Evidence that GAD65 mediates increased GABA synthesis during intense neuronal activity in vivo

Journal of Neurochemistry

Volumn 97, Issue 2, 2006, Pages 385-396

  Patel, Anant B ^a,c   De Graaf, Robin A ^a   Martin, David L ^b   Battaglioli, Gino ^b   Behar, Kevin L ^a,c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WADSWORTH CENTER   (United States)

^c TAC MRRC   (United States)

Author keywords

1H nuclear magnetic resonance; Bicuculline; Gabaculine; Glutamate decarboxylase; Seizures; Vigabatrin

Indexed keywords

4 AMINOBUTYRATE AMINOTRANSFERASE; 4 AMINOBUTYRIC ACID; GABACULINE; GLUTAMATE DECARBOXYLASE 65; VIGABATRIN; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; ANTICONVULSIVE AGENT; BICUCULLINE; GLUTAMATE DECARBOXYLASE; ISOENZYME; ISOPROTEIN;

ANIMAL EXPERIMENT; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; IMMUNOBLOTTING; MALE; NERVE CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SEIZURE; ANIMAL; CHEMICALLY INDUCED DISORDER; DOSE RESPONSE; METABOLISM; METHODOLOGY; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; TIME; WESTERN BLOTTING;

ANIMALIA;

4-AMINOBUTYRATE TRANSAMINASE; ANIMALS; ANTICONVULSANTS; BICUCULLINE; BLOTTING, WESTERN; DOSE-RESPONSE RELATIONSHIP, DRUG; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; ISOENZYMES; MAGNETIC RESONANCE SPECTROSCOPY; MALE; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; TIME FACTORS; VIGABATRIN;

EID: 33645288871     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03741.x     Document Type: Article

References (60)

