Glutamic acid decarboxylase-expressing astrocytes exhibit enhanced energetic metabolism and increase PC12 cell survival under glucose deprivation

Journal of Neurochemistry

Volumn 75, Issue 1, 2000, Pages 56-64

  Bellier, J P ^a   Sacchettoni, S ^a   Prod'hon, C ^a   Perret Liaudet, A ^b   Belin, M F ^a   Jacquemont, B ^a,c  

^a INSERM   (France)

^b Hop Neurologique Wertheimer   (France)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

Energetic metabolism; Glutamic acid decarboxylase transgene; Neuroprotection; PC12 cells

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; ADENOSINE TRIPHOSPHATE; GLUCOSE; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; LACTIC ACID;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL KINETICS; CELL METABOLISM; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; ENERGY METABOLISM; GENE EXPRESSION; GLUCOSE METABOLISM; NEUROPROTECTION; NEWBORN; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; RAT; TRANSGENE;

ADENOSINE TRIPHOSPHATE; ANIMALS; ASTROCYTES; CELL LINE, TRANSFORMED; CELL SURVIVAL; CULTURE MEDIA, CONDITIONED; ENERGY METABOLISM; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; GLUCOSE; GLUTAMATE DECARBOXYLASE; GLYCOGEN; ISOENZYMES; LACTIC ACID; PC12 CELLS; PYRUVIC ACID; RATS; TRANSFECTION;

ANIMALIA;

EID: 0034046910     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.0750056.x     Document Type: Article

References (61)

