Regulation of glutamate-synthesizing enzymes by NMDA and potassium in cerebellar granule cells

European Journal of Neuroscience

Volumn 19, Issue 8, 2004, Pages 2030-2038

  Caballero Benítez, Andrea ^a   Alavez, Silvestre ^a   Uribe, Rosa María ^b   Morán, Julio ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Aspartate aminotransferase; Depolarization; Development; Glutaminase; Neuronal culture

Indexed keywords

ASPARTATE AMINOTRANSFERASE; GLUTAMIC ACID; GLUTAMINASE; MESSENGER RNA; MITOCHONDRIAL ENZYME; N METHYL DEXTRO ASPARTIC ACID; POTASSIUM CHLORIDE;

ANIMAL CELL; ARTICLE; CEREBELLUM; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME REGULATION; ENZYME SYNTHESIS; GRANULE CELL; MICHAELIS CONSTANT; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; ASPARTATE AMINOTRANSFERASES; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; GLUTAMIC ACID; GLUTAMINASE; N-METHYLASPARTATE; POTASSIUM CHLORIDE; RATS;

EID: 2342572890     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0953-816X.2004.03321.x     Document Type: Article

References (60)

1. Alavez, S., Gutierrez-Kobeh, L. & Morán, J. (1996) Characterization of the activation of glutaminase induced by N-Methyl-D-Aspartate and potassium in cerebellar granule cells. J. Neurosci. Res., 45, 637-646.
2. Alavez, S., Pedroza, D. & Morán, J. (2000) Role of heat-shock proteins in the effect of NMDA and KCl on cerebellar granule cells survival. Neurochem. Res., 25, 341-347.
3. Alavez, S., Pedroza, D. & Morán, J. (2003) Mechanisms of cell death by deprivation of depolarizing conditions during cerebellar granule neurons maturation. Neurochem. Int., 43, 581-590.
4. Aloisi, F., Ciotti, M.T. & Levi, G. (1985) Characterization of GABAergic neurons in cerebellar primary cultures and selective neurotoxicity of a serum fraction. J. Neurosci., 5, 2001-2008.
5. Altschuler, R.A., Monaghan, D.T., Haser, W.G., Wenthold, R.J., Curthoys, N.P. & Cotman, C.W. (1985) Immunocytochemical localization of glutaminase-like and aspartate aminotransferase-like immunoreactivities in the rat and guinea pig hippocampus. Brain Res., 330, 225-233.
6. Altschuler, R.A., Neises, G.R., Harmison, G.G., Wenthold, R.J. & Fex, J. (1981) Immunocytochemical localization of aspartate aminotransferase immunoreactivity in cochlear nucleus of the guinea pig. Proc. Natl Acad. Sci. USA, 78, 6553-6557.
7. Balàzs, R., Gallo, V. & Kingsbury, A. (1988a) Effect of depolarization on the maturation of cerebellar granule cells in culture. Dev. Brain. Res., 40, 269-279.
8. Balàzs, R., Hack, N. & Jorgensen, O.S. (1988b) Stimulation of the N-methyl-D-aspartate receptor has a trophic effect on differentiating cerebellar granule cells. Neurosci. Lett., 87, 80-86.
9. Balàzs, R., Jorgensen, O.S. & Hack, N. (1988c) N-methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neuroscience, 27, 437-451.
10. Balàzs, R., Hack, N. & Jorgensen, O.S. (1990) Selective stimulation of excitatory amino acid receptor subtypes and the survival of cerebellar granule cells in culture: effect of kainic acid. Neuroscience, 17, 251-258.
11. +-induced depolarization and NMDA treatment. Neuron, 12, 87-95.
12. Black, I.B. (1978) Regulation of autonomic development. Annu. Rev. Neurosci., 1, 182-214.
13. Bradford, 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.
14. Bradford, H.F., Ward, H.K. & Thomas, A.J. (1979) Glutamine as a major substrate for nerve-endings. J. Neurochem., 30, 1453-1459.
15. Bulleit, R.F., Cui, H., Wang, J.C. & Lin, X. (1994) NMDA receptor activation in differentiating cerebellar cell cultures regulates the expression of a new Pou gene, CNS-1. J. Neurosci., 14, 1584-1595.
16. Chomczsynski, P. & Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162, 156-159.
17. Cull Candy, S.G. & Ogden, D.C. (1985) Ion channels activated by 1-glutamate and GABA in cultured cerebellar neurons of the rat. Proc. R. Soc. Lond. B. Biol. Sci., 224, 367-373.
18. Daikhin, Y. & Yudkoff, M. (2000) Compartmentation of brain glutamate metabolism in neurons and glia. J. Nutr., 130, 1026S-1031S.
