Inhibition of cystine uptake disrupts the growth of primary brain tumors

Journal of Neuroscience

Volumn 25, Issue 31, 2005, Pages 7101-7110

  Chung, Wook Joon ^a   Lyons, Susan A ^a   Nelson, Gina M ^a   Hamza, Hashir ^a   Gladson, Candece L ^b   Yancey Gillespie, G ^c   Sontheimer, Harald ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

(S) 4 carboxyphenylglycine; Excitotoxicity; Glial progenitor cells; Glutamate transport; Glutathione; Sulfasalazine

Indexed keywords

4 CARBOXYPHENYLGLYCINE; AMINO ACID TRANSPORT SYSTEM XC; AMINO ACID TRANSPORTER; ANTIOXIDANT; CARRIER PROTEIN; CASPASE; CYSTINE; CYSTINE GLUTAMATE EXCHANGER; GLUTAMIC ACID; GLUTATHIONE; REACTIVE OXYGEN METABOLITE; SALAZOSULFAPYRIDINE; SODIUM ION; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER MODEL; CARCINOGENESIS; CONTROLLED STUDY; DRUG EFFECT; EXCITOTOXICITY; FEMALE; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; MOUSE; NERVE CELL NECROSIS; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; STEM CELL; TUMOR GROWTH;

AMINO ACID TRANSPORT SYSTEMS; ANIMALS; APOPTOSIS; BENZOATES; BRAIN NEOPLASMS; CASPASES; CELL DIVISION; CYSTINE; DNA, NEOPLASM; GLUTATHIONE; GLYCINE; HUMANS; RATS; RATS, SPRAGUE-DAWLEY; SULFASALAZINE; TIME FACTORS; TUMOR CELLS, CULTURED;

EID: 23444449591     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5258-04.2005     Document Type: Article

References (43)

