Glutamine is required for persistent epileptiform activity in the disinhibited neocortical brain slice

Journal of Neuroscience

Volumn 30, Issue 4, 2010, Pages 1288-1300

  Tani, Hiroaki ^a   Dulla, Chris G ^a   Huguenard, John R ^a   Reimer, Richard J ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE AMMONIA LIGASE; GLUTAMIC ACID; GLUTAMINE;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN SLICE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; EPILEPTIC DISCHARGE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE;

ACTION POTENTIALS; ANIMALS; CARRIER PROTEINS; EPILEPSY; GLUTAMIC ACID; GLUTAMINE; NEOCORTEX; NERVE NET; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONS; ORGAN CULTURE TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION;

EID: 75349093906     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0106-09.2010     Document Type: Article

References (67)

1. Albrecht J, Sonnewald U, Waagepetersen HS, Schousboe A (2007) Glutamine in the central nervous system: function and dysfunction. Front Biosci 12:332-343.
2. Appelgren LE, Lindqvist I, Nilsson O, Ronquist G (1982) Distribution of some non-physiological amino acids (AIB, DAB, MeAIB) in mice. Acta Physiol Scand 115:261-268.
3. Aram JA, Lodge D (1988) Validation of a neocortical slice preparation for the study of epileptiform activity. J Neurosci Methods 23:211-224.
4. Bacci A, Sancini G, Verderio C, Armano S, Pravettoni E, Fesce R, Franceschetti S, MatteoliM (2002) Block of glutamate-glutamine cycle between astrocytes and neurons inhibits epileptiform activity in hippocampus. J Neurophysiol 88:2302-2310.
5. Blin M, Crusio WE, Hévor T, Cloix JF (2002) Chronic inhibition of glutamine synthetase is not associated with impairment of learning and memory in mice. Brain Res Bull 57:11-15.
6. Bröer S, Brookes N (2001) Transfer of glutamine between astrocytes and neurons. J Neurochem 77:705-719.
7. Broman J, Hassel B, Rinvik E, Ottersen OP (2000) Biochemistry and anatomy of transmitter glutamate. In: Glutamate (Ottersen OP, Storm-Mathisen J, eds), pp 1-44. Amsterdam: Elsevier.
8. Brugger F, Wicki U, Olpe HR, Froestl W, Mickel S (1993) The action of new potent GABAB receptor antagonists in the hemisected spinal cord preparation of the rat. Eur J Pharmacol 235:153-155.
9. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264 -278.
10. Chaudhry FA, Reimer RJ, Edwards RH (2002) The glutamine commute: take the N line and transfer to the A. J Cell Biol 157:349 -355.
11. Christensen HN (1962) Biological transport. New York: W. A. Benjamin. Christensen HN, Oxender DL, Liang M, Vatz KA (1965) The use of N-methylation to direct route of mediated transport of amino acids. J Biol Chem 240:3609-3616.
12. Conti F, Melone M (2006) The glutamine commute: lost in the tube? Neurochem Int 48:459-464.
13. Courtney KR, Prince DA (1977) Epileptogenesis in neocortical slices. Brain Res 127:191-196.
14. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105.
15. Darmaun D, Manary MJ, Matthews DE (1985) A method for measuring both glutamine and glutamate levels and stable isotopic enrichments. Anal Biochem 147:92-102.
16. Deuschle K, Okumoto S, Fehr M, Looger LL, Kozhukh L, Frommer WB (2005) Construction and optimization of a family of genetically encoded metabolite sensors by semirational protein engineering. Protein Sci 14:2304-2314.
17. Dulla C, Tani H, Okumoto S, Frommer WB, Reimer RJ, Huguenard JR (2008) Imaging of glutamate in brain slices using FRET sensors. J Neurosci Methods 168:306-319.
18. Eid T, Thomas MJ, Spencer DD, Rundén-Pran E, Lai JC, Malthankar GV, Kim JH, Danbolt NC, Ottersen OP, de Lanerolle NC (2004) Loss of glutamine synthetase in the human epileptogenic hippocampus: possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy. Lancet 363:28-37.
19. Eid T, Ghosh A, Wang Y, Beckström H, Zaveri HP, Lee TS, Lai JC, Malthankar-Phatak GH, de LanerolleNC (2008) Recurrent seizures and brain pathology after inhibition of glutamine synthetase in the hippocampus in rats. Brain 131:2061-2070.
20. Erecińska M, Silver IA (1990) Metabolism and role of glutamate in mammalian brain. Prog Neurobiol 35:245-296.
