Cooperative action of glutamate transporters and cystine/glutamate antiporter system Xc- protects from oxidative glutamate toxicity

Journal of Neurochemistry

Volumn 98, Issue 3, 2006, Pages 916-925

  Lewerenz, Jan ^a   Klein, Mathias ^a   Methner, Axel ^b  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Cystine glutamate antiporter; Excitatory amino acid transporter; Glutathione; Neuroprotection; Oxidative glutamate toxicity

Indexed keywords

2,4 PYRROLIDINEDICARBOXYLIC ACID; ANTIOXIDANT; ANTIPORTER; ASPARTIC ACID DERIVATIVE; CYSTINE; CYSTINE GLUTAMATE ANTIPORTER; EXCITATORY AMINO ACID TRANSPORTER; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; GLUTATHIONE; PROTEIN SUBUNIT; REACTIVE OXYGEN METABOLITE; THREO BETA BENZYLOXYASPARTIC ACID; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DEPLETION; DISEASE EXACERBATION; GENE OVEREXPRESSION; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CONTENT;

AMINO ACID TRANSPORT SYSTEM X-AG; AMINO ACID TRANSPORT SYSTEM Y+; ANIMALS; ANTIPORTERS; CELL DEATH; CELL LINE; GLUTAMIC ACID; MICE; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS;

EID: 33745890604     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03921.x     Document Type: Article

References (50)

