Blockade of GABA synthesis only affects neural excitability under activated conditions in rat hippocampal slices

Neurochemistry International

Volumn 53, Issue 1-2, 2008, Pages 22-32

  Dericioglu, Nese ^a   Garganta, Cheryl L ^b   Petroff, Ognen A ^c   Mendelsohn, Dara ^c   Williamson, Anne ^c  

^a HACETTEPE UNIVERSITY   (Turkey)

^b TUFTS MEDICAL CENTER   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

GABA synthesis; GAD; Glutamate glutamine cycling

Indexed keywords

3 MERCAPTOPROPRIONIC ACID; 4 AMINOBUTYRIC ACID; GLUCOSE; GLUTAMIC ACID; POTASSIUM; THIOL DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; EPILEPSY; EVOKED RESPONSE; HIPPOCAMPUS; LIQUID CHROMATOGRAPHY; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; TANDEM MASS SPECTROMETRY;

3-MERCAPTOPROPIONIC ACID; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CREATINE; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID ANTAGONISTS; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLUTAMINE; HIPPOCAMPUS; MEMBRANE POTENTIALS; NERVE NET; NEURONS; POTASSIUM; RATS; SEIZURES; TANDEM MASS SPECTROMETRY;

RATTUS;

EID: 45849136327     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2008.04.006     Document Type: Article

References (58)