1. Asada H. Kawamura Y. Maruyama K. et al. 1996 Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but are susceptible to seizures. Biochem. Biophys. Res. Commun. 229 891 895.
2. Asada H. Kawamura Y. Maruyama K. Kume H. Ding R. G. Kanbara N. Kuzume H. Sanbo M. Yagi T. Obata K. 1997 Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc. Natl Acad. Sci. USA 94 6496 6499.
3. Battaglioli G. Liu H. Martin D. L. 2003 Kinetic differences between the isoforms of glutamate decarboxylase: implications for the regulation of GABA synthesis. J. Neurochem. 86 879 887.
4. 31P NMR spectroscopic study of rat brain in vivo. Magn. Reson. Med. 31 660 667.
5. + and glutamate activates different neurotransmitter release mechanisms in GABAergic neurons: vesicular versus non-vesicular release of GABA. Neuroscience 54 1019 1034.
6. 1H magnetic resonance spectroscopy. NMR Biomed. 17 60 68.
7. Bradford M. M. 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 248 254.
8. Castañeda M. T. Sanabria E. R. Hernandez S. Ayala A. Reyna T. A. Wu J.-Y. Colom L. V. 2005 Glutamic acid decarboxylase isoforms are differentially distributed in the septal region of the rat. Neurosci. Res. 52 107 119.
9. Casu M. Gale K. 1981 Intracerebral injection of gamma vinyl GABA: method for measuring rates of GABA synthesis in specific brain regions in vivo. Life Sci. 29 681 688.
10. Chapman A. G. Evans M. C. 1983 Cortical GABA turnover during bicuculline seizures in rats. J. Neurochem. 41 886 889.
11. Chapman A. G. Meldrum B. S. Siesjo B. K. 1977 Cerebral metabolic changes during prolonged epileptic seizures in rats. J. Neurochem. 28 1025 1035.
12. Chapman A. G. Westerberg E. Siesjo B. K. 1981 The metabolism of purine and pyrimidine nucleotides in rat cortex during insulin-induced hypoglycemia and recovery. J. Neurochem. 36 179 189.
13. Ereciñska M. Nelson D. Daikhin Y. Yudkoff M. 1996 Regulation of GABA level in rat brain synaptosomes: fluxes through enzymes of the GABA shunt and effects of glutamate, calcium, and ketone bodies. J. Neurochem. 67 2325 2334.
14. Erlander M. G. Tillakaratne N. J. Feldblum S. Patel N. Tobin A. J. 1991 Two genes encode distinct glutamate decarboxylases. Neuron 7 91 100.
15. de Graaf R. A. Nicolay K. 1998 Adiabatic water suppression using frequency selective excitation. Magn. Reson. Med. 40 690 696.
16. 13C]-NMR spectroscopy. Magn. Reson. Med. 49 37 46.
17. de Graaf R. A. Patel A. B. Rothman D. L. Behar K. L. 2005 Acute regulation of steady-state GABA levels following GABA-transaminase inhibition in rat cerebral cortex. Neurochem. Int. xx xxx xxx in press )q7.
18. Gruetter R. 1993 Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn. Reson. Med. 29 804 811.
19. Haase A. Frahm J. Matthaei D. Hanicke W. Merboldt K. D. 1986 FLASH imaging. Rapid NMR imaging using low flip-angle pulses. J. Magn. Reson. 67 258 266.
20. Hassel B. Johannessen C. U. Sonnewald U. Fonnum F. 1998 Quantification of the GABA shunt and the importance of the GABA shunt versus the 2-oxoglutarate dehydrogenase pathway in GABAergic neurons. J. Neurochem. 71 1511 1518.
21. Hensch T. K. Fagiolini M. Mataga N. Stryker M. P. Baekkeskov S. Kash S. F. 1998 Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282 1504 1508.
22. Hsu C. C. Thomas C. Chen W. Davis K. M. Foos T. Chen J. L. Wu E. Floor E. Schloss J. V. Wu J. Y. 1999 Role of synaptic vesicle proton gradient and protein phosphorylation on ATP-mediated activation of membrane-associated brain glutamate decarboxylase. J. Biol. Chem. 274 24 366 24 371. q8
23. Itoh M. Uchimura H. 1981 Regional differences in cofactor saturation of glutamate decarboxylase (GAD) in discrete brain nuclei of the rat. Effect of repeated administration of haloperidol on GAD activity in the substantia nigra. Neurochem. Res. 6 1283 1289.
24. Jin H. Wu H. Osterhaus G. Wei J. Davis K. Sha D. Floor E. Hsu C. C. Kopke R. D. Wu J. Y. 2003 Demonstration of functional coupling between gamma-aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles. Proc. Natl Acad. Sci. USA 100 4293 4298.
25. de Jong B. M. Romijn H. J. Buijs R. M. 1987 Postembedding immunocytochemical GABA labeling in rat neocortex cultures: applicability in quantitative studies. Neurosci. Lett. 75 23 30.
26. Kash S. F. Johnson R. S. Tecott L. H. Noebels J. L. Mayfield R. D. Hanahan D. Baekkeskov S. 1997 Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc. Natl Acad. Sci. USA 94 14 060 14 065.
27. Kaufman D. L. Houser C. R. Tobin A. J. 1991 Two forms of the gamma-aminobutyric-acid synthetic enzyme glutamate-decarboxylase have distinct intraneuronal distributions and cofactor interactions. J. Neurochem. 56 720 723.
28. Krnjević K. 1970 Glutamate and gamma-aminobutyric acid in brain. Nature 228 119 124.
29. Löscher W. 1980 Comparative study of the inhibition of GABA aminotransferase by different anticonvulsant drugs. Arch. Int. Pharmacodyn. Ther. 243 48 55.