1. Allen J. W., Shanker G., Tan K. H. and Aschner M. (2002) The consequences of methylmercury exposure on interactive functions between astrocytes and neurons. Neurotoxicology 23, 755-759.
2. Baker D. A., Xi Z. X., Shen H., Swanson C. J. and Kalivas P. W. (2002) The origin and neuronal function of in vivo nonsynaptic glutamate. J. Neurosci. 22, 9134-9141.
3. Bannai S. (1986) Exchange of cystine and glutamate across plasma membrane of human fibroblasts. J. Biol. Chem. 261, 2256-2263.
4. Beal M. F. (1996) Mitochondria, free radicals, and neurodegeneration. Cuir. Opin. Neurobiol. 6, 661-666.
5. Chen C. J., Liao S. L. and Kuo J. S. (2000) Gliotoxic action of glutamate on cultured astrocytes. J. Neurochem. 75, 1557-1565.
6. Chen Y. and Swanson R. A. (2003) The glutamate transporters EAAT2 and EAAT3 mediate cysteine uptake in cortical neuron cultures. J. Neurochem. 84, 1332-1339.
7. Choi D. W. (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634.
8. Coyle J. T. and Puttfarcken P. (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science 262, 689-695.
9. Dargusch R. and Schubert D. (2002) Specificity of resistance to oxidative stress. J. Neurochem. 81, 1394-1400.
10. Davis J. B. and Maher P. (1994) Protein kinase C activation inhibits glutamate-induced cytotoxicity in a neuronal cell line. Brain Res. 652, 169-173.
11. Dringen R. (2000) Metabolism and functions of glutathione in brain. Prog. Neurobiol. 62, 649-671.
12. Dringen R., Pawlowski P. G. and Hirrlinger J. (2005) Peroxide detoxification by brain cells. J. Neurosci. Res. 79, 157-165.
13. Dunlop J., Grieve A. and Griffiths R. (1993) 1-trans-pyrrolidine-2,4- dicarboxylic acid (1-transPDC) has properties consistent with that of a competitive substrate for the plasma membrane glutamate transporter. Biochem. Soc. Trans. 21, 111S.
14. Hansen M. B., Niilsen S. E. and Berg K. (1989) Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Meth 119, 203-210.
15. Himi T., Ikeda M., Yasuhara T., Nishida M. and Morita I. (2003) Role of neuronal glutamate transporter in the cysteine uptake and intracellular glutathione levels in cultured cortical neurons. J. Neural Transm 110, 1337-1348.
16. +-dependent glutamate and aspartate transporter supports glutathione maintenance and survival of CHO-K1 cells. Somat Cell Mol Genet 24, 341-352.
17. Ishii T., Itoh K., Takahashi S., Sato H., Yanagawa T., Katoh Y., Bannai S. and Yamamoto M. (2000) Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biol. Chem. 275, 16 023-16 029.
18. Kanai Y. and Hediger M. A. (2004) The glutamate/neutral amino acid transporter family SLC1: molecular, physiological and pharmacological aspects. Pflugers Arch. 447, 469-479.
19. Knickelbein R. G., Seres T., Lam G., Johnston R. B. Jr and Warshaw J. B. (1997) Characterization of multiple cysteine and cystine transporters in rat alveolar type II cells. Am. J. Physiol. 273, L1147-L1155.
20. Lewerenz J., Letz J. and Methner A. (2003) Activation of stimulatory heterotrimeric G proteins increases glutathione and protects neuronal cells against oxidative stress. J. Neurochem. 87, 522-531.
21. Li Y., Maher P. and Schubert D. (1997a) A role for 12-lipoxygenase in nerve cell death caused by glutathione depletion. Neuron 19, 453-463.
22. Li Y., Maher P. and Schubert D. (1997b) Requirement for cGMP in nerve cell death caused by glutathione depletion. J. Cell Biol. 139, 1317-1324.
23. Maher P. and Davis J. B. (1996) The role of monoamine metabolism in oxidative glutamate toxicity. J. Neurosci. 16, 6394-6401.
24. McBean G. J. and Flynn J. (2001) Molecular mechanisms of cystine transport. Biochem. Soc. Trans. 29, 717-722.
25. Miyamoto M., Murphy T. H., Schnaar R. L. and Coyle J. T. (1989) Antioxidants protect against glutamate-induced cytotoxicity in a neuronal cell line. J. Pharmacol. Exp Ther 250, 1132-1140.
26. Murphy T. H., Miyamoto M., Sastre A., Schnaar R. L. and Coyle J. T. (1989) Glutamate toxicity in a neuronal cell line involves inhibition of cystine transport leading to oxidative stress. Neuron 2, 1547-1558.
27. Murphy T. H., Schnaar R. L. and Coyle J. T. (1990) Immature cortical neurons are uniquely sensitive to glutamate toxicity by inhibition of cystine uptake. Faseb J. 4, 1624-1633.
28. Nguyen T., Sherratt P. J. and Pickett C. B. (2003) Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43, 233-260.
29. Oka A., Belliveau M. J., Rosenberg P. A. and Volpe J. J. (1993) Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms, and prevention. J. Neurosci. 13, 1441-1453.
30. Patel S. A., Warren B. A., Rhoderick J. F. and Bridges R. J. (2004) Differentiation of substrate and non-substrate inhibitors of transport system xc (-): an obligate exchanger of 1-glutamate and 1-cystine. Neuropharmacology 46, 273-284.
31. Pratico D. (2002) Alzheimer's disease and oxygen radicals: new insights. Biochem. Pharmacol. 63, 563-567.
32. Ratan R. R., Murphy T. H. and Baraban J. M. (1994) Oxidative stress induces apoptosis in embryonic cortical neurons. J. Neurochem. 62, 376-379.
33. Reichelt W., Stabel-Burow J., Pannicke T., Weichert H. and Heinemann U. (1997) The glutathione level of retinal Muller glial cells is dependent on the high-affinity sodium-dependent uptake of glutamate. Neuroscience 77, 1213-1224.
34. Rimaniol A. C., Mialocq P., Clayette P., Dormont D. and Gras G. (2001) Role of glutamate transporters in the regulation of glutathione levels in human macrophages. Am. J. Physiol. Cell Physiol. 281, C1964-C1970.
35. Sagara Y., Dargusch R., Chambers D., Davis J., Schubert D. and Maher P. (1998) Cellular mechanisms of resistance to chronic oxidative stress. Free Radic Biol. Med. 24, 1375-1389.
36. Sagara Y., Dargusch R., Klier F. G., Schubert D. and Behl C. (1996) Increased antioxidant enzyme activity in amyloid beta protein-resistant cells. J. Neurosci. 16, 497-505.
37. Sasaki H., Sato H., Kuriyama-Matsumura K., Sato K., Maebara K., Wang H., Tamba M., Itoh K., Yamamoto M. and Bannai S. (2002) Electrophile response element-mediated induction of the cystine/glutamate exchange transporter gene expression. J. Biol. Chem. 277, 44 765-44 771.
38. Sato H., Nomura S., Maebara K., Sato K., Tamba M. and Bannai S. (2004) Transcriptional control of cystine/glutamate transporter gene by amino acid deprivation. Biochem. Biophys. Res. Commun 325, 109-116.
39. Sato H., Tamba M., Ishii T. and Bannai S. (1999) Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J. Biol. Chem. 274, 11 455-11 458.
40. Schubert D. and Piasecki D. (2001) Oxidative glutamate toxicity can be a component of the excitotoxicity cascade. J. Neurosci. 21, 7455-7462.
41. Schulz J. B., Lindenau J., Seyfried J. and Dichgans J. (2000) Glutathione, oxidative stress and neurodegeneration. Eur J. Biochem. 267, 4904-4911.
42. Shanker G., Allen J. W., Mutkus L. A. and Aschner M. (2001) The uptake of cysteine in cultured primary astrocytes and neurons. Brain Res. 902, 156-163.
43. Shih A. Y., Johnson D. A., Wong G., Kraft A. D., Jiang L., Erb H., Johnson J. A. and Murphy T. H. (2003) Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J. Neurosci. 23, 3394-3406.
44. Shih A. Y. and Murphy T. H. (2001) xCt cystine transporter expression in HEK293 cells: pharmacology and localization. Biochem. Biophys. Res. Commun 282, 1132-1137.
45. Tan S., Sagara Y., Liu Y., Maher P. and Schubert D. (1998) The regulation of reactive oxygen species production during programmed cell death. J. Cell Biol. 141, 1423-1432.
46. Tan S., Schubert D. and Maher P. (2001) Oxytosis: a novel form of programmed cell death. Curr. Top Med. Chem. 1, 497-506.
47. Thimmulappa R. K., Mai K. H., Srisuma S., Kensler T. W., Yamamoto M. and Biswal S. (2002) Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 62, 5196-5203.
48. Trotti D., Danbolt N. C. and Volterra A. (1998) Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration? Trends Pharmacol. Sci. 19, 328-334.
49. Waagepetersen H. S., Shimamoto K. and Schousboe A. (2001) Comparison of effects of DL-threo-beta-benzyloxyaspartate (DL-TBOA) and 1-trans-pyrrolidine-2, 4-dicarboxylate (t-2,4-PDC) on uptake and release of [3h]D-aspartate in astrocytes and glutamatergic neurons. Neurochem. Res. 26, 661-666.
50. Wang X. F. and Cynader M. S. (2000) Astrocytes provide cysteine to neurons by releasing glutathione. J. Neurochem. 74, 1434-1442.