1. Adcock T., and Taberner P.V. Measuring changes in cerebral glutamate and GABA metabolism prior to convulsions induced by 3-mercaptopropionate. Biochem. Pharmacol. 27 (1978) 246-248
2. Axmacher N., Stemmler M., Engel D., Draguhn A., and Ritz R. Transmitter metabolism as a mechanism of synaptic plasticity: a modeling study. J. Neurophysiol. 91 (2004) 25-39
3. Bak L.K., Schousboe A., and Waagepetersen H.S. The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J. Neurochem. 98 (2006) 641-653
4. Battaglioli G., Liu H., and Martin D.L. Kinetic differences between the isoforms of glutamate decarboxylase: implications for the regulation of GABA synthesis. J. Neurochem. 86 (2003) 879-887
5. Blindermann J.M., Maitre M., Ossola L., and Mandel P. Purification and some properties of l-glutamate decarboxylase from human brain. Eur. J. Biochem. 86 (1978) 143-152
6. Bolteus A.J., Garganta C., and Bordey A. Assays for measuring extracellular GABA levels and cell migration rate in acute slices. Brain Res. Brain Res. Protoc. 14 (2005) 126-134
7. Chagnac-Amitai Y., and Connors B.W. Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J. Neurophysiol. 61 (1989) 747-758
8. Chiu C.S., Brickley S., Jensen K., Southwell A., McKinney S., Cull-Candy S., Mody I., and Lester H.A. GABA transporter deficiency causes tremor, ataxia, nervousness, and increased GABA-induced tonic conductance in cerebellum. J. Neurosci. 25 (2005) 3234-3245
9. Chowdhury G.M., Patel A.B., Mason G.F., Rothman D.L., and Behar K.L. Glutamatergic and GABAergic neurotransmitter cycling and energy metabolism in rat cerebral cortex during postnatal development. J. Cerebr. Blood Flow Metab. 27 (2007) 1895-1907
10. Crick E.W., Osorio I., Bhavaraju N.C., Linz T.H., and Lunte C.E. An investigation into the pharmacokinetics of 3-mercaptopropionic acid and development of a steady-state chemical seizure model using in vivo microdialysis and electrophysiological monitoring. Epilepsy Res. 74 (2007) 116-125
11. Duarte J.M., Cunha R.A., and Carvalho R.A. Different metabolism of glutamatergic and GABAergic compartments in superfused hippocampal slices characterized by nuclear magnetic resonance spectroscopy. Neuroscience 144 (2007) 1305-1313
12. Engel D., Pahner I., Schulze K., Frahm C., Jarry H., Ahnert-Hilger G., and Draguhn A. Plasticity of rat central inhibitory synapses through GABA metabolism. J. Physiol. 535 (2001) 473-482
13. Esclapez M., and Houser C.R. Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy. J. Comp. Neurol. 412 (1999) 488-505
14. Fan S.G., Wusteman M., and Iversen L.L. 3-mercaptopropionic acid inhibits GABA release from rat brain slices in vitro. Brain Res. 229 (1981) 371-377
15. Farrant M., and Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci. 6 (2005) 215-229
16. Feldblum S., Ackermann R.F., and Tobin A.J. Long-term increase of glutamate decarboxylase mRNA in a rat model of temporal lobe epilepsy. Neuron 5 (1990) 361-371
17. French J.A. Vigabatrin. Epilepsia 40 Suppl. 5 (1999) S11-S16
18. Golan H., Talpalar A.E., Schleifstein-Attias D., and Grossman Y. GABA metabolism controls inhibition efficacy in the mammalian CNS. Neurosci Lett. 217 (1996) 25-28
19. Fricke M.N., Jones-Davis D.M., and Mathews G.C. Glutamine uptake by System A transporters maintains neurotransmitter GABA synthesis and inhibitory synaptic transmission. J. Neurochem. 102 (2007) 1895-1904
20. Horton R.W., and Meldrum B.S. Seizures induced by allylglycine, 3-mercaptopropionic acid and 4-deoxypyridoxine in mice and photosensitive baboons, and different modes of inhibition of cerebral glutamic acid decarboxylase. Br. J. Pharmacol. 49 (1973) 52-63
21. Jin H., Wu H., Osterhaus G., Wei J., Davis K., Sha D., Floor E., Hsu C.C., Kopke R.D., and Wu J.Y. Demonstration of functional coupling between gamma-aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 4293-4298
22. Kapetanovic I.M., Yonekawa W.D., and Kupferberg H.J. Time-related loss of glutamine from hippocampal slices and concomitant changes in neurotransmitter amino acids. J. Neurochem. 61 (1993) 865-872
23. Karlsson A., Fonnum F., Malthe-Sorenssen D., and Storm-Mathisen J. Effect of the convulsive agent 3-mercaptopropionic acid on the levels of GABA, other amino acids and glutamate decarboxylase in different regions of the rat brain. Biochem. Pharmacol. 23 (1974) 3053-3061
24. Keros S., and Hablitz J.J. Subtype-specific GABA transporter antagonists synergistically modulate phasic and tonic GABAA conductances in rat neocortex. J. Neurophysiol. 94 (2005) 2073-2085
25. Lamar Jr. C. Mercaptopropionic acid: a convulsant that inhibits glutamate decarboxylase. J. Neurochem. 17 (1970) 165-170
26. Liang S.L., Carlson G.C., and Coulter D.A. Dynamic regulation of synaptic GABA release by the glutamate-glutamine cycle in hippocampal area CA1. J. Neurosci. 26 (2006) 8537-8548
27. Loscher W. gamma-Acetylenic GABA antagonizes the decrease in synaptosomal GABA concentrations but not the seizures induced by 3-mercaptopropionic acid in rats. Biochem. Pharmacol. 35 (1986) 3176-3180
28. Loscher W., and Vetter M. In vivo effects of aminooxyacetic acid and valproic acid on nerve terminal (synaptosomal) GABA levels in discrete brain areas of the rat. Correlation to pharmacological activities. Biochem. Pharmacol. 34 (1985) 1747-1756
29. Maguire J.L., Stell B.M., Rafizadeh M., and Mody I. Ovarian cycle-linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat. Neurosci. 8 (2005) 797-804
30. Mares P., Kubova H., Zouhar A., Folbergrova J., Koryntova H., and Stankova L. Motor and electrocorticographic epileptic activity induced by 3-mercaptopropionic acid in immature rats. Epilepsy Res. 16 (1993) 11-18