21. Fonnum F (1993) Regulation of the synthesis of the transmitter glutamate pool. Prog Biophys Mol Biol 60:47-57.
22. Fricke MN, Jones-Davis DM, Mathews GC (2007) Glutamine uptake by system A transporters maintains neurotransmitter GABA synthesis and inhibitory synaptic transmission. J Neurochem 102:1895-1904.
23. Furness DN, Dehnes Y, Akhtar AQ, Rossi DJ, Hamann M, Grutle NJ, Gundersen V, Holmseth S, Lehre KP, Ullensvang K, Wojewodzic M, Zhou Y, Attwell D, Danbolt NC (2008) A quantitative assessment of glutamate uptake into hippocampal synaptic terminals and astrocytes: new insights into a neuronal role for excitatory amino acid transporter 2 (EAAT2). Neuroscience 157:80 -94.
24. Geng MY, Saito H, Nishiyama N (1997) Protective effects of pyridoxal phosphate against glucose deprivation-induced damage in cultured hippocampal neurons. J Neurochem 68:2500-2506.
25. Gibbs ME, O'Dowd BS, Hertz L, Robinson SR, Sedman GL, Ng KT (1996) Inhibition of glutamine synthetase activity prevents memory consolidation. Brain Res Cogn Brain Res 4:57-64.
26. Giove F, Garreffa G, Peca S, Carní M, Macrì MA, Di Bonaventura C, Vaudano AE, Giallonardo AT, Prencipe M, Bozzao L, Pantano P, Colonnese C, Maraviglia B (2006) Metabolic alteration transients during paroxysmal activity in an epileptic patient with fixation-off sensitivity: a case study. Magn Reson Imaging 24:373-379.
27. Gutnick MJ, Connors BW, Prince DA (1982) Mechanisms of neocortical epileptogenesis in vitro. J Neurophysiol 48:1321-1335.
28. Hamberger AC, Chiang GH, Nylén ES, Scheff SW, CotmanCW (1979) Glutamate as a CNS transmitter. I. Evaluation of glucose and glutamine as precursors for the synthesis of preferentially released glutamate. Brain Res 168:513-530.
29. Henry PG, Russeth KP, Tkac I, Drewes LR, Andrews MT, Gruetter R (2007) Brain energy metabolism and neurotransmission at near-freezing temperatures: in vivo (1)H MRS study of a hibernating mammal. J Neurochem 101:1505-1515.
30. Hrabetová S, Nicholson C (2000) Dextran decreases extracellular tortuosity in thick-slice ischemia model. J Cereb Blood Flow Metab 20:1306-1310.
31. Kam K, Nicoll R (2007) Excitatory synaptic transmission persists independently of the glutamate-glutamine cycle. J Neurosci 27:9192-9200.
32. Kanamori K, Ross BD (2006) Kinetics of glial glutamine efflux and the mechanism of neuronal uptake studied in vivo in mildly hyperammonemic rat brain. J Neurochem 99:1103-1113.
33. Kaneko T (2000) Enzymes responsible for glutamate synthesis and degradation. In: Handbook of chemical neuroanatomy: glutamate, Vol 18, Chap VII (Ottersen OP, Storm-Mathisen J, eds), pp 202-230. Amsterdam: Elsevier Science.
34. Kapetanovic IM, Yonekawa WD, Kupferberg HJ (1993) Time-related loss of glutamine from hippocampal slices and concomitant changes in neurotransmitter amino acids. J Neurochem 61:865- 872.
35. Katz B (1962) The transmission of impulses from nerve to muscle, and the subcellular unit of synaptic action. Proc R Soc Lond B Biol Sci 155:455-477.
36. Katz B, Miledi R (1965) Release of acetylcholine from a nerve terminal by electric pulses of variable strength and duration. Nature 207: 1097-1098.
37. Katz B, Miledi R (1968) The role of calcium in neuromuscular facilitation. J Physiol 195:481-492.
38. Kvamme E (1998) Synthesis of glutamate and its regulation. Prog Brain Res 116:73- 85.
39. Lamar C Jr, Sellinger OZ (1965) The inhibition in vivo of cerebral glutamine synthetase and glutamine transferase by the convulsant methionine sulfoximine. Biochem Pharmacol 14:489-506.
40. Lerma J, Herranz AS, Herreras O, Abraira V, Martín del Río R (1986) In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res 384:145-155.
41. Liang SL, Carlson GC, Coulter DA (2006) Dynamic regulation of synaptic GABA release by the glutamate-glutamine cycle in hippocampal area CA1. J Neurosci 26:8537-8548.
42. Lieth E, LaNoue KF, Berkich DA, Xu B, Ratz M, Taylor C, Hutson SM (2001) Nitrogen shuttling between neurons and glial cells during glutamate synthesis. J Neurochem 76:1712-1723.
43. Mackenzie B, Erickson JD (2004) Sodium-coupled neutral amino acid (system N/A) transporters of the SLC38 gene family. Pflugers Arch 447:784-795.
