Knockout of GAD65 has major impact on synaptic GABA synthesized from astrocyte-derived glutamine

Journal of Cerebral Blood Flow and Metabolism

Volumn 31, Issue 2, 2011, Pages 494-503

  Walls, Anne B ^a,b   Eyjolfsson, Elvar M ^a   Smeland, Olav B ^a   Nilsen, Linn Hege ^a   Schousboe, Inger ^c   Schousboe, Arne ^b   Sonnewald, Ursula ^a   Waagepetersen, Helle S ^b  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

13C isotopes; g vinylGABA (GVG; glutamate decarboxylase; hypometabolism; neuronal glial trafficking; nuclear magnetic resonance; vigabatrin)

Indexed keywords

4 AMINOBUTYRIC ACID; ACETIC ACID; CARBON 13; GLUCOSE; GLUTAMATE DECARBOXYLASE 65; GLUTAMINE; TRICARBOXYLIC ACID; VIGABATRIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; HIPPOCAMPUS; HOMEOSTASIS; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYNAPSE;

ACETATES; ANIMALS; ASTROCYTES; BLOTTING, WESTERN; CEREBRAL CORTEX; CITRIC ACID CYCLE; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GLUCOSE; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; GLUTAMINE; HIPPOCAMPUS; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SYNAPSES; VIGABATRIN;

EID: 79551616518     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/jcbfm.2010.115     Document Type: Article

References (41)