1. Alliot F. and Pessac B. (1984) Astrocytic cell clones derived from established cultures of 8 day postnatal mouse cerebella. Brain Res. 306, 283-291.
2. 13C NMR spectroscopy. Neuroreport 6, 2201-2204.
3. 13C) glutamate metabolism in astrocytes during hypoglycemia and hypoxia. J. Neurosci. Res. 51, 636-645.
4. Balázs R., Machiyama Y., Hammond B. J., Julian T., and Richter D. (1970) The operation of the gamma-aminobutyrate bypath of the tricarboxylic acid cycle in brain tissue in vitro. Biochem. J. 116, 445-467.
5. Bartlett W. P. and Banker G. A. (1984) An electron microscopic study of the development of axon and dendrites by hippocampal neurons in culture. I. Cells which develop without intercellular contacts. J. Neurosci. 4, 1944-1953.
6. Berridge M. V. and Tan A. S. (1993) Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch. Biochem. Biophys. 303, 474-482.
7. Blakemore W. F. and Franklin R. J. M. (1991) Transplantation of glial cells into the CNS. Trends Neurosci. 14, 323-327.
8. Bradford M. M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
9. Bröer S., Rahman B., Pellegri G., Pellerin L., Martin J. L., Verleysdonk S., Hamprecht B., and Magistretti P. J. (1997) Comparison of lactate transport in astroglial cells and monocarboxylate transporter 1 (MCT1) expressing Xenopus laevis oocytes. J. Biol. Chem. 272, 30096-30102.
10. DeLuca M. and McElroy W. D. (1984) Two kinetically distinguishable ATP sites in firefly luciferase. Biochem. Biophys. Res. Commun. 123, 764-770.
11. Demestre M., Boutelle M., and Fillenz M. (1997) Stimulated release of lactate in freely moving rats is dependent on the uptake of glutamate. J. Physiol. (Lond.) 499, 825-832.
12. de Montigny P., Stobaugh J. F., Givens R. S., Carlson R. G., Srinivasackar K., Sternson L. A., and Higuchi T. (1987) Naphthalene-1,3-dicarboxaldehyde/cyanide ion: a rationally designated fluorogenic reagent for primary amines. Anal. Chem. 79, 1096-1101.
13. Denner L. A. and Wu J.-Y. (1985) Two forms of rat brain glutamic acid decarboxylase differ in their dependence on free pyridoxal phosphate. J. Neurochem. 44, 957-965.
14. Desagher S., Glowinski J., and Premont J. (1997) Pyruvate protects neurons against hydrogen peroxide-induced toxicity. J. Neurosci. 17, 9060-9067.
15. Erecińska M. and Silver I. A. (1990) Metabolism and role of glutamate in mammalian brain. Prog. Neurobiol. 35, 245-296.
16. Erecińska M., Nelson D., Daikhin Y., and 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.
17. Erlander M. G., Tillakaratne N. J. K., Feldblum S., Patel N., and Tobin A. J. (1991) Two distinct glutamate decarboxylases. Neuron 7, 91-100.
18. Geng M.-Y., Saito H., and Nishiyama N. (1997) Protective effects of pyridoxal phosphate against glucose deprivation-induced damage in cultured hippocampal neurons. J. Neurochem. 68, 2500-2506.
19. Gorovits R., Avidan N., Avisar N., Snaked I., and Vardimon L. (1997) Glutamine synthetase protects against neuronal degeneration in injured retinal tissue. Proc. Natl. Acad. Sci. USA 94, 7024-7029.
20. Greene L. A. and Tischler A. S. (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl Acad. Sci. USA 73, 2424-2428.
21. 3H) GABA from hippocampal neurons in primary culture. Brain Res. 482, 23-33.
22. Hassel B., Bachelard H., Jones P., Fonnum F., and 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, 1230-1238.
23. Hassel B., Johannessen C. U., Sonnewald U., and Fonnum F. (1998) Quantification of the GABA shunt and the importance of the GABA shunt versus the 2-oxoglutamate dehydrogenase pathway in GABAergic neurons. J. Neurochem. 71, 1511-1518.
24. Ho D. Y., Saydam T. C., Fink S. L., Lawrence M. S., and Sapolsky R. M. (1995) Detective herpes simplex virus vectors expressing the rat brain glucose transporter protect cultured neurons from necrotic insults. J. Neurochem. 65, 842-850.
25. Izumi Y., Benz A. M., Zorumski C. F., and Olney J. W. (1994) Effects of lactate and pyruvate on glucose deprivation in rat hippocampal slices. Neuroreport 5, 617-620.
26. Izumi Y., Benz A. M., Katsuki H., and Zorumski C. F. (1997) Endogenous monocarboxylates sustain hippocampal synaptic function and morphological integrity during energy deprivation. J. Neurosci. 17, 9448-9457.
27. La Gamma E. F., Weisinger G., Lenn N. J., and Strecker R. E. (1993) Genetically modified primary astrocytes as cellular vehicles for gene therapy in the brain. Cell Transplant. 2, 207-214.
28. Larsson O. M., Gram L., Schousboe I., and Schousboe A. (1986) Differential effects of gamma-vinyl GABA and valproate on GABA-transaminase from cultured neurons and astrocytes. Neuropharmacology 25, 617-625.
29. Lawrence M. S., Ho D. Y., Dash R., and Sapolsky R. M. (1995) Herpes simplex virus vectors overexpressing the glucose transporter gene protect against seizure-induced neuron loss. Proc. Nail. Acad. Sci. USA 92, 7247-7251.
