Compromised glutamate transport in human glioma cells: Reduction- mislocalization of sodium-dependent glutamate transporters and enhanced activity of cystine-glutamate exchange

Journal of Neuroscience

Volumn 19, Issue 24, 1999, Pages 10767-10777

  Ye, Zu Cheng ^a   Rothstein, Jeffrey D ^b   Sontheimer, Harald ^a  

^a University of Alabama at Birmingham   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brain tumor; Cystine glutamate exchange; Epilepsy; Excitotoxicity; Glutamate release; Glutamate transporter; System x(c)

Indexed keywords

CYSTINE; GLUTAMIC ACID; SODIUM;

ARTICLE; ASTROCYTE; BRAIN TUMOR; CELL MEMBRANE TRANSPORT; EPILEPSY; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; NERVE CELL CULTURE; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; PRIORITY JOURNAL; SEIZURE;

EID: 0033573392     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-24-10767.1999     Document Type: Article

References (61)

1. Arriza JL, Eliasof S, Kavanaugh MP, Amara SG (1997) Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci USA 94:4155-4160.
2. Attwell D, Barbour B, Szatkowski M (1993) Nonvesicular release of neurotransmitter. Neuron 11:401-407.
3. Bannai S, Ishii T (1982) Transport of cystine and cysteine and cell growth in cultured human diploid fibroblasts: effect of glutamate and homocysteate. J Cell Physiol 112:265-272.
4. Bannai S, Ishii T (1988) A novel function of glutamine in cell culture: utilization of glutamine for the uptake of cystine in human fibroblasts. J Cell Physiol 137:360-366.
5. Bannai S, Kitamura E (1980) Transport interaction of L-cystine and L-glutamate in human diploid fibroblasts in culture. J Biol Chem 255:2372-2376.
6. Bergles DE, Jahr CE (1998) Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J Neurosci 18:7709-7716.
7. Bronfman M, Loyola G, Koenig CS (1998) Isolation of intact organelles by differential centrifugation of digitonin-treated hepatocytes using a table Eppendorf centrifuge. Anal Biochem 255:252-256.
8. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J (1995) Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711-720.
9. Cho Y, Bannai S (1990) Uptake of glutamate and cysteine in C6 glioma cells and in cultured astrocytes. J Neurochem 55:2091-2097.
10. Choi DW (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634.
11. Davis KE, Straff DJ, Weinstein EA, Bannerman PG, Correale DM, Rothstein JD, Robinson MB (1998) Multiple signaling pathways regulate cell surface expression and activity of the excitatory amino acid carrier 1 subtype of Glu transporter in C6 glioma. J Neurosci 18:2475-2485.
12. Fairman WA, Vandenberg RJ, Arriza JL, Kavanaugh MP, Amara SG (1995) An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375:599-603.
13. Fosse VM, Kolstad J, Fonnum F (1986) A bioluminescence method for the measurement of L-glutamate: applications to the study of changes in the release of 1-glutamate from lateral geniculate nucleus and superior colliculus after visual cortex ablation in rats. J Neurochem 47:340-349.
14. Haugeto O, Ullensvang K, Levy LM, Chaudhry FA, Honore T, Nielsen M, Lehre KP, Danbolt NC (1996) Brain glutamate transporter proteins form homomultimers. J Biol Chem 271:27715-27722.
15. Hertz L, Murthy CRK, Schousboe A (1988) Metabolism of glutamate and related amino acids. In: The biochemical pathology of astrocytes (Norenberg MD, Hertz L, Schousboe A, eds), pp 395-406. New York: Liss.
16. Kanai Y, Hediger MA (1992) Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360:467-471.
17. Kessler M, Baudry M, Lynch G (1987) Use of cystine to distinguish glutamate binding from glutamate sequestration. Neurosci Lett 81:221-226.
18. Kimelberg HK, Mongin AA (1998) Swelling-activated release of excitatory amino acids in the brain: Relevance for pathophysiology. Contrib Nephrol 123:240-257.
19. + in primary astrocyte cultures. J Neurosci 9:1141-1149.
20. Laake JH, Slyngstad TA, Haug F-MS, Ottersen OP (1995) Glutamine from glial cells is essential for the maintenance of the nerve terminal pool of glutamate: Immunogold evidence from hippocampal slice cultures. J Neurochem 65:871-881.
21. Lehre KP, Danbolt NC (1998) The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 18:8751-8757.
22. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC (1995) Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J Neurosci 15:1835-1853.
23. Levi G, Patrizio M (1992) Astrocyte heterogeneity: endogenous amino acid levels and release evoked by non-N-methyl-D-aspartate receptor agonists and by potassium-induced swelling in type-1 and type-2 astrocytes. J Neurochem 58:1943-1952.
24. Lipton SA, Rosenberg PA (1994) Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330:613-622.
25. Longuemare MC, Swanson RA (1995) Excitatory amino acid release from astrocytes during energy failure by reversal of sodium-dependent uptake. J Neurosci Res 40:379-386.
26. Magistretti PJ, Pellerin L, Rothman DL, Shulman RG (1999) Energy on demand. Science 283:496-497.
27. Murphy TH, Miyamoto M, Sastre A, Schnaar RL, Coyle JT (1989) Glutamate toxicity in a neuronal cell line involves inhibition of cystine transport leading to oxidative stress. Neuron 2:1547-1558.