19. Didier, M., Roux, P., Piechaczyk, M., Mangeat, P., Devilliers, G., Bockaert, J. & Pin, J.P. (1992) Long-term expression of the c-fos protein during in vitro differentiation in cerebellar granule cells induced by potassium or NMDA. Brain. Res. Mol. Brain. Res., 12, 249-258.
20. Erakovic, V., Zupan, G., Varljen, J., Laginja, J. & Simonic, A. (2001) Altered activities of rat brain metabolic enzymes in electroconvulsive shock-induced seizures. Epilepsia, 42, 181-189.
21. Fonnum, F. (1984) Glutamate: a neurotransmitter in mammalian brain. J. Neurochem., 42, 1-11.
22. Gallo, G., Ciotti, M.T., Aloisi, F. & Levi, G. (1986) Developmental features of rat cerebellar neural cells cultured in a chemically defined medium. J. Neurosci. Res., 15, 289-301.
23. Gallo, V., Kingsbury, A., Balàzs, R. & Jorgensen, O.S. (1987) The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J. Neurosci., 7, 2203-2213.
24. Gianfreda, L., Marino, G., Palescandolo, R. & Scardi, V. (1974) Effect of pH, ionic strength and univalent inorganic ions on the reconstitution of aspartate aminotransferase. Biochem. J., 137, 199-203.
25. Harlow, E.D. & Lane, D. (1988) Antibodies: a Laboratory Manual. Cold Spring Harbor Press, New York.
26. Hudson, D.B., Balcana, T., Bean, G. & Timiras, P.A. (1976) Glutamic acid: a strong candidate as the transmitter of the cerebellar granule cells. Neurochem. Res., 1, 73-81.
27. Juretić N., Mattes, U., Ziak, M., Chirsten, P. & Jaussi, R. (1990) Structure of the genes of two homologous intracellularly heterotopic isoenzymes, Cytosolic and mitochondrial aspartate aminotransferase of chicken. Eur. J. Biochem., 192, 119-126.
28. Kingsbury, A., Gallo, V., Woodhams, P.L. & Balàzs, R. (1985) Survival, morphology and adhesion properties of cerebellar interneurones cultured in chemically defined and serum-supplemented medium. Dev. Brain Res., 17, 17-25.
29. Kvamme, E., Svenneby, G., Hertz, L. & Schousboe, A. (1982) Properties of phosphate-activated glutaminase in astrocytes cultured from mouse brain. Neurosci. Res., 7, 761-760.
30. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage. Nature, 227, 680-685.
31. Lai, J.C.K., Murthy, C.R.K., Cooper, A.J.L., Hertz, E. & Hertz, L. (1989) Differential effects of ammonia and β-methylene-DL-aspartate on metabolism of glutamate and related amino acids by astrocytes and neurons in primary culture. Neurochem. Res., 14, 377-389.
32. LaNoue, K.F., Berkich, D.A., Conway, M., Barber, A.J., Hu, L.Y., Taylor, C. & Hutson, S. (2001) Role of specific aminotransferases in de novo glutamate synthesis and redox shuttling in the retina. J. Neurosci. Res., 66, 914-922.
33. Lasher, J. & Zagon, R. (1972) The effect of potassium on neuronal differentiation in cultures of dissociated newborn rat cerebellum. Brain Res., 7, 761-770.
34. Magee, S.C. & Phillips, A.T. (1971) Molecular properties of the multiple aspartate aminotransferases purified from rat brain. Biochemistry, 10, 3397-3405.
35. Mattson, M.P. & Hauser, K.F. (1991) Spatial and temporal integration of neurotransmitter signals in the development of neural circuitry. Neurochem. Int., 19, 17-24.
36. McKenna, M.C., Stevenson, J.H., Huang, X. & Hopkins, I.B. (2000) Differential distribution of the enzymes glutamate dehydrogenase and aspartate aminotransferase in cortical synaptic mitochondria contributes to metabolic compartmentation in cortical synaptic terminals. Neurochem. Int., 37, 229-241.
37. Meier, E., Hertz, L. & Schousboe, A. (1991) Neurotransmitters as developmental signals. Neurochem. Int., 19, 1-15.
38. Morán, J., Alavez, S., Rivera-Gaxiola, M., Valencia, A. & Hurtado, S. (1999a) Effect of NMDA antagonists on the activity of glutaminase and aspartate aminotransferase in the developing rat cerebellum. Int. J. Dev. Neurosci., 17, 57-65.
39. Morán, J., Itho, T., Reddy, U.R., Chen, M., Alnemri, E. & Pleasure, D. (1999b) Caspase-3 expression by cerebellar granule neurons is regulated by calcium and cyclic AMP. J. Neurochem., 73, 568-577.
