Increased expression of glutamate transporter GLT-1 in peritumoral tissue associated with prolonged survival and decreases in tumor growth in a rat model of experimental malignant glioma

Journal of Neurosurgery

Volumn 119, Issue 4, 2013, Pages 878-886

  Sattler, Rita ^a,b   Tyler, Betty ^b   Hoover, Benjamin ^a   Coddington, Luke T ^a   Recinos, Violette ^b   Hwang, Lee ^b   Brem, Henry ^b   Rothstein, Jeffrey D ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

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

Author keywords

EAAT2; Glioblastoma; GLT 1; Glutamate; Glutamate transporter; Oncology; Rat; Thiamphenicol

Indexed keywords

BIOLOGICAL MARKER; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; THIAMPHENICOL; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOPSY; BRAIN CELL CULTURE; BRAIN TISSUE; CELL PROLIFERATION; CELLS; CHEMICAL ANALYSIS; CONTROLLED STUDY; DEPRESSION; DOSE RESPONSE; EUROPE; GLIOBLASTOMA; GLIOMA; GLIOSARCOMA; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SURVIVAL; SURVIVAL TIME; TUMOR GROWTH; TUMOR VOLUME; UPREGULATION;

ANIMALS; ASTROCYTES; BRAIN; BRAIN NEOPLASMS; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID TRANSPORTER 2; GLIOSARCOMA; NEURONS; RATS; RATS, INBRED F344; THIAMPHENICOL;

EID: 84885341492     PISSN: 00223085     EISSN: 19330693     Source Type: Journal    
DOI: 10.3171/2013.6.JNS122319     Document Type: Article

References (52)