44. Manning JM, Moore S, Rowe WB, Meister A (1969) Identification of L-methionine S-sulfoximine as the diastereoisomer of L-methionine SRsulfoximine that inhibits glutamine synthetase. Biochemistry 8:2681-2685.
45. Martinez-Hernandez A, Bell KP, Norenberg MD (1977) Glutamine synthetase: glial localization in brain. Science 195:1356 -1358.
46. Masson J, Darmon M, Conjard A, Chuhma N, Ropert N, Thoby-Brisson M, Foutz AS, Parrot S, Miller GM, Jorisch R, Polan J, Hamon M, Hen R, Rayport S (2006) Mice lacking brain/kidney phosphate-activated glutaminase have impaired glutamatergic synaptic transmission, altered breathing, disorganized goal-directed behavior and die shortly after birth. J Neurosci 26:4660-4671.
47. McKenna MC (2007) The glutamate-glutamine cycle is not stoichiometric: fates of glutamate in brain. J Neurosci Res 85:3347-3358.
48. Mienville JM, Vicini S (1987) A pyridazinyl derivative of gammaaminobutyric acid (GABA), SR 95531, is a potent antagonist of Clchannel opening regulated by GABAA receptors. Neuropharmacology 26:779 -783.
49. Min MY, Appenteng K (1996) Multimodal distribution of amplitudes of miniature and spontaneous EPSPs recorded in rat trigeminal motoneurones. J Physiol 494:171-182.
50. Otsuki T, Nakama H, Kanamatsu T, Tsukada Y (2005) Glutamate metabolism in epilepsy: 13C-magnetic resonance spectroscopy observation in the human brain. Neuroreport 16:2057-2060.
51. 2 fixation increases with brain activity. J Neurosci 24:11273-11279.
52. Pan JW, Williamson A, Cavus I, Hetherington HP, Zaveri H, Petroff OA, Spencer DD (2008) Neurometabolism in human epilepsy. Epilepsia 49 [Suppl 3]:31- 41.
53. Prince DA (1966) Modification of focal cortical epileptogenic discharge by afferent influences. Epilepsia 7:181-201.
54. Pyle JL, Kavalali ET, Choi S, Tsien RW (1999) Visualization of synaptic activity in hippocampal slices with FM1-43 enabled by fluorescence quenching. Neuron 24:803-808.
55. Rae C, Hare N, Bubb WA, McEwan SR, Bröer A, McQuillan JA, Balcar VJ, Conigrave AD, Bröer S (2003) Inhibition of glutamine transport depletes glutamate and GABA neurotransmitter pools: further evidence for metabolic compartmentation. J Neurochem 85:503-514.
56. Rothman DL, Behar KL, Hyder F, Shulman RG (2003) In vivo NMR studies of the glutamate neurotransmitter flux and neuroenergetics: implications for brain function. Annu Rev Physiol 65:401- 427.
57. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16:675-686.
58. Rowe WB, Meister A (1970) Identification of L-methionine-S-sulfoximine as the convulsant isomer of methionine sulfoximine. Proc Natl Acad Sci U S A 66:500-506.
59. Sandow N, Zahn RK, Gabriel S, Heinemann U, Lehmann TN (2009) Glutamine induces epileptiform discharges in superficial layers of the medial entorhinal cortex from pilocarpine-treated chronic epileptic rats in vitro. Epilepsia 50:849-858.
60. Shank RP, Bennett GS, Freytag SO, Campbell GL (1985) Pyruvate carboxylase: an astrocyte-specific enzyme implicated in the replenishment of amino acid neurotransmitter pools. Brain Res 329:364 -367.
61. Sibson NR, Mason GF, Shen J, Cline GW, Herskovits AZ, Wall JE, Behar KL, Rothman DL, Shulman RG (2001) In vivo (13)C NMR measurement of neurotransmitter glutamate cycling, anaplerosis and TCA cycle flux in rat brain during. J Neurochem 76:975-989.
62. Su TZ, Campbell GW, Oxender DL (1997) Glutamine transport in cerebellar granule cells in culture. Brain Res 757:69-78.
63. Syková E, NicholsonC (2008) Diffusion in brain extracellular space. Physiol Rev 88:1277-1340.
64. Tamarappoo BK, Raizada MK, Kilberg MS (1997) Identification of a system N-like Na(+)-dependent glutamine transport activity in rat brain neurons. J Neurochem 68:954-960.
65. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, Wada K (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276:1699 -1702.
66. Tani H, Bandrowski AE, Parada I, Wynn M, Huguenard JR, Prince DA, Reimer RJ (2007) Modulation of epileptiform activity by glutamine and system A transport in a model of post-traumatic epilepsy. Neurobiol Dis 25:230 -238.
67. Wolosker H, de Souza DO, de Meis L (1996) Regulation of glutamate transport into synaptic vesicles by chloride and proton gradient. J Biol Chem 271:11726 -11731.