40. Morán, J. & Patel, A.J. (1989a) Effect of potassium depolarization on phosphate-activated glutaminase activity in primary cultures of cerebellar granule neurons and astroglial cells during development. Dev. Brain. Res., 46, 97-105.
41. Morán, J. & Patel, A.J. (1989b) Stimulation of the N-methyl-D- aspartate receptor promotes the biochemical differentiation of cerebellar granule neurons and not astrocytes. Brain. Res., 486, 15-25.
42. Morán, J. & Rivera-Gaxiola, M. (1992) Effect of potassium and NMDA on the aspartate aminotransferase activity in cultured cerebellar granule cells. J. Neurosci. Res., 33, 239-247.
43. Mossman, T. (1983) Rapid colorimetric assay of cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Meth., 65, 55-63.
44. Nissim, I. (1999) Newer aspects of glutamine/glutamate metabolism: the role of acute pH changes. Am. J. Physiol., 277 (Renal Physiol., 46), F493-F497.
45. Palaiologos, G., Hertz, L. & Schousboe, A. (1988) Evidence that aspartate aminotransferase activity and ketodicarboxylate carrier function are essential for biosynthesis of transmitter glutamate. J. Neurochem., 51, 317-320.
46. Palaiologos, G., Hertz, L. & Schousboe, A. (1989) Role of aspartate aminotransferase and mitochondrial dicarboxylate transport for release of endogenously and exogenously supplied neuro-transmitter in glutamatergic neurons. Neurochem. Int., 14, 359-366.
47. Parli, J.A., Godfrey, D.A. & Ross, C.D. (1987) Separate enzymatic microassays for aminotransferase isoenzymes. Biochim. Biophys. Acta, 925, 175-184.
48. Patel, A.J., Hunt, A., Gordon, R.D. & Balàzs, R. (1982) The activities in different neural cell types of certain enzymes associated with the metabolic compartamentation of glutamate. Dev. Brain Res., 4, 3-11.
49. Patel, A.J., Hunt, A. & Hayashi, M. (1987) Effect of thyroid deficiency on the regional development of glutaminase, a glutamatergic neuron marker in the rat brain. Int. J. Dev. Neurosci., 5, 295-303.
50. Sakurai, H., Kurusu, R., Sano, K., Tsuchiya, T. & Tsuda, M. (1992) Stimulation of cultured cerebellar granule cells via glutamate receptor induces TRE- and CKE- binding activities mediated by common DNA-binding complexes: J. Neurochem., 59, 2067-2075.
51. Schousboe, A. (1987) An overview of the biochemistry and pharmacology of glutamic and GABAergic neurotransmission. Biochem. Soc. Trans., 15, 205-208.
52. Schousboe, A., Westergaard, N., Waagrepetersen, H.S., Larsson, O.M., Bakken, I.J. & Sonnewald, U. (1997) Trafficking between glia and neurons of TCAcycle intermediates and relatedmetabolites. Glia, 21, 99-105.
53. Schwartz, J.P. (1992) Neurotransmitters as neurotrophic factors: a new set of functions. Int. Rev. Neurobiol., 34, 1-23.
54. Sciancalepore, M., Forti, L. & Morán, O. (1989) Changes of N-methyl-D-aspartate activated channels of cerebellar granule cells with days in culture. Biochem. Biophys. Res. Comm., 165, 481-487.
55. Somogyi, P., Halasy, K., Somogyi, J., Storm-Mathisen, J. & Ottersen, O.P. (1986) Quantification of immunogold labeling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience, 19, 1045-1050.
56. Sonnewald, U., Westergaard, N., Petersen, S.B., Unsgard, G. & Schousboe, A. (1993) Metabolism of [U-13C]glutamate in astrocytes studied by 13C NMR spectroscopy: incorporation of more label into lactate than into glutamine demonstrates the importance of the tricarboxylic acid cycle. J. Neurochem., 61, 1179-1182.
57. Toescu, E.C. (1999) Activity of voltage-operated calcium channels in rat cerebellar granule neurons and neuronal survival. Neuroscience, 94, 561-570.
58. Waagepetersen, H.S., Sonnewald, U., Larsson, O.M. & Schousboe, A. (2000) Compartmentation of TCA cycle metabolism in cultured neocortical neurons revealed by 13C MR spectroscopy. Neurochem. Int., 36, 349-358.
59. Wenthold, R.J., Skaggs, K.K. & Altschuler, R.A. (1986) Immunocytochemical localization of aspartate aminotransferase and glutaminase immunoreactivities in the cerebellum. Brain. Res., 363, 371-375.
60. Yudkoff, M., Nissim, I. & Pleasure, D. (1988) Astrocyte metabolism of 15N-glutamine: implications for the glutamine-glutamate cycle. J. Neurochem., 51, 843-850.