1. Arcella A, Carpinelli G, Battaglia G, D'Onofrio M, Santoro F, Ngomba RT, et al: Pharmacological blockade of group II metabotropic glutamate receptors reduces the growth of glioma cells in vivo. Neuro Oncol 7: 236-245, 2005 (Pubitemid 41079133)
2. Azzollini F, Gazzaniga A, Lodola E: Thiamphenicol excretion in subjects with renal insufficiency. Int Z Klin Pharmakol Ther Toxikol 4: 303-308, 1970
3. Buckingham SC, Campbell SL, Haas BR, Montana V, Robel S, Ogunrinu T, et al: Glutamate release by primary brain tumors induces epileptic activity. Nat Med 17: 1269-1274, 2011
4. Chung WJ, Lyons SA, Nelson GM, Hamza H, Gladson CL, Gillespie GY, et al: Inhibition of cystine uptake disrupts the growth of primary brain tumors. J Neurosci 25: 7101-7110, 2005 (Pubitemid 41113926)
5. Chung WJ, Sontheimer H: Sulfasalazine inhibits the growth of primary brain tumors independent of nuclear factor-kappaB. J Neurochem 110: 182-193, 2009
6. Danbolt NC: Glutamate uptake. Prog Neurobiol 65: 1-105, 2001 (Pubitemid 32479155)
7. de Groot J, Sontheimer H: Glutamate and the biology of gliomas. Glia 59: 1181-1189, 2011
8. de Groot JF, Gilbert MR: New molecular targets in malignant gliomas. Curr Opin Neurol 20: 712-718, 2007 (Pubitemid 350085016)
9. de Groot JF, Liu TJ, Fuller G, Yung WK: The excitatory amino acid transporter-2 induces apoptosis and decreases glioma growth in vitro and in vivo. Cancer Res 65: 1934-1940, 2005 (Pubitemid 40478623)
10. de Groot JF, Piao Y, Lu L, Fuller GN, Yung WK: Knockdown of GluR1 expression by RNA interference inhibits glioma proliferation. J Neurooncol 88: 121-133, 2008
11. DiMeco F, Rhines LD, Hanes J, Tyler BM, Brat D, Torchiana E, et al: Paracrine delivery of IL-12 against intracranial 9L gliosarcoma in rats. J Neurosurg 92: 419-427, 2000 (Pubitemid 30112382)
12. Ferrari V: Salient features of thiamphenicol: review of clinical pharmacokinetics and toxicity. Sex Transm Dis 11 (4 Suppl): 336-339, 1984 (Pubitemid 15188100)
13. Ginsberg MD: Neuroprotection for ischemic stroke: past, present and future. Neuropharmacology 55: 363-389, 2008
14. Grossman SA, Reinhard C, Colvin OM, Chasin M, Brundrett R, Tamargo RJ, et al: The intracerebral distribution of BCNU delivered by surgically implanted biodegradable polymers. J Neurosurg 76: 640-647, 1992
15. Grossman SA, Ye X, Chamberlain M, Mikkelsen T, Batchelor T, Desideri S, et al: Talampanel with standard radiation and temozolomide in patients with newly diagnosed glioblastoma: a multicenter phase II trial. J Clin Oncol 27: 4155-4161, 2009
16. Grossman SA, Ye X, Piantadosi S, Desideri S, Nabors LB, Rosenfeld M, et al: Survival of patients with newly diagnosed glioblastoma treated with radiation and temozolomide in research studies in the United States. Clin Cancer Res 16:2443- 2449, 2010
17. Guerin C, Olivi A, Weingart JD, Lawson HC, Brem H: Recent advances in brain tumor therapy: local intracerebral drug delivery by polymers. Invest New Drugs 22: 27-37, 2004 (Pubitemid 38196980)
18. Hota SK, Barhwal K, Ray K, Singh SB, Ilavazhagan G: Ceftriaxone rescues hippocampal neurons from excitotoxicity and enhances memory retrieval in chronic hypobaric hypoxia. Neurobiol Learn Mem 89: 522-532, 2008
19. Iwamoto FM, Kreisl TN, Kim L, Duic JP, Butman JA, Albert PS, et al: Phase 2 trial of talampanel, a glutamate receptor inhibitor, for adults with recurrent malignant gliomas. Cancer 116: 1776-1782, 2010
20. Jelenkovic AV, Jovanovic MD, Stanimirovic DD, Bokonjic DD, Ocic GG, Boskovic BS: Beneficial effects of ceftriaxone against pentylenetetrazole-evoked convulsions. Exp Biol Med (Maywood) 233: 1389-1394, 2008
21. Kong Q, Takahashi K, Schulte D, Stouffer N, Lin Y, Lin CL: Increased glial glutamate transporter EAAT2 expression reduces epileptogenic processes following pilocarpine-induced status epilepticus. Neurobiol Dis 47: 145-154, 2012
22. Lai PC, Huang YT, Wu CC, Lai CJ, Wang PJ, Chiu TH: Ceftriaxone attenuates hypoxic-ischemic brain injury in neonatal rats. J Biomed Sci 18:69, 2011
23. Lee SG, Kim K, Kegelman TP, Dash R, Das SK, Choi JK, et al: Oncogene AEG-1 promotes glioma-induced neurodegeneration by increasing glutamate excitotoxicity. Cancer Res 71: 6514-6523, 2011
24. Li Y, Sattler R, Yang EJ, Nunes A, Ayukawa Y, Akhtar S, et al: Harmine, a natural beta-carboline alkaloid, upregulates astroglial glutamate transporter expression. Neuropharmacology 60: 1168-1175, 2011
25. Lipski J, Wan CK, Bai JZ, Pi R, Li D, Donnelly D: Neuroprotective potential of ceftriaxone in in vitro models of stroke. Neuroscience 146: 617-629, 2007 (Pubitemid 46617069)
26. Lukas RV, Boire A, Nicholas MK: Emerging therapies for malignant glioma. Expert Rev Anticancer Ther 7 (12 Suppl): S29-S36, 2007
27. Marcus HJ, Carpenter KL, Price SJ, Hutchinson PJ: In vivo assessment of high-grade glioma biochemistry using microdialysis: a study of energy-related molecules, growth factors and cytokines. J Neurooncol 97: 11-23, 2010
