Neuronal and astrocytic shuttle mechanisms for cytosolic-mitochondrial transfer of reducing equivalents: Current evidence and pharmacological tools

Biochemical Pharmacology

Volumn 71, Issue 4, 2006, Pages 399-407

  McKenna, Mary C ^a   Waagepetersen, Helle S ^b   Schousboe, Arne ^b   Sonnewald, Ursula ^c  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

3 NPA; AOAA; aralar1; Aspartate aminotransferase; Astrocytes; BMA; Glycerol 3 phosphate shuttle; Malate dehydrogenase; Malate aspartate shuttle; Malate ketoglutarate carrier; Neuronal and astrocytic shuttle mechanisms; Neurons; Phenylsuccinate

Indexed keywords

2 OXOGLUTARIC ACID; 3 METHYLENEASPARTIC ACID; 3 NITROPROPIONIC ACID; AMINOOXYACETIC ACID; ASPARTATE AMINOTRANSFERASE; ASPARTATE GLUTAMATE CARRIER ARALAR1; ASPARTIC ACID; ASPARTIC ACID DERIVATIVE; DIHYDROXYACETONE PHOSPHATE; GALLIC ACID PROPYL ESTER; GLUTAMINE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; GLYCEROPHOSPHATE; MALATE DEHYDROGENASE; NEUROTRANSMITTER; OXALOACETIC ACID; PHENYLSUCCINATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUCCINATE DEHYDROGENASE; SUCCINIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ASTROCYTE; BRAIN SYNAPTOSOME; CELLULAR DISTRIBUTION; CYTOSOL; DRUG ACTIVITY; DRUG EFFECT; DRUG MECHANISM; ENERGY METABOLISM; GLUCOSE METABOLISM; GLYCOLYSIS; HUMAN; MITOCHONDRION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 30444437034     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2005.10.011     Document Type: Note

References (53)

