT1 support specialized roles in central neurons. J. Biol. Chem. 2003, 278(26):23720-23730.
45. Mathern G.W., Cifuentes F., Leite J.P., Pretorius J.K., Babb T.L. Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalogr. Clin. Neurophysiol. 1993, 87(5):326-339.
46. +-coupled neutral amino acid transporter 2 in the cerebral cortex. Neuroscience 2006, 140:281-292.
47. Morimoto K., Fahnestock M., Racine R.J. Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog. Neurobiol. 2004, 73(1):1-60.
48. Nagelhus E.A., Lehmann A., Ottersen O.P. Neuronal and glial handling of glutamate and glutamine during hypoosmotic stress; a biochemical and quantitative immunocytochemical analysis using the rat cerebellum as a model. Neuroscience 1996, 72:743-755.
49. Obrenovitch T.P., Urenjak J., Zilkha E. Evidence disputing the link between seizure activity and high extracellular glutamate. J. Neurochem. 1996, 66(6):2446-2454.
50. Ottersen O.P., Zhang N., Walberg F. Metabolic compartmentation of glutamate and glutamine; morphological evidence obtained by quantitative immunocytochemistry in rat cerebellum. Neuroscience 1992, 46:519-534.
51. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1997, Academic Press, New York. 3rd ed.
52. Riban V., Bouilleret V., Pham-Le B.T., Fritschy J.M., Marescaux C., Depaulis A. Evolution of hippocampal epileptic activity during the development of hippocampal sclerosis in a mouse model of temporal lobe epilepsy. Neuroscience 2002, 112(1):101-111.
53. Ronne-Engström E., Hillered L., Flink R., Spannare B., Ungerstedt U., Carlson H. Intracerebral microdialysis of extracellular amino acids in the human epileptic focus. J. Cereb. Blood Flow Metab. 1992, 12(5):873-876.
54. Rothstein J.D., Dykes-Hoberg M., Pardo C.A., Bristol L.A., Jin L., Kunci R.W., Kanai Y., Hediger M.A., Wang Y., Shielke J.P., Welty D.F. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996, 16(3):675-686.
55. Shank R.P., Aprison M.H. Present status and significance of the glutamine cycle in neural tissues. Life Sci. 1981, 28(8):837-842.
56. Shennan D.B. Swelling-induced taurine transport: relationship with chloride channels, anion-exchangers and other swelling-activated transport pathways. Cell Physiol. Biochem. 2008, 21(1-3):15-28.
57. Solbu T.T., Bjørkmo M., Berghuis P., Harkany T., Chaudhry F.A. SAT1, a glutamine transporter, is preferentially expressed in GABAergic neurons. Front. Neuroanat. 2010, 4:1-13.
58. Stafford M.M., Brown M.N., Mishra P., Stanwood G.D., Mathews G.C. Glutamate spillover augments GABA synthesis and release from axodendritic synapses in rat hippocampus. Hippocampus 2010, 20(1):134-144.
59. Su T.Z., Campbell G.W., Oxender D.L. Glutamine transport in cerebellar granule cells in culture. Brain Res. 1997, 757(1):69-78.
60. Takazawa A., Murashima Y.L., Minatogawa Y., Kojima T., Tanaka K., Yamauchi T. In vivo microdialysis monitoring for extracellular glutamate and GABA in the ventral hippocampus of the awake rat during kainate-induced seizures. Psychiatry Clin. Neurosci. 1995, 49(3):S275-S277.
61. Tanaka T., Tanaka S., Fujita T., Takano K., Fukuda H., Sako K., Yonemasu Y. Experimental complex partial seizures induced by a microinjection of kainic acid into limbic structures. Prog. Neurobiol. 1992, 38(3):317-334.
62. Tani H., Bandrowski A.E., Parada I., Wynn M., Huguenard J.R., Prince D.A., Reimer R.J. Modulation of epileptiform activity by glutamine and system A transport in a model of post-traumatic epilepsy. Neurobiol. Dis. 2007, 25(2):230-238.
63. Thomas P.M., Phillips J.P., O'Connor W.T. Hippocampal microdialysis during spontaneous intraoperative epileptiform activity. Acta Neurochir. (Wien) 2004, 146(2):143-151.
64. Ueda Y., Doi T., Tokumaru J., Yokoyama H., Nakajima A., Mitsuyama Y., Ohya-Nishiguchi H., Kamada H., Willmore L.J. Collapse of extracellular glutamate regulation during epileptogenesis: down-regulation and functional failure of glutamate transporter function in rats with chronic seizures induced by kainic acid. J. Neurochem. 2001, 76(3):892-900.
65. Varoqui H., Zhu H., Yao D., Ming H., Erickson J.D. Cloning and functional identification of a neuronal glutamine transporter. J. Biol. Chem. 2000, 275(6):4049-4054.
66. Vincent P., Mulle C. Kainate receptors in epilepsy and excitotoxicity. Neuroscience 2009, 158(1):309-323.
67. Wilson C.L., Maidment N.T., Shomer M.H., Behnke E.J., Ackerson L., Fried I., Engel J. Comparison of seizure related amino acid release in human epileptic hippocampus versus a chronic, kainate rat model of hippocampal epilepsy. Epilepsy Res. 1996, 26(1):245-254.
68. +/neutral amino acid cotransport. J. Biol. Chem. 2000, 275(30):22790-22797.