28. Miller BR, Dorner JL, Shou M, Sari Y, Barton SJ, Sengelaub DR, et al: Up-regulation of GLT1 expression increases glutamate uptake and attenuates the Huntington's disease phenotype in the R6/2 mouse. Neuroscience 153: 329-337, 2008
29. Ohgaki H, Kleihues P: Genetic alterations and signaling pathways in the evolution of gliomas. Cancer Sci 100: 2235-2241, 2009
30. Pfenninger J, Furrer H, Fürst M, Vogt J, Widmer H: Thiamphenicol in treatment of Haemophilus influenzae meningitis. Helv Paediatr Acta 32: 207-216, 1977 (Pubitemid 8185469)
31. Ramos KM, Lewis MT, Morgan KN, Crysdale NY, Kroll JL, Taylor FR, et al: Spinal upregulation of glutamate transporter GLT-1 by ceftriaxone: therapeutic efficacy in a range of experimental nervous system disorders. Neuroscience 169:1888- 1900, 2010
32. Robe PA, Bentires-Alj M, Bonif M, Rogister B, Deprez M, Haddada H, et al: In vitro and in vivo activity of the nuclear factor-kappaB inhibitor sulfasalazine in human glioblastomas. Clin Cancer Res 10: 5595-5603, 2004 (Pubitemid 39100501)
33. Robe PA, Martin D, Albert A, Deprez M, Chariot A, Bours V: A phase 1-2, prospective, double blind, randomized study of the safety and efficacy of Sulfasalazine for the treatment of progressing malignant gliomas: study protocol of [ISRCTN45828668]. BMC Cancer 6:29, 2006
34. Robe PA, Martin DH, Nguyen-Khac MT, Artesi M, Deprez M, Albert A, et al: Early termination of ISRCTN45828668, a phase 1/2 prospective, randomized study of sulfasalazine for the treatment of progressing malignant gliomas in adults. BMC Cancer 9:372, 2009
35. Rothstein JD, Brem H: Excitotoxic destruction facilitates brain tumor growth. Nat Med 7: 994-995, 2001 (Pubitemid 32937369)
36. Rothstein JD, Patel S, Regan MR, Haenggeli C, Huang YH, Bergles DE, et al: Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 433: 73-77, 2005 (Pubitemid 40101145)
37. Rzeski W, Turski L, Ikonomidou C: Glutamate antagonists limit tumor growth. Proc Natl Acad Sci U S A 98: 6372-6377, 2001 (Pubitemid 32488244)
38. Sato H, Tamba M, Ishii T, Bannai S: Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J Biol Chem 274:11455- 11458, 1999
39. Sattler R, Ayukawa Y, Coddington L, Sawa A, Block D, Chipkin R, et al: Human nasal olfactory epithelium as a dynamic marker for CNS therapy development. Exp Neurol 232:203- 211, 2011
40. Savaskan NE, Heckel A, Hahnen E, Engelhorn T, Doerfler A, Ganslandt O, et al: Small interfering RNA-mediated xCT silencing in gliomas inhibits neurodegeneration and alleviates brain edema. Nat Med 14: 629-632, 2008 (Pubitemid 351809547)
41. Savaskan NE, Seufert S, Hauke J, Tränkle C, Eyüpoglu IY, Hahnen E: Dissection of mitogenic and neurodegenerative actions of cystine and glutamate in malignant gliomas. Oncogene 30: 43-53, 2011
42. Sondheimer I, Knackstedt LA: Ceftriaxone prevents the induction of cocaine sensitization and produces enduring attenuation of cue- and cocaine-primed reinstatement of cocaine-seeking. Behav Brain Res 225: 252-258, 2011
43. Sontheimer H: Malignant gliomas: perverting glutamate and ion homeostasis for selective advantage. Trends Neurosci 26: 543-549, 2003 (Pubitemid 37176909)
44. Takano T, Lin JH, Arcuino G, Gao Q, Yang J, Nedergaard M: Glutamate release promotes growth of malignant gliomas. Nat Med 7: 1010-1015, 2001 (Pubitemid 32937380)
45. Thöne-Reineke C, Neumann C, Namsolleck P, Schmerbach K, Krikov M, Schefe JH, et al: The beta-lactam antibiotic, ceftriaxone, dramatically improves survival, increases glutamate uptake and induces neurotrophins in stroke. J Hypertens 26: 2426-2435, 2008
46. Tyler B, Fowers KD, Li KW, Recinos VR, Caplan JM, Hdeib A, et al: A thermal gel depot for local delivery of paclitaxel to treat experimental brain tumors in rats. Laboratory investigation. J Neurosurg 113: 210-217, 2010
47. van Vuurden DG, Yazdani M, Bosma I, Broekhuizen AJ, Postma TJ, Heimans JJ, et al: Attenuated AMPA receptor expression allows glioblastoma cell survival in glutamate-rich environment. PLoS ONE 4:e5953, 2009
48. Vanhoutte N, Abarca-Quinones J, Jordan BF, Gallez B, Maloteaux JM, Hermans E: Enhanced expression of the high affinity glutamate transporter GLT-1 in C6 glioma cells delays tumour progression in rat. Exp Neurol 218: 56-63, 2009
49. Ye ZC, Rothstein JD, Sontheimer H: 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, 1999 (Pubitemid 30235723)
50. Ye ZC, Sontheimer H: Glioma cells release excitotoxic concentrations of glutamate. Cancer Res 59: 4383-4391, 1999 (Pubitemid 29418758)
51. Yuen TI, Morokoff AP, Bjorksten A, D'Abaco G, Paradiso L, Finch S, et al: Glutamate is associated with a higher risk of seizures in patients with gliomas. Neurology 79: 883-889, 2012
52. Zeng LH, Bero AW, Zhang B, Holtzman DM, Wong M: Modulation of astrocyte glutamate transporters decreases seizures in a mouse model of Tuberous Sclerosis Complex. Neurobiol Dis 37: 764-771, 2010