1. J.M. Berg, J.L. Tymoczko, and L. Stryer Biochemistry 5th ed. 2002 W.H. Freeman and Company New York
2. S.M. Fitzpatrick, A.J. Cooper, and T.E. Duffy Use of beta-methylene-d,l- aspartate to assess the role of aspartate aminotransferase in cerebral oxidative metabolism J Neurochem 41 1983 1370 1383
3. J.C. Lai, C.R. Murthy, A.J. Cooper, E. Hertz, and L. Hertz Differential effects of ammonia and beta-methylene-dl-aspartate on metabolism of glutamate and related amino acids by astrocytes and neurons in primary culture Neurochem Res 14 1989 377 389
4. A.J. Cheeseman, and J.B. Clark Influence of the malate-aspartate shuttle on oxidative metabolism in synaptosomes J Neurochem 50 1988 1559 1565
5. M. Ramos, A. del Arco, B. Pardo, A. Martinez-Serrano, J.R. Martinez-Morales, and K. Kobayashi Developmental changes in the Ca2+-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord Brain Res Dev Brain Res 143 2003 33 46
6. S.C. Dennis, and J.B. Clark The regulation of glutamate metabolism by tricarboxylic acid-cycle activity in rat brain mitochondria Biochem J 172 1978 155 162
7. N.H. Nguyen, A. Bråthe, and B. Hassel Neuronal uptake and metabolism of glycerol and the neuronal expression of mitochondrial glycerol-3-phosphate dehydrogenase J Neurochem 85 2003 831 842
8. K.F. LaNoue, and M.E. Tischler Electrogenic characteristics of the mitochondrial glutamate-aspartate antiporter J Biol Chem 249 1974 7522 7528
9. A. Del Arco, J. Morcillo, J.R. Martinez-Morales, C. Galian, V. Martos, and P. Bovolenta Expression of the aspartate/glutamate mitochondrial carriers aralar1 and citrin during development and in adult rat tissues Eur J Biochem 269 2002 3313 3320
10. 2+ within electropermeabilized insulin-secreting cells (INS-I) Biochim Biophys Acta 1175 1992 107 113
11. P.J. Leveille, J.F. McGinnis, D.S. Maxwell, and J. de Vellis Immunocytochemical localization of glycerol-3-phosphate dehydrogenase in rat oligodendrocytes Brain Res 196 1980 287 305
12. W. Cammer, D.S. Snyder, T.R. Zimmerman Jr., M. Farooq, and W.T. Norton Glycerol phosphate dehydrogenase, glucose-6-phosphate dehydrogenase, and lactate dehydrogenase: activities in oligodendrocytes, neurons, astrocytes, and myelin isolated from developing rat brains J Neurochem 38 1982 360 367
13. M.C. McKenna, J.T. Tildon, J.H. Stevenson, R. Boatright, and S. Huang Regulation of energy metabolism in synaptic terminals and cultured rat brain astrocytes: differences revealed using aninooxyacetate Dev Neurosci 15 1993 320 329
14. A. Atlante, S. Gagliardi, E. Marra, P. Calissano, and S. Passarella Glutamate neurotoxicity in rat cerebellar granule cells involves cytochrome c release from mitochondria and mitochondrial shuttle impairment J Neurochem 73 1999 237 246
15. H.S. Waagepetersen, H. Qu, A. Schousboe, and U. Sonnewald Elucidation of the quantitative significance of pyruvate carboxylation in cultured cerebellar neurons and astrocytes J Neurosci Res 66 2001 763 770
16. W.W. Wells, D.P. Xu, M.P. Washburn, H.K. Cirrito, and L.K. Olson Polyhydroxybenzoates inhibit ascorbic acid activation of mitochondrial glycerol-3-phosphate dehydrogenase. Implications for glucose metabolism and insulin secretion J Biol Chem 276 2001 2404 2410
17. A. Schousboe, J-Y. Wu, and E. Roberts Subunit structure and kinetic properties of 4-aminobutyrate-2-ketoglutarate transaminase from mouse brain J Neurochem 23 1974 1189 1195
18. J.Y. Wu, and E. Roberts Properties of brain l-glutamate decarboxylase: inhibition studies J Neurochem 23 1974 759 767
19. A.S. Bender, D.M. Woodbury, and H.S. White Beta-dl-methylene-aspartate, an inhibitor of aspartate aminotransferase, potently inhibits l-glutamate uptake into astrocytes Neurochem Res 14 1989 641 646
20. 14C]-labeled glutamate in astrocytes in primary cultures J Neurochem 39 1982 954 960
21. A.J. Cooper, S.M. Fitzpatrick, J.Z. Ginos, C. Kaufman, and P. Dowd Inhibition of glutamate-aspartate transaminase by beta-methylene-dl-aspartate Biochem Pharmacol 32 1983 679 689
22. 3H]aspartate from cultured cerebellar granule cells: The role of glutamate receptor activation coupled to reversal of the acidic amino acid plasma membrane carrier Neuroscience 50 1992 107 115
23. G. Palaiologos, L. Hertz, and A. Schousboe Evidence that aspartate aminotransferase activity and ketodicarboxylate carrier function are essential for biosynthesis of transmitter glutamate J Neurochem 51 1988 317 320
24. A.C.H. Yu, J. Drejer, L. Hertz, and A. Schousboe Pyruvate carboxylase activity in primary cultures of astrocytes and neurons J Neurochem 41 1983 1484 1487
25. T.A. Alston, L. Mela, and H.J. Bright 3-Nitropropionate, the toxic substance of Indigofera, is a suicide inactivator of succinate dehydrogenase Proc Natl Acad Sci 74 1977 3767 3771
26. J.B. Gramsbergen, M. Sandberg, B. Kornblit, and J. Zimmer Pyruvate protects against 3-nitropropionic acid neurotoxicity in corticostriatal slice cultures Neuroreport 11 2000 2743 2747
