EFFECTS OF GLUTAMATE TRANSPORT SUBSTRATES AND GLUTAMATE RECEPTOR LIGANDS ON THE ACTIVITY OF Na+/K+-ATPase IN BRAIN TISSUE IN VITRO (original) (raw)

2004, Clinical and Experimental Pharmacology and Physiology

Abstract

1. It has been suggested that Na + /K + -ATPase and Na +dependent glutamate transport (GluT) are tightly linked in brain tissue. In the present study, we have investigated Na + /K + -ATPase activity using Rb + uptake by 'minislices' (prisms) of the cerebral cortex. This preparation preserves the morphology of neurons, synapses and astrocytes and is known to possess potent GluT that has been well characterized. Uptake of Rb + was determined by estimating Rb + in aqueous extracts of the minislices, using atomic absorption spectroscopy.

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References (56)

  1. Danbolt NC. Glutamate uptake. Prog. Neurobiol. 2001; 65: 1-105.
  2. Vandenberg RJ. Molecular pharmacology and physiology of glutamate transporters in the central nervous system. Clin. Exp. Pharmacol. Physiol. 1998; 25: 393-400.
  3. Balcar VJ. Molecular pharmacology of the Na + -dependent transport of acidic amino acids in the mammalian central nervous system. Biol. Pharm. Bull. 2002; 25: 291-301.
  4. O'Shea RD. Roles and regulation of glutamate transporters in the central nervous system. Clin. Exp. Pharmacol. Physiol. 2002; 29: 1018-23.
  5. Rae C, Lawrance ML, Dias LS, Provis T, Bubb WA, Balcar VJ. Strategies for studies of neurotoxic mechanisms involving deficient glutamate transport of L-glutamate: Antisense knockout in rat brain in vivo and changes in neurotransmitter metabolism following inhibition of glutamate transport in guinea pig brain slices. Brain Res. Bull. 2000; 53: 373-81.
  6. Rae C, Hare N, Bubb WA et al. Inhibition of glutamine transport depletes glutamate and GABA neurotransmitter pools: Further evidence for metabolic compartmentation. J. Neurochem. 2003; 85: 503-14.
  7. Moussa CE-H, Mitrovic AD, Vandenberg RJ et al. Effects of L-glutamate transport inhibition by a conformationally restricted glutamate analogue (2S,1ЈS,2ЈR)-2-(carboxycyclopropyl)-glycine (L-CCG III) on metabolism in brain tissue in vitro analysed by NMR spectroscopy. Neurochem. Res. 2002; 27: 27-35.
  8. Blitzblau R, Gupta S, Djali S, Robinon M, Rosenberg PA. The glutamate transport inhibitor 1-trans-pyrrolidine-2,4-dicarboxylate indirectly evokes NMDA receptor mediated neurotoxicity in rat cortical cultures. Eur. J. Neurosci. 1996; 8: 1840-52.
  9. Rothstein JD, Dykes-Hoberg M, Pard CA et al. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996; 16: 675-86.
  10. Sanchez-Carbente MR, Massieu L. Transient inhibition of glutamate uptake in vivo induces neurodegeneration when energy metabolism is impaired. J. Neurochem. 1999; 72: 129-38.
  11. Garcia O, Massieu L. Strategies for neuroprotection against 1-trans-pyrrolidine-2,4-dicarboxylate-induced neuronal damage during energy impairment in vitro. J. Neurosci. Res. 2001; 64: 418-28.
  12. Robinson MB, Dowd LA. Heterogeneity and functional subtypes of Na + -dependent glutamate transporters in the mammalian CNS. Adv. Pharmacol. 1997; 37: 69-115.
  13. Danbolt NC. Sodium-and potassium-dependent excitatory amino acid transporters in brain plasma membranes. In: Björklund A, Hökfelt T (eds). Handbook of Chemical Neuroanatomy, Vol. 18: Glutamate. Elsevier, Amsterdam. 2000; 231-54.
  14. Hertz L, Dringen R, Schousboe A, Robinson SR. Minireview. Astrocytes: Glutamate producers for neurons. J. Neurosci. Res. 1999; 57: 417-28.
  15. Chatton J-Y, Marquet P, Magistretti PJ. A quantitative analysis of L-glutamate-regulated Na + dynamics in mouse cortical astrocytes: Implications for cellular bioenergetics. Eur. J. Neurosci. 2000; 12: 3843-53.