30. Löscher W. (1980) Effect of inhibitors of GABA transaminase on the synthesis, binding, uptake, and metabolism of GABA. J. Neurochem. 34, 1603-1608.
31. Lowry O. H., Rosebrough N. J., Farr A. L., and Randall R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
32. Mattson M. P., Zhang Y., and Bose S. (1993) Growth factors prevent mitochondrial dysfunction, loss of calcium, homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp. Neurol 121, 1-13.
33. McKenna M. C., Sonnewald U., Huang X., Stevenson J., and Zielke H. R. (1996) Exogenous glutamate concentration regulates the metabolic fate of glutamate in astrocytes. J. Neurochem. 66, 386-393.
34. McKenna M. C., Sonnewald U., and Johnsen S. F. (1998) γ-Aminobutyric acid (GABA) modulates glutamate metabolism in astrocytes. (Abstr.) J. Neurochem. 70 (Suppl.), S19A.
35. Meier T. J., Ho D. Y., and Sapolsky R. M. (1997) Increased expression of calbindin D28k via herpes simplex virus amplicon vector decreases calcium ion mobilization and enhances neuronal survival after hypoglycemic challenge. J. Neurochem. 69, 1039-1047.
36. Mosmann T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
37. Mucke L., OIdstone M. B. A., Morris J. C., and Nerenberg M. I. (1991) Rapid activation of astrocyte-specific expression of GFAP-lacZ transgene by focal injury. New Biol. 3, 465-474.
38. Paulsen R. E. and Fonnum F. (1988) Regulation of transmitter γ-aminobutyric acid (GABA) synthesis and metabolism illustrated by the effect of γ-vinyl GABA and hypoglycemia. J. Neurochem. 50, 1151-1157.
39. Pellerin L. and Magistretti P. J. (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. USA 91, 10625-10629.
40. Pellerin L., Stolz M. T., Sorg O., Martin J. L., Deschepper C. F., and Magistretti P. J. (1997) Regulation of energy metabolism by neurotransmitters in astrocytes in primary cultures and in an immortalized cell line. Glia 21, 74-83.
41. Pereira C., Santos M. S., and Oliveira C. (1998) Metabolic inhibition increases glutamate susceptibility on a PC12 cell line. J. Neurosci. Res. 51, 360-370.
42. Porter T. G., Spink D. C., Martin S. B., and Martin D. L. (1985) Transaminations catalysed by brain glutamate decarboxylase. Biochem. J. 231, 705-712.
43. Ridet J. L., Malhotra S. K., Privat A., and Gage F. H. (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20, 570-577.
44. Rothstein J. D., Martin L., Levey A. I., Dykes-Hoberg M., Jin L., Wu D., Nash N., and Kuncl R. W. (1994) Localization of neuronal and glial glutamate transporters. Neuron 13, 713-725.
45. Sacchettoni S. A., Benchaibi M., Sindou M., Belin M. F., and Jacquemont B. (1998) Glutamate-modulated production of GABA in immortalized astrocytes transduced by a glutamic acid decarboxylase-expressing retrovirus. Glia 22, 86-93.
46. Saji M. and Reis D. J. (1987) Delayed transneuronal death of substantia nigra neurons prevented by γ-aminobutyric acid agonist. Science 235, 66-69.
47. +ATPase in mammalian astrocytes. Glia 21, 35-45.
48. Sonnewald U., Westergaard N., and Schousboe A. (1997) Glutamate transport and metabolism in astrocytes. Glia 21, 56-63.
49. Stanimirovic D., Ball R., and Durkin J. P. (1997) Stimulation of glutamate uptake and Na,K-ATPase activity in rat astrocytes exposed to ischemia-like insults. Glia 19, 123-134.
50. Swanson R. A., Yu A. C. H., Chan P. H., and Sharp F. R. (1990) Glutamate increases glycogen content and reduces glucose utilization in primary astrocyte culture. J. Neurochem. 54, 490-496.
51. Tsacopoulos M. and Magistretti P. J. (1996) Metabolic coupling between glia and neurons. J. Neurosci. 16, 877-885.
52. Walz W. and Mukerji S. (1988) Lactate release from astrocytes and neurons: a comparison. Glia 1, 366-370.
53. Waniewski R. A. and Martin D. L. (1986) Exogenous glutamate is metabolized to glutamine and exported by rat primary astrocyte cultures. J. Neurochem. 47, 304-313.
54. 3H]aminobutyric acid from striatal neurons in primary culture. J. Neurochem. 51, 435-441.
55. Westergaard N., Larsson O. M., Jensen B., and Schousboe A. (1992) Synthesis and release of GABA in cerebral co-cultured with astrocytes from cerebral cortex or cerebellum. Neurochem. Int. 20, 567-575.
56. Westergaard N., Sonnewald U., and Schousboe A. (1995) Metabolic trafficking between neurons and astrocytes: the glutamate/glutamine cycle revisited. Dev. Neurosci. 17, 203-211.
57. 13C glutamate. Glia 17, 160-168.
58. Wiesinger H., Hamprecht B., and Dringen R. (1997) Metabolic pathways for glucose in astrocytes. Glia 21, 22-34.
59. Wood T. (1968) The inhibition of pyruvate kinase by ATP. Biochem. Biophys. Res. Commun. 31, 779-785.
60. Yu A. C. H., Lee Y. L., and Eng L. F. (1992) Glutamate as an energy substrate for neuronal-astrocytic interactions. Prog. Brain Res. 94, 251-259.
61. 15N) glutamate by cultured astrocytes. Biochem. J. 234, 185-192.