27. A. Atlante, L. de Bari, A. Bobba, E. Marra, P. Calissano, and S. Passarella Cytochrome c, released from cerebellar granule cells undergoing apoptosis or excitotoxic death, can generate protonmotive force and drive ATP synthesis in isolated mitochondria J Neurochem 86 2003 591 604
28. W. Loscher, M. Vetter, G. Bohme, and G. Stoltenburg-Didinger In vivo effects of anticonvulsant drugs on nerve terminal (synaptosomal) GABA levels in 11 brain regions of the rat J Neural Trans 63 1985 157 167
29. H.E. Scharfman Hyperexcitability of entorhinal cortex and hippocampus after application of aminooxyacetic acid (AOAA) to layer III of the rat medial entorhinal cortex in vitro J Neurophysiol 76 1996 2986 3001
30. D.H. Williamson, P. Lund, and H.A. Krebs The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver Biochem J 103 1967 514 527
31. M.C. McKenna, J.T. Tildon, J.H. Stevenson, and I.B. Hopkins Energy metabolism in cortical synaptic terminals from weanling and mature rat brain: Evidence for multiple compartments of tricarboxylic acid (TCA) cycle activity Dev Neurosci 16 1994 291 300
32. A.N. Murphy, G. Fiskum, and M.F. Beal Mitochondria in neurodegeneration: bioenergetic function in cell life and death J Cereb Blood Flow Metab 19 1999 231 245
33. M.F. Beal, K.J. Swartz, B.T. Hyman, E. Storey, S.F. Finn, and W. Koroshetz Aminooxyacetic acid results in excitotoxin lesions by a novel indirect mechanism J Neurochem 57 1991 1068 1073
34. G. Therrien, J.F. Giguere, and R.F. Butterworth Increased cerebrospinal fluid lactate reflects deterioration of neurological status in experimental portal-systemic encephalopathy Metab Brain Dis 6 1991 225 231
35. L. Faff-Michalak, and J. Albrecht Aspartate aminotransferase, malate dehydrogenase, and pyruvate carboxylase activities in rat cerebral synaptic and nonsynaptic mitochondria: effects of in vitro treatment with ammonia, hyperammonemia and hepatic encephalopathy Metab Brain Dis 6 1991 187 197
36. S. Surendran, K.M. Matalon, S. Szucs, S.K. Tyring, and R. Matalon Metabolic changes in the knockout mouse for Canavan's disease: implications for patients with Canavan's disease J Child Neurol 18 2003 611 615
37. M. Erecinska, and D. Nelson Effects of 3-nitropropionic acid on synaptosomal energy and transmitter metabolism: relevance to neurodegenerative brain diseases J Neurochem 63 1994 1033 1041
38. U. Sonnewald, L.R. White, E. Odegard, N. Westergaard, I.J. Bakken, and J. Aasly MRS study of glutamate metabolism in cultured neurons/glia Neurochem Res 121 1996 987 993
39. M.F. Beal, E. Brouillet, B. Jenkins, R. Henshaw, B. Rosen, and B.T. Hyman Age-dependent striatal excitotoxic lesions produced by the endogenous mitochondrial inhibitor malonate J Neurochem 61 1993 1147 1150
40. B. Hassel, and U. Sonnewald Selective inhibition of the tricarboxylic acid cycle of GABAergic neurons with 3-nitropropionic acid in vivo J Neurochem 65 1995 1184 1191
41. B. Hassel, and U. Sonnewald Glial formation of pyruvate and lactate from TCA cycle intermediates: implications for the inactivation of transmitter amino acids? J Neurochem 65 1995 2227 2234
42. I.J. Bakken, S.F. Johnsen, L.R. White, G. Unsgard, J. Aasly, and U. Sonnewald NMR spectroscopy study of the effect of 3-nitropropionic acid on glutamate metabolism in cultured astrocytes J Neurosci Res 47 1997 642 649
43. A. Almeida, J. Almeida, J.P. Bolanos, and S. Moncada Different responses of astrocytes and neurons to nitric oxide: The role of glycolytically generated ATP in astrocyte protection Proc Natl Acad Sci USA 98 2001 15294 15299
44. J.D. Cheng, A. Espinosa de los Monteros, and J. de Vellis Glial- and fat-specific expression of the rat glycerol phosphate dehydrogenase-luciferase fusion gene in transgenic mice J Neurosci Res 50 1997 300 311
45. R.S. Rust Jr., J.G. Carter, D. Martin, J.M. Nerbonne, P.A. Lampe, and M.E. Pusateri Enzyme levels in cultured astrocytes, oligodendrocytes and Schwann cells, and neurons from the cerebral cortex and superior cervical ganglia of the rat Neurochem Res 16 1991 991 999
46. 31P-n.m.r. study Biochem J 291 1993 915 919
47. A. Lu, Y. Tang, R. Ran, J.F. Clark, B.J. Aronow, and F.R. Sharp Genomics of the periinfarction cortex after focal cerebral ischemia J Cereb Blood Flow Metab 23 2003 786 810
48. M.C. McKenna, U. Sonnewald, X. Huang, J. Stevenson, and H.R. Zielke Exogenous glutamate concentration regulates the metabolic fate of glutamate in astrocytes J Neurochem 66 1996 386 393
49. M.C. McKenna, J.T. Tildon, J.H. Stevenson, and X. Huang New insights into the compartmentation of glutamate and glutamine metabolism in astrocytes Dev Neurosci 18 1996 380 390
50. 13C]glutamate Glia 17 1996 160 168
51. 13C NMR spectroscopy: incorporation of more label into lactate than into glutamine demonstrates the importance of the tricarboxylic acid cycle J Neurochem 61 1993 1179 1182
52. A.J. Cooper, and F. Plum Biochemistry and physiology of brain ammonia Physiol Rev 67 1987 440 519
53. M.A. Jalil, L. Begum, L. Contreras, B. Pardo, M. Iijima, and M.X. Li Reduced N-acetylaspartate levels in mice lacking aralar, a brain- and muscle-type mitochondrial aspartate-glutamate carrier J Biol Chem 280 2005 31333 31339