28. Murphy TH, Schnaar RL, Coyle JT (1990) Immature cortical neurons are uniquely sensitive to glutamate toxicity by inhibition of cystine uptake. FASEB J 4:1624-1633.
29. Nicholls D, Attwell D (1990) The release and uptake of excitatory amino acids. Trends Pharmacol Sci 11:462-468.
30. Olney JW (1982) The toxic effects of glutamate and related compounds in the retina and the brain. Retina 2:341-359.
31. Paillas JE (1994) A review of 2,413 tumors operated over a 30-year period. J Neuroradiol 2:79-106.
32. Peghini P, Janzen J, Stoffel W (1997) Glutamate transporter EAAC-1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. EMBO J 16:3822-3832.
33. c in the macrophage-induced glutamate-dependent cytotoxicity to neurons. J Immunol 152:3578-3585.
34. Pines G, Danbolt NC, Bjoras M, Zhang Y, Bendahan A, Eide L, Koepsell H, Storm-Mathisen J, Seeberg E, Kanner BI (1992) Cloning and expression of a rat brain L-glutamate transporter. Nature 360:464-467.
35. Puka-Sundvall M, Gilland E, Bona E, Lehmann A, Sandberg M, Hagberg H (1996) Development of brain damage after neonatal hypoxia-ischemia: excitatory amino acids and cysteine. Metab Brain Dis 11:109-123.
36. Qian Y, Galli A, Ramamoorthy S, Risso S, DeFelice LJ, Blakely RD (1997) Protein kinase C activation regulates human serotonin transporters in HEK-293 cells via altered cell surface expression. J Neurosci 17:45-57.
37. Rothstein JD, Tabakoff B (1984) Alteration of striatal glutamate release after glutamine synthetase inhibition. J Neurochem 43:1438-1446.
38. Rothstein JD, Tsai G, Kunel RW, Clawson L, Cornblath DR, Drachman DB, Pestronk A, Stauch BL, Coyle JT (1990) Abnormal excitatory amino acid metabolism in amyotrophic lateral sclerosis. Ann Neurol 28:18-25.
39. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, Kunel RW (1994) Localization of neuronal and glial glutamate transporters. Neuron 13:713-725.
40. Rothstein JD, Van Kammen M, Levey AI, Martin LJ, Kunel RW (1995) Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol 38:73-84.
41. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L Kunel RW, Kanai Y, Hediger MA, Wang YF, Schielke JP, Welty DF (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16:675-686.
42. Sagara J, Miura K, Bannai S (1993) Maintenance of neuronal glutathione by glial cells. J Neurochem 61:1672-1676.
43. c- and maintenance of intracellular glutathione levels in pancreatic acinar and islet cell lines. Biochim Biophys Acta 1414:85-94.
44. Sato H, Tamba M, Ishii T, Bannai S (1999) Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J Biol Chem 274:11455-11458.
45. 13C NMR measurements of cerebral glutamine synthesis as evidence for glutamate-glutamine cycling. Proc Natl Acad Sci USA 94:2699-2704.
46. Slivka A, Cohen G (1993) Brain ischemia markedly elevates levels of the neurotoxic amino acid, cysteine. Brain Res 608:33-37.
47. Stachowiak MK, Moffett J, Joy A, Puchacz E, Florkiewicz R, Stachowiak EK (1994) Regulation of bFGF gene expression and subcellular distribution of bFGF protein in adrenal medullary cells. J Cell Biol 127:203-223.
48. + -dependent glutamate/aspartate transporter from rat brain. Proc Natl Acad Sci USA 89:10955-10959.
49. Szatkowski M, Barbour B, Attwell D (1990) Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348:443-446.
50. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, Wada K (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276:1699-1702.
51. Torp R, Danbolt NC, Babaie E, Bjoras M, Seeberg E, Storm-Mathisen J, Ottersen OP (1994) Differential expression of two glial glutamate transporters in the rat brain: an in situ hybridization study. Eur J Neurosci 6:936-942.
52. Waniewski RA, Martin DL (1986) Exogenous glutamate is metabolized to glutamine and exported by rat primary astrocyte cultures. J Neurochem 47:304-313.
53. Watanabe H, Bannai S (1987) Induction of cystine transport activity in mouse peritoneal macrophages. J Exp Med 165:628-640.
54. Whittemore SR, Neary JT, Kleitman N, Sanon HR, Benigno A, Donahue RP, Norenberg MD (1994) Isolation and characterization of conditionally immortalized astrocyte cell lines derived from adult human spinal cord. Glia 10:211-226.
55. Ye ZC, Sontheimer H (1996) Cytokine modulation of glial glutamate uptake: a possible involvement of nitric oxide. NeuroReport 7:2181-2185.
56. Ye ZC, Sontheimer H (1998) Astrocytes protect neurons from neurotoxic injury by serum glutamate. Glia 22:237-248.
57. Ye ZC, Sontheimer H (1999a) Metabotropic glutamate receptor agonists reduce glutamate release from cultured astrocytcs. Glia 25:270-281.
58. Ye ZC, Sontheimer H (1999b) Glioma cells release excitotoxic concentrations of glutamate. Cancer Res 59:4383-4391.
59. Zaczek R, Balm M, Arlis S, Drucker H, Coyle JT (1987) Quisqualate-sensitive, chloride-dependent transport of glutamate into rat brain synaptosomes. J Neurosci Res 18:425-431.
60. Zerangue N, Kavanaugh MP (1996a) Flux coupling in a neuronal glutamate transporter. Nature 383:634-637.
61. Zerangue N, Kavanaugh MP (1996b) Interaction of L-cysteine with a human excitatory amino acid transporter. J Physiol (Lond) 493: 419-423.