1. Asada H, Kawamura Y, Maruyama K, Kume H, Ding R, Ji FY, Kanbara N, Kuzume H, Sanbo M, Yagi T, Obata K (1996) Mice lacking the 65kDa 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 229:891-5
2. Asada H, Kawamura Y, Maruyama K, Kume H, Ding RG, 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 94:6496-9
3. Bak LK, Schousboe A, Waagepetersen HS (2006) The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem 98:641-53
4. Battaglioli G, Martin DL (1991) GABA synthesis in brain slices is dependent on glutamine produced in astro-cytes. Neurochem Res 16:151-6
5. Behar KL, Rothman DL (2001) In vivo nuclear magnetic resonance studies of glutamate-gamma-aminobutyric acid-glutamine cycling in rodent and human cortex: the central role of glutamine. J Nutr 131:2498S-504S
6. Bogen IL, Risa O, Haug KH, Sonnewald U, Fonnum F, Walaas SI (2008) Distinct changes in neuronal and astrocytic amino acid neurotransmitter metabolism in mice with reduced numbers of synaptic vesicles. J Neurochem 105:2524-34
7. Bradford HF, Ward HK, Thomas AJ (1978) Glutamine-a major substrate for nerve endings. J Neurochem 30:1453-9
8. Chowdhury GM, Gupta M, Gibson KM, Patel AB, Behar KL (2007) Altered cerebral glucose and acetate metabolism in succinic semialdehyde dehydrogenase-deficient mice: evidence for glial dysfunction and reduced glutamate/glutamine cycling. J Neurochem 103:2077-91
9. Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ (1991) Two genes encode distinct glutamate dec-arboxylases. Neuron 7:91-100
10. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR (1994) Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14:1834-55
11. Feldblum S, Erlander MG, Tobin AJ (1993) Different distributions of GAD65 and GAD67 mRNAs suggest thatthe two glutamate decarboxylases play distinctive functional roles. J Neurosci Res 34:689-706
12. Gram L, Larsson OM, Johnsen AH, Schousboe A (1988) Effects of valproate, vigabatrin and aminooxyacetic acid on release of endogenous and exogenous GABA from cultured neurons. Epilepsy Res 2:87-95
13. Geyer MA (2006) The family of sensorimotor gating disorders: comorbidities or diagnostic overlaps? Neuro-tox Res 10:211-20
14. Hassel B, Bachelard H, Jones P, Fonnum F, Sonnewald U (1997) Trafficking of amino acids between neurons and glia in vivo. Effects of inhibition of glial metabolism by fluoroacetate. J Cereb Blood Flow Metab 17:1230-8
15. Heldt SA, Green A, Ressler KJ (2004) Prepulse inhibition deficits in GAD65 knockout mice and the effect of antipsychotic treatment. Neuropsychopharmacology 29:1610-9
16. Kash SF, Johnson RS, Tecott LH, Noebels JL, Mayfield RD, Hanahan D, Baekkeskov S (1997) Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 94:14060-5
17. Kaufman DL, Houser CR, Tobin AJ (1991) Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J Neurochem 56:720-3
18. Kondziella D, Alvestad S, Vaaler A, Sonnewald U (2007) Which clinical and experimental data link temporal lobe epilepsy with depression? J Neurochem 103: 2136-52
19. Kubo K, Nishikawa K, Ishizeki J, Hardy-Yamada M, Yanagawa Y, Saito S (2009) Thermal hyperalgesia via supraspinal mechanisms in mice lacking glutamate decarboxylase 65. J Pharmacol Exp Ther 331:162-9
20. Laake JH, Takumi Y, Eidet J, Torgner IA, Roberg B, Kvamme E, Ottersen OP (1999) Postembedding immunogold labelling reveals subcellular localization and pathway-specific enrichment of phosphate activated glutaminase in rat cerebellum. Neuroscience 88:1137-51
21. Martin DL, Martin SB, Wu SJ, Espina N (1991) 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 11:2725-31
22. Mason GF, Rothman DL, Behar KL, Shulman RG (1992) NMR determination of the TCA cycle rate and a-ketoglutarate/glutamate exchange rate in rat brain. J Cereb Blood Flow Metab 12:434-47
23. Mawhinney TP, Robinett RS, Atalay A, Madson MA (1986) Analysis of amino acids as their tert.-butyldimethylsilyl derivatives by gas-liquid chromatography and mass spectrometry. J Chromatogr 358:231-42
24. Ottersen OP, Storm-Mathisen J (1985) Different neuronal localization of aspartate-like and glutamate-like immu-noreactivities in the hippocampus of rat, guinea-pig and Senegalese baboon (Papio papio), with a note on the distribution of gamma-aminobutyrate. Neuroscience 16:589-606
25. Ottersen OP, Zhang N, Walberg F (1992) Metabolic compartmentation of glutamate and glutamine: morphological evidence obtained by quantitative immunocyto-chemistry in rat cerebellum. Neuroscience 46:519-34
26. Patel AB, de Graaf RA, Mason GF, Rothman DL, Shulman RG, Behar KL (2005) The contribution of GABA to glutamate/ glutamine cycling and energy metabolism in the rat cortex in vivo. Proc Natl Acad Sci USA 102:5588-93
27. Qu H, Haberg A, Haraldseth O, Unsgard G, Sonnewald U (2000) (13)C MR spectroscopy study of lactate as substrate for rat brain. Dev Neurosci 22:429-36
28. Schousboe A, Sarup A, Bak LK, Waagepetersen HS, Larsson OM (2004) Role of astrocytic transport processes in glutamatergic and GABAergic neurotransmis-sion. Neurochem Int 45:521-7
29. Sheikh SN, Martin SB, Martin DL (1999) Regional distribution and relative amounts of glutamate decarboxylase isoforms in rat and mouse brain. Neu-rochem Int 35:73-80
30. 13C NMR. Proc Natl Acad Sci USA 96:8235-40
31. 13C]glucose infusion. J Neurochem 76:975-89
32. Sonnewald U, Kondziella D (2003) Neuronal glial interaction in different neurological diseases studied by ex vivo 13C NMR spectroscopy. NMR Biomed 16:424-9
33. Sonnewald U, Westergaard N, Schousboe A, Svendsen JS, Unsgard G, Petersen SB (1993) Direct demonstration by [13C]NMR spectroscopy that glutamine from astrocytes is a precursor for GABA synthesis in neurons. Neuro-chem Int 22:19-29
34. Stork O, Ji FY, Kaneko K, Stork S, Yoshinobu Y, Moriya T, Shibata S, Obata K (2000) Postnatal development of a GABA deficit and disturbance of neural functions in mice lacking GAD65. Brain Res 865:45-58
35. Tamminga CA, Holcomb HH (2005) Phenotype of schizophrenia: a review and formulation. Mol Psychiatry 10:27-39
36. Tian N, Petersen C, Kash S, Baekkeskov S, Copenhagen D, Nicoll R (1999) The role of the synthetic enzyme GAD65 in the control of neuronal gamma-aminobutyric acid release. Proc Natl Acad Sci USA 96:12911-6
37. Van den Berg CJ, Krzalic L, Mela P, Waelsch H (1969) Compartmentation of glutamate metabolism in brain. Evidence for the existence of two different tricarboxylic acid cycles in brain. Biochem J 113:281-90
38. Waagepetersen HS, Sonnewald U, Schousboe A (1999a) The GABA paradox: multiple roles as metabolite, neurotransmitter, and neurodifferentiative agent. J Neuro-chem 73:1335-42
39. Waagepetersen HS, Sonnewald U, Larsson OM, Schousboe A (1999b) Synthesis of vesicular GABA from glutamine involves TCA cycle metabolism in neocortical neurons. J Neurosci Res 57:342-9
40. Waagepetersen HS, Sonnewald U, Gegelashvili G, Larsson OM, Schousboe A (2001) Metabolic distinction between vesicular and cytosolic GABA in cultured GABAergic neurons using 13C magnetic resonance spectroscopy. J Neurosci Res 63:347-55
41. Waniewski RA, Martin DL (1998) Preferential utilization of acetate by astrocytes is attributable to transport. J Neurosci 18:5225-33