30. Löscher W. Honack D. Gramer M. 1989 Use of inhibitors of gamma-aminobutyric acid (GABA) transaminase for the estimation of GABA turnover in various brain regions of rats: a reevaluation of aminooxyacetic acid. J. Neurochem. 53 1737 1750.
31. Mackie M. Hughes D. I. Maxwell D. J. Tillakaratne N. J. Todd A. J. 2003 Distribution and colocalisation of glutamate decarboxylase isoforms in the rat spinal cord. Neurosci. 119 461 472.
32. 13C]glucose is reduced in rats treated with the GABA-transaminase inhibitor vigabatrin (gamma-vinyl GABA). Neurochem. Res. 21 1031 1041.
33. Martin D. L. Rimvall K. 1993 Regulation of gamma-aminobutyric acid synthesis in the brain. J. Neurochem. 60 395 407.
34. Martin D. L. Martin S. B. Wu S. J. Espina N. 1991a Regulatory properties of brain glutamate decarboxylase (GAD): the apoenzyme of GAD is present principally as the smaller of two molecular forms of GAD in brain. J. Neurosci. 11 2725 2731.
35. Martin D. L. Martin S. B. Wu S. J. Espina N. 1991b Cofactor interactions and the regulation of glutamate decarboxylase activity. Neurochem. Res. 16 243 249.
36. 67 protein. Brain Res. 914 81 91.
37. McCormick D. A. 1989 GABA as an inhibitory neurotransmitter in human cerebral cortex. J. Neurophysiol. 62 1018 1027.
38. Miller L. P. Walters J. R. Martin D. L. 1977 Post-mortem changes implicate adenine nucleotides and pyridoxal-5′-phosphate in regulation of brain glutamate decarboxylase. Nature 266 847 848.
39. Nagai T. McGeer P. L. McGeer E. G. 1983 Distribution of GABA-T-intensive neurons in the rat forebrain and midbrain. J. Comp. Neurol. 218 220 238.
40. Patel A. B. Rothman D. L. Cline G. W. Behar K. L. 2001 Glutamine is the major precursor for GABA synthesis in rat neocortex in vivo following acute GABA-transaminase inhibition. Brain Res. 919 207 220.
41. Patel A. B. de Graaf R. A. Mason G. F. Rothman D. L. Shulman R. G. Behar K. L. 2005 The contribution of GABA to glutamate/glutamine cycling and energy metabolism in the rat cortex in vivo. Proc. Natl Acad. Sci. USA 102 5588 5593.
42. Paulsen R. Fonnum F. 1987 Comparison of results obtained with different methods for estimating GABA turnover in rat neostriatum. Biochem. Pharmacol. 36 1539 1544.
43. Petroff O. A. Prichard J. W. Behar K. L. Alger J. R. Shulman R. G. 1984 In vivo phosphorus nuclear magnetic resonance spectroscopy in status epilepticus. Ann. Neurol. 16 169 177.
44. 1H-NMR spectroscopy coupled with microdialysis. Exp. Brain Res. 127 321 327.
45. Ponten U. Ratcheson R. A. Salford L. G. Siesjo B. K. 1973 Optimal freezing conditions for cerebral metabolites in rats. J. Neurochem. 21 1127 1138.
46. Porter T. G. Martin D. L. 1988 Stability and activation of glutamate apodecarboxylase from pig brain. J. Neurochem. 51 1886 1891.
47. Pow D. V. Baldridge W. Crook D. K. 1996 Activity-dependent transport of GABA analogues into specific cell types demonstrated at high resolution using a novel immunocytochemical strategy. Neuroscience 73 1129 1143.
48. Provencher S. W. 1993 Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn. Reson. Med. 30 672 679.
49. Rando R. R. Bangerter F. W. 1976 The irreversible inhibition of mouse brain gamma-aminobutyric acid (GABA)-alpha-ketoglutaric acid transaminase by gabaculine. J. Am. Chem. Soc. 98 6762 6764.
50. Rando R. R. Bangerter F. W. Farb D. H. 1981 The inactivation of gamma-aminobutyric acid transaminase in dissociated neuronal cultures from spinal cord. J. Neurochem. 36 985 990.
51. Richerson G. B. Wu Y. 2003 Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J. Neurophysiol. 90 1363 1374.
52. Rimvall K. Martin D. L. 1992 Increased intracellular gamma-aminobutyric acid selectively lowers the level of the larger of two glutamate decarboxylase proteins in cultured GABAergic neurons from rat cerebral cortex. J. Neurochem. 58 158 166.
53. Rimvall K. Martin D. L. 1994 The level of GAD67 protein is highly sensitive to small increases in intraneuronal gamma-aminobutyric acid levels. J. Neurochem. 62 1375 1381.
54. Schousboe A. Larsson O. M. Seiler N. 1986 Stereoselective uptake of the GABA-transaminase inhibitors gamma-vinyl GABA and gamma-acetylenic GABA into neurons and astrocytes. Neurochem. Res. 11 1497 1505.
55. Sheikh S. N. Martin D. L. 1998 Elevation of brain GABA levels with vigabatrin (gamma-vinyl GABA) differentially affects GAD65 and GAD67 expression in various regions of rat brain. J. Neurosci. Res. 52 736 741.
56. Sheikh S. N. Martin S. B. Martin D. L. 1999 Regional distribution and relative amounts of glutamate decarboxylase isoforms in rat and mouse brain. Neurochem. Int. 35 73 80.
57. Soghomonian J. J. Martin D. L. 1998 Two isoforms of glutamate decarboxylase: why? Trends Pharmacol. Sci. 19 500 505.
58. Waagepetersen H. S. Sonnewald U. Larsson O. M. Schousboe A. 1999 Synthesis of vesicular GABA from glutamine involves TCA cycle metabolism in neocortical neurons. J. Neurosci. Res. 57 342 349.
59. 13C magnetic resonance spectroscopy. J. Neurosci. Res. 63 347 355.
60. 13C] d -glucose. Magn. Reson. Med. 53 1258 1267.