  16. Balcar VJ, Johnston GAR. The structural specificity of the high affinity uptake of L-glutamate and L-aspartate by rat brain slices. J. Neurochem. 1972; 19: 2657-66.
  17. Balcar VJ, Borg J, Mandel P. High affinity uptake of L-glutamate and L-aspartate by glial cells. J. Neurochem. 1977; 28: 87-93.
  18. Pellerin L, Magistretti PJ. Glutamate uptake stimulates Na + ,K + - ATPase activity in astrocytes via activation of a distinct subunit highly sensitive to ouabain. J. Neurochem. 1997; 69: 2132-7.
  19. Balcar VJ, Takamoto A, Yoneda Y. Neurochemistry of L-glutamate transport in the CNS. A review of thirty years of progress. Collect. Czech. Chem. Commun. 2001; 66: 1315-40.
  20. Mcilwain H, Bachelard H. Biochemistry and the Central Nervous System. Churchill Livingstone, Edinburgh. 1985.
  21. Badar-Goffer R, Bachelard H, Morris P. Cerebral metabolism of acetate and glucose studied by 13 C NMR spectroscopy. Biochem. J. 1990; 266: 133-9.
  22. Balcar VJ, Johnston GAR. Ontogeny of high affinity uptake of GABA studied in 'minislices' (tissue prisms) of rat cerebral cortex. Dev. Brain Res. 1989; 49: 295-9.
  23. Balcar VJ, Damm S, Wolff JR. Ontogeny of K + -stimulated release of [ 3 H]GABA in rat cerebral cortex studied by a simple technique in vitro. Neurochem. Int. 1986; 8: 573-80.
  24. Balcar VJ, Johnston GAR. Liberation of amino acids during the preparation of brain slices. Brain Res. 1975; 83: 173-5.
  25. Munson PJ, Rodbard D. LIGAND. A versatile computerized approach for characterization of ligand-binding systems. Anal. Biochem. 1980; 107: 220-39.
  26. McGonigle P, Molinoff PB. Quantitative aspects of drug-receptor interactions. In: Siegel GJ, Agranoff BW, Albers RW, Molinoff PB (eds). Basic Neurochemistry. Raven Press, New York. 1989; 183-202.
  27. Shimamoto K, Lebrun B, Yasuda-Kamatani Y et al. DL-threo-␤- Benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol. Pharmacol. 1998; 53: 195-201.
  28. Bridges RJ, Lovering FE, Koch H, Cotman CW, Chamberlain AR. A conformationally constrained competitive inhibitor of the Na + - dependent transporter in the forebrain synaptosomes: 1-anti,endo-3,4- Methanopyrrolidine dicarboxylate. Neurosci. Lett. 1994; 174: 193-7.
  29. Bridges RJ, Stanley MS, Anderson MW, Cotman CW, Chamberlain AR. Conformationally defined neurotransmitter analogues. Selective inhibition of glutamate uptake by one pyrrolidine-2,4-dicarboxylate diastereoisomer. J. Med. Chem. 1991; 34: 717-25.
  30. Bridges RJ, Kavanaugh MP, Chamberlain AR. A pharmacological review of competitive inhibitors and substrates of high affinity, sodium dependent glutamate transport in the central nervous system. Curr. Pharm. Des. 1999; 5: 363-79.
  31. Shimamoto K, Ohfune Y. Syntheses and conformational analyses of glutamate analogs: 2-(2-Carboxy-3-substituted-cyclopropyl) glycines as useful probes for excitatory amino acid receptors. J. Med. Chem. 1996; 39: 407-23.
  32. Nakamura Y, Kataoka K, Ishida M, Shinozaki H. (2S,3S,4R)-2- (Carboxycyclopropyl) glycine, a potent and competitive inhibitor of both glial and neuronal uptake of glutamate. Neuropharmacology 1993; 32: 833-7.
  33. Stanton D, Liao L, Rae C, Bubb WA, Moussa CE-H, Balcar VJ. Can inhibition of glutamate transport contribute to the action of neuro- leptics? Psychiatrie 2003; 7: 6-11.
  34. Balcar VJ, Johnston GAR, Twitchin B. Stereospecificity of the inhibition of L-glutamate and L-aspartate high affinity uptake in rat brain slices by threo-3-hydroxyaspartate. J. Neurochem. 1977; 28: 1145-6.
  35. Johnston GAR, Kennedy SME, Twitchin B. Action of neurotoxin kainic acid on high affinity uptake of L-glutamic acid in rat brain slices. J. Neurochem. 1979; 32: 121-8.