31. Martin D.L., and Tobin A.J. Mechanisms controlling GABA synthesis and degradation in the brain. In: Martin D.L., and Olsen R. (Eds). GABA in the Nervous System (2000), Williams & Wilkins, Philadelphia: Liponcott 25-41
32. Mathews G.C., and Diamond J.S. Neuronal glutamate uptake Contributes to GABA synthesis and inhibitory synaptic strength. J. Neurosci. 23 (2003) 2040-2048
33. McBain C.J. Hippocampal inhibitory neuron activity in the elevated potassium model of epilepsy. J. Neurophysiol. 73 (1995) 2853-2863
34. Moulder K.L., Jiang X., Taylor A.A., Olney J.W., and Mennerick S. Physiological activity depresses synaptic function through an effect on vesicle priming. J. Neurosci. 26 (2006) 6618-6626
35. Moulder K.L., Meeks J.P., and Mennerick S. Homeostatic regulation of glutamate release in response to depolarization. Mol. Neurobiol. 33 (2006) 133-153
36. Netopilova M., Drsata J., Haugvicova R., Kubova H., and Mares P. Inhibition of glutamate decarboxylase activity by 3-mercaptopropionic acid has different time course in the immature and adult rat brains. Neurosci. Lett. 226 (1997) 68-70
37. Netopilova M., Drsata J., Kubova H., and Mares P. Differences between immature and adult rats in brain glutamate decarboxylase inhibition by 3-mercaptopropionic acid. Epilepsy Res. 20 (1995) 179-184
38. Nusser Z., and Mody I. Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J. Neurophysiol. 87 (2002) 2624-2628
39. Patel A.B., de Graaf R.A., Martin D.L., Battaglioli G., and Behar K.L. Evidence that GAD65 mediates increased GABA synthesis during intense neuronal activity in vivo. J. Neurochem. 97 (2006) 385-396
40. Patrylo P.R., Spencer D.D., and Williamson A. GABA uptake and heterotransport are impaired in the dentate gyrus of epileptic rats and humans with temporal lobe sclerosis. J. Neurophysiol. 85 (2001) 1533-1542
41. Petroff O.A.C. GABA and glutamate in the human brain. Neuroscientist 8 (2002) 562-573
42. Petroff O.A., Errante L.D., Rothman D.L., Kim J.H., and Spencer D.D. Glutamate-glutamine cycling in the epileptic human hippocampus. Epilepsia 43 (2002) 703-710
43. Petroff O.A., Mattson R.H., and Rothman D.L. Proton MRS: GABA and glutamate. Adv. Neurol. 83 (2000) 261-271
44. Rae C., Hare N., Bubb W.A., McEwan S.R., Broer A., McQuillan J.A., Balcar V.J., Conigrave A.D., and Broer S. Inhibition of glutamine transport depletes glutamate and GABA neurotransmitter pools: further evidence for metabolic compartmentation. J. Neurochem. 85 (2003) 503-514
45. Rothman D.L., Behar K.L., Hetherington H.P., den Hollander J.A., Bendall M.R., Petroff O.A., and Shulman R.G. 1H-observe/13C-decouple spectroscopic measurements of lactate and glutamate in the rat brain in vivo. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 1633-1637
46. Rutecki P.A., Lebeda F.J., and Johnston D. Epileptiform activity induced by changes in extracellular potassium in hippocampus. J. Neurophysiol. 54 (1985) 1363-1374
47. Sanchez-Vives M.V., and McCormick D.A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3 (2000) 1027-1034
48. Sepkuty J.P., Cohen A.S., Eccles C., Rafiq A., Behar K., Ganel R., Coulter D.A., and Rothstein J.D. A neuronal glutamate transporter contributes to neurotransmitter GABA synthesis and epilepsy. J. Neurosci. 22 (2002) 6372-6379
49. Sibson N.R., Mason G.F., Shen J., Cline G.W., Herskovits A.Z., Wall J.E., Behar K.L., Rothman D.L., and Shulman R.G. In vivo (13)C NMR measurement of neurotransmitter glutamate cycling, anaplerosis and TCA cycle flux in rat brain during 2-13C glucose infusion. J. Neurochem. 76 (2001) 975-989
50. Sonnewald U., and McKenna M. Metabolic compartmentation in cortical synaptosomes: influence of glucose and preferential incorporation of endogenous glutamate into GABA. Neurochem. Res. 27 (2002) 43-50
51. Tagamets M.A., and Horwitz B. Interpreting PET and fMRI measures of functional neural activity: the effects of synaptic inhibition on cortical activation in human imaging studies. Brain Res. Bull. 54 (2001) 267-273
52. Tani H., Bandrowski A.E., Parada I., Wynn M., Huguenard J.R., Prince D.A., and Reimer R.J. Modulation of epileptiform activity by glutamine and system A transport in a model of post-traumatic epilepsy. Neurobiol. Dis. 25 (2007) 230-238
53. Waagepetersen H.S., Sonnewald U., Gegelashvili G., Larsson O.M., and Schousboe A. Metabolic distinction between vesicular and cytosolic GABA in cultured GABAergic neurons using 13C magnetic resonance spectroscopy. J. Neurosci. Res. 63 (2001) 347-355
54. Waagepetersen H.S., Sonnewald U., and Schousboe A. The GABA paradox: multiple roles as metabolite, neurotransmitter, and neurodifferentiative agent. J. Neurochem. 73 (1999) 1335-1342
55. Wu H., Jin Y., Buddhala C., Osterhaus G., Cohen E., Jin H., Wei J., Davis K., Obata K., and Wu J.-Y. Role of glutamate decarboxylase (GAD) isoform, GAD65, in GABA synthesis and transport into synaptic vesicles-evidence from GAD65-knockout mice studies. Brain Res. 1154 (2007) 80-83
56. Wu Y., Wang W., and Richerson G.B. GABA transaminase inhibition induces spontaneous and enhances depolarization-evoked GABA efflux via reversal of the GABA transporter. J. Neurosci. 21 (2001) 2630-2639
57. Wu Y., Wang W., and Richerson G.B. Vigabatrin induces tonic inhibition via GABA transporter reversal without increasing vesicular GABA release. J. Neurophysiol. 89 (2003) 2021-2034
58. Wu Y., Wang W., Diez-Sampedro A., and Richerson G.B. Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56 (2007) 851-865