1. Barger SW, Basile AS (2001) Activation of microglia by secreted amyloid precursor protein evokes release of glutamate by cystine exchange and attenuates synaptic function. J Neurochem 76:846-854.
2. c. Pflügers Arch 442:286-296.
3. Baud O, Greene AE, Li J, Wang H, Volpe JJ, Rosenberg PA (2004) Glutathione peroxidase-catalase cooperativity is required for resistance to hydrogen peroxide by mature rat oligodendrocytes. J Neurosci 24:1531-1540.
4. Behrens PF, Langemann H, Strohschein R, Draeger J, Hennig J (2000) Extracellular glutamate and other metabolites in and around RG2 rat glioma: an intracerebral microdialysis study. J Neurooncol 47:11-22.
5. Dai C, Holland EC (2001) Glioma models. Biochim Biophys Acta 1551:M19-M27.
6. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105.
7. Deng W, Rosenberg PA, Volpe JJ, Jensen FE (2003) Calcium-permeable AMPA/kainate receptors mediate toxicity and preconditioning by oxygen-glucose deprivation in oligodendrocyte precursors. Proc Natl Acad Sci USA 100:6801-6806.
8. Espey MG, Kustova Y, Sei Y, Basile AS (1998) Extracellular glutamate levels are chronically elevated in the brains of LP-BM5-infected mice: a mechanism of retrovirus-induced encephalopathy. J Neurochem 71:2079-2087.
9. 35S]cystine transport into rat brain synaptosomes. Neurochem Int 36:513-521.
10. Fojo T, Bates S (2003) Strategies for reversing drug resistance. Oncogene 22:7512-7523.
11. Freitas RM, Vasconcelos SM, Souza FC, Viana GS, Fonteles MM (2005) Oxidative stress in the hippocampus after pilocarpine-induced status epilepticus in Wistar rats. FEBS J 272:1307-1312.
12. Gout PW, Buckley AR, Simms CR, Bruchovsky N (2001) Sulfasalazine, a potent suppressor of lymphoma growth by inhibition of the x(c)- cystine transporter: a new action for an old drug. Leukemia 15:1633-1640.
13. Hammoud MA, Sawaya R, Shi W, Thall PF, Leeds NE (1996) Prognostic significance of preoperative MRI scans in glioblastoma multiforme. J Neurooncol 27:65-73.
14. Jefferies H, Coster J, Khalil A, Bot J, McCauley RD, Hall JC (2003) Glutathione. ANZ J Surg 73:517-522.
15. Kim JY, Kanai Y, Chairoungdua A, Cha SH, Matsuo H, Kim DK, Inatomi J, Sawa H, Ida Y, Endou H (2001) Human cystine/glutamate transporter: cDNA cloning and upregulation by oxidative stress in glioma cells. Biochim Biophys Acta 1512:335-344.
16. Kleihues P, Burger PC, Scheithauer BW (1993) The new WHO classification of brain tumours. Brain Pathol 3:255-268.
17. Louw DF, Bose R, Sima AA, Sutherland GR (1997) Evidence for a high free radical state in low-grade astrocytomas. Neurosurgery 41:1146-1150.
18. McBean GJ (2002) Cerebral cystine uptake: a tale of two transporters. Trends Pharmacol Sci 23:299-302.
19. 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.
20. Noseworthy JH, O'Brien P, Erickson BJ, Lee D, Sneve D, Ebers GC, Rice GP, Auty A, Hader WJ, Kirk A, Duquette P, Carter J, Francis G, Metz L, Shuster E (1998) The Mayo Clinic-Canadian Cooperative trial of sulfasalazine in active multiple sclerosis. Neurology 51:1342-1352.
21. Oberndorfer S, Schmal T, Lahrmann H, Urbanits S, Lindner K, Grisold W (2002) The frequency of seizures in patients with primary brain tumors or cerebral metastases. An evaluation from the Ludwig Boltzmann Institute of Neuro-Oncology and the Department of Neurology, Kaiser Franz Josef Hospital, Vienna. Wien Klin Wochenschr 114:911-916.
22. Oka A, Belliveau MJ, Rosenberg PA, Volpe JJ (1993) Vulnerability of oligodendroglia to glutamate: pharamacology, mechanisms, and prevention. J Neurosci 13:1441-1453.
23. -: an obligate exchanger of L-glutamate and L-cystine. Neuropharmacology 46:273-284.
24. Ratan RR, Murphy TH, Baraban JM (1994) Oxidative stress induces apoptosis in embryonic cortical neurons. J Neurochem 62:376-379.
25. Raza SM, Lang FF, Aggarwal BB, Fuller GN, Wildrick DM, Sawaya R (2002) Necrosis and glioblastoma: a friend or a foe? A review and a hypothesis. Neurosurgery 51:2-12.
26. 1H MR spectroscopic imaging. NMR Biomed 16:12-18.
27. Robe PA, Bentires-Alj M, Bonif M, Rogister B, Deprez M, Haddada H, Khac MT, Jolois O, Erkmen K, Merville MP, Black PM, Bours V (2004) In vitro and in vivo activity of the nuclear factor-kappaB inhibitor sulfasalazine in human glioblastomas. Clin Cancer Res 10:5595-5603.
28. Roslin M, Henriksson R, Bergstrom P, Ungerstedt U, Bergenheim AT (2003) Baseline levels of glucose metabolites, glutamate and glycerol in malignant glioma assessed by stereotactic microdialysis. J Neurooncol 61:151-160.
29. Rothstein JD (2002) Paving new pathways. Nat Med 8:938-940.
30. 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.
31. -, in the mouse brain. J Neurosci 22:8028-8033.
32. Shanker G, Aschner M (2001) Identification and characterization of uptake systems for cystine and cysteine in cultured astrocytes and neurons: evidence for methylmercury-targeted disruption of astrocyte transport. J Neurosci Res 66:998-1002.
33. Sharon P, Drab EA, Linder JS, Weidman SW, Sabesin SM, Rubin DB (1992) The effect of sulfasalazine on bovine endothelial cell proliferation and cell cycle phase distribution. Comparison with olsalazine, 5-aminosalicylic acid, and sulfapyridine. J Lab Clin Med 119:99-107.
34. Shibata T, Burger PC, Kleihues P (1988) Ki-67 immunoperoxidase stain as marker for the histological grading of nervous system tumours. Acta Neurochir Suppl (Wien) 43:103-106.
35. Shih AY, Johnson DA, Wong G, Kraft AD, Jiang L, Erb H, Johnson JA, Murphy TH (2003) Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J Neurosci 23:3394-3406.
36. Sontheimer H (2003) Malignant gliomas: perverting glutamate and ion homeostasis for selective advantage. Trends Neurosci 26:543-549.
37. Soroceanu L, Gillespie Y, Khazaeli MB, Sontheimer H (1998) Useofchlorotoxin for targeting of primary brain tumors. Cancer Res 58:4871-4879.
38. Takano T, Lin JH, Arcuino G, Gao Q, Yang J, Nedergaard M (2001) Glutamate release promotes growth of malignant gliomas. Nat Med 7:1010-1015.
39. Wu G, Fang YZ, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134:489-492.
40. Ye ZC, Sontheimer H (1998) Astrocytes protect neurons from neurotoxic injury by serum glutamate. Glia 22:237-248.
41. Ye ZC, Sontheimer H (1999) Glioma cells release excitotoxic concentrations of glutamate. Cancer Res 59:4383-4391.
42. Ye ZC, Rothstein JD, Sontheimer H (1999) Compromised glutamate transport in human glioma cells: reduction-mislocalization of sodium-dependent glutamate transporters and enhanced activity of cystine-glutamate exchange. J Neurosci 19:10767-10777.
43. Yonezawa M, Back SA, Gan X, Rosenberg PA, Volpe JJ (1996) Cystine deprivation induces oligodendroglial death: rescue by free radical scavengers and by a diffusible glial factor. J Neurochem 67: 566-573.