  36. Cooper B, Chebib M, Shen J et al. Structural selectivity and molecular nature of L-glutamate transport in cultured human fibroblasts. Arch. Biochem. Biophys. 1998; 353: 356-64.
  37. Takamoto A, Quiggin LB, Lieb I, Shave E, Balcar VJ, Yoneda Y. Differences between D-and L-aspartate binding to the Na + -dependent binding sites on glutamate transporters in frozen sections of rat brain. Life Sci. 2002; 70: 991-1001.
  38. Ransnas LA, Motulsky HJ. Fitting curves to data using non-linear regression. A practical and non-mathematical review. FASEB J. 1987; 1: 365-74.
  39. Yamada KA, Tang C-M. Benzothiadiazides inhibit rapid glutamate desensitization and enhance rapid glutamatergic synaptic currents. J. Neurosci. 1993; 13: 3904-15.
  40. Zorumski CF, Yamada KA, Price MT, Olney JW. A benzodiazepine recognition site associated with the non-NMDA glutamate receptor. Neuron 1993; 10: 61-7.
  41. Schoepp DD, Smith CG, Lodge D et al. L-(Tetrazol-5-yl) glycine. A novel and highly potent NMDA receptor agonist. Eur. J. Pharmacol. 1991; 203: 237-43.
  42. Neale JH, Bzdega T, Wroblewska B. N-Acetylaspartylglutamate: The most abundant peptide neurotransmitter in the mammalian central nervous system. J. Neurochem. 2000; 75: 553-62.
  43. De Blasi A, Conn PJ, Pin J-P, Nicoletti F. Molecular determinants of metabotropic glutamate receptor signalling. Trends Pharmacol. Sci. 2001; 22: 114-19.
  44. Sweadner KJ. Isozymes of Na + ,K + -ATPase. Biochim. Biophys. Acta 1985; 988: 185-220.
  45. Blanco G, Mercer RW. Isoenzymes of Na + ,K + -ATPase, heterogeneity in structure, diversity and function. Am. J. Physiol. 1998; 275: F633-50.
  46. O'Brien JW, Lingrel LB, Wallick ET. Ouabain binding kinetics of the rat alpha 2 and alpha 3 isoforms of the Na + ,K + -ATPase. Arch. Biochem. Biophys. 1994; 310: 32-9.
  47. Sweadner KJ. Na + ,K + -ATPase isozymes in neurons and glia. Can. J. Physiol. Pharmacol. 1992; 70 (Suppl.): S255-9.
  48. Cameron R, Klein L, Shyjan LW, Rakic P, Levenson R. Neurons and astroglia express distinct subsets of the Na + ,K + -ATPase ␣ and ␤ subunits. Mol. Brain. Res. 1994; 21: 599-603.
  49. Balcar VJ, Schousboe A, Spoerri PE, Wolff JR. Differences between substrate specificities of L-glutamate uptake by neurons and glia, studied in cell lines and primary cultures. Neurochem. Int. 1987; 10: 213-18.
  50. Abe K, Saito H. Involvement of Na + ,K + pump in L-glutamate clearance by cultured rat cortical astrocytes. Biol. Pharm. Bull. 2000; 23: 1051-4.
  51. Casale CH, Previtali G, Barra HS. Involvement of acetylated tubulin in the regulation of Na + ,K + -ATPase activity in cultured astrocytes. FEBS Lett. 2003; 534: 115-18.
  52. Cholet N, Pellerin L, Magistretti PJ, Hamel E. Similar perisynaptic glial localization for the Na + ,K + -ATPase alpha 2-subunit and the glutamate transporters GLAST and GLT in the rat somatosensory cortex. Cereb. Cortex 2002; 12: 515-25.
  53. Cholet N, Pellerin L, Welker E et al. Local injection of antisense oligonucleotides targeted to the glial glutamate transporter GLAST decreases the metabolic response to somatosensory activation. J. Cereb. Blood Flow 2001; 21: 404-12.
  54. Balcar VJ. Effects of variations in ionic concentrations on high affinity uptake of L-glutamate in non-glutamatergic neurons and non-neuronal cells cultured from neonatal rat cortex. Neurochem. Internat 1991; 18: 43-9.
  55. Gottlieb M, Wang Y, Teichberg VI. Blood-mediated scavenging of cerebrospinal fluid glutamate. J. Neurochem. 2003; 87: 119-26.
  56. Pliss L, S ˇkultétyová I, Jez ˇová D, Balcar VJ, S ˇt'astný F. N-Acetyl-L- aspartyl-L-glutamate (NAAG) changes functional and structural properties of rat blood-brain barrier. Neurosci. Lett. 2002; 317: 85-8.