DNA methylation dependent silencing of the human glutamate transporter EAAT2 gene in glial cells

GLIA

Volumn 55, Issue 7, 2007, Pages 663-674

  Zschocke, Jürgen ^a   Allritz, Claudia ^b   Engele, Jürgen ^b   Rein, Theo ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

CpG island; DNA methylation; GLT 1; Histone deacetylation

Indexed keywords

BISULFITE; DNA METHYLTRANSFERASE; GLUTAMATE TRANSPORTER; MESSENGER RNA; NUCLEAR FACTOR; PROTEIN EAAT2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; BINDING SITE; BRAIN TISSUE; CELL LINE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ENZYME INHIBITION; EPIGENETICS; GEL MOBILITY SHIFT ASSAY; GENE SILENCING; GLIA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; RNA TRANSCRIPTION; SEQUENCE ANALYSIS;

ANIMALS; ASTROCYTES; BRAIN; BRAIN CHEMISTRY; BRAIN NEOPLASMS; CELLS, CULTURED; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE SILENCING; GENES, REPORTER; GLIOMA; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; GLUTAMIC ACID; HELA CELLS; HUMANS; NEUROGLIA; PROMOTER REGIONS (GENETICS); RATS; RATS, SPRAGUE-DAWLEY;

EID: 34247538936     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20497     Document Type: Article

References (53)

1. Arriza JL, Fairman WA, Wadiche JI, Murdoch GH, Kavanaugh MP, Amara SG. 1994. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J Neurosci 14:5559-5569.
2. Ballestar E, Wolffe AP. 2001. Methyl-CpG-binding proteins. Targeting specific gene repression. Eur J Biochem 268:1-6.
3. Bar-Peled O, Ben-Hur H, Biegon A, Groner Y, Dewhurst S, Furuta A, Rothstein JD. 1997. Distribution of glutamate transporter subtypes during human brain development. J Neurochem 69:2571-2580.
4. Boston-Howes W, Gibb SL, Williams EO, Pasinelli P, Brown RHJ, Trotti D. 2006. Caspase-3 cleaves and inactivates the glutamate transporter EAAT2. J Biol Chem 281:14076-14084.
5. Christman JK. 2002. 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: Mechanistic studies and their implications for cancer therapy. Oncogene 21:5483-5495.
6. de Groot JF, Liu TJ, Fuller G, Yung WK. 2005. The excitatory amino acid transporter-2 induces apoptosis and decreases glioma growth in vitro and in vivo. Cancer Res 65:1934-1940.
7. Detich N, Bovenzi V, Szyf M. 2003. Valproate induces replication- independent active DNA demethylation. J Biol Chem 278:27586-27592
8. Driever PH, Knupfer MM, Cinatl J, Wolff JEA. 1999. Valproic acid for the treatment of pediatric malignant glioma. Klinische Padiatrie 211:323-328.
9. Erecinska M, Silver IA. 1990. Metabolism and role of glutamate in mammalian brain. Prog Neurobiol 35:245-296.
10. Evans RJ, Wyllie FS, Wynford-Thomas D, Kipling D, Jones CJ. 2003. A P53-dependent, telomere-independent proliferative life span barrier in human astrocytes consistent with the molecular genetics of glioma development. Cancer Res 63:4854-4861.
11. Fan G, Martinowich K, Chin MH, He F, Fouse SD, Hutnick L, Hattori D, Ge W, Shen Y, Wu H, ten Hoeve J, Shuai K, Sun YE. 2005. DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132:3345-3356.
12. Figiel M, Engele J. 2000. Pituitary adenylate cyclase-activating polypeptide (PACAP), a neuron-derived peptide regulating glial glutamate transport and metabolism. J Neurosci 20:3596-3605.
13. Foltz G, Ryu GY, Yoon JG, Nelson T, Fahey J, Frakes A, Lee H, Field L, Zander K, Sibenaller Z, Ryken TC, Vibhakar R, Hood L, Madan A. 2006. Genome-wide analysis of epigenetic silencing identifies BEX1 and BEX2 as candidate tumor suppressor genes in malignant glioma. Cancer Res 66:6665-6674.
14. Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL. 1992. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci USA 89:1827-1831.
15. Gardiner-Garden M, Frommer M. 1987. CpG islands in vertebrate genomes. J Mol Biol 196:261-282.
16. Gegelashvili G, Schousboe A. 1998. Cellular distribution and kinetic properties of high-affinity glutamate transporters. Brain Res Bull 45:233-238.
17. Gottlicher M, Minucci S, Zhu P, Kramer OH, Schimpf A, Giavara S, Sleeman JP, Lo Coco F, Nervi C, Pelicci PG, Heinzel T. 2001. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 20:6969-6978.
18. Grayson DR, Jia XM, Chen Y, Sharma RP, Mitchell CP, Guidotti A, Costa E. 2005. Reelin promoter hypermethylation in schizophrenia. Proc Natl Acad Sci USA 102:9341-9346.
19. Guo H, Lai L, Butchbach ME, Lin CL. 2002. Human glioma cells and undifferentiated primary astrocytes that express aberrant EAAT2 mRNA inhibit normal EAAT2 protein expression and prevent cell death. Mol Cell Neurosci 21:546-560.
20. Hassel B, Iversen EG, Gjerstad L, Tauboll E. 2001. Up-regulation of hippocampal glutamate transport during chronic treatment with sodium valproate. J Neurochem 77:1285-1292.
21. 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.
22. Iwamoto K, Bundo M, Yamada K, Takao H, Iwayama-Shigeno Y, Yoshikawa T, Kato T. 2005. DNA methylation status of SOX10 correlates with its downregulation and oligodendrocyte dysfunction in schizophrenia. J Neurosci 25:5376-5381.
23. Johannessen CU. 2000. Mechanisms of action of valproate: A commentatory. Neurochem Int 37:103-110.
24. Levy LM, Warr O, Attwell D. 1998. Stoichiometry of the glial glutamate transporter GLT-1 expressed inducibly in a Chinese hamster ovary cell line selected for low endogenous Na+-dependent glutamate uptake. J Neurosci 18:9620-9628.
25. Li S, Mallory M, Alford M, Tanaka S, Masliah E. 1997. Glutamate transporter alterations in Alzheimer disease are possibly associated with abnormal APP expression. J Neuropathol Exp Neurol 56:901-911.
26. Lin CL, Bristol LA, Jin L, Dykes-Hoberg M, Crawford T, Clawson L, Rothstein JD. 1998. Aberrant RNA processing in a neurodegenerative disease: The cause for absent EAAT2, a glutamate transporter, in amyotrophic lateral sclerosis. Neuron 20:589-602.
27. Maragakis NJ, Rothstein JD. 2001. Glutamate transporters in neurologic disease. Arch Neurol 58:365-370.
28. Milton ID, Banner SJ, Ince PG, Piggott NH, Fray AE, Thatcher N, Horne CH, Shaw PJ. 1997. Expression of the glial glutamate transporter EAAT2 in the human CNS: An immunohistochemical study. Brain Res Mol Brain Res 52:17-31.
29. Namihira M, Nakashima K, Taga T. 2004. Developmental stage dependent regulation of DNA methylation and chromatin modification in a immature astrocyte specific gene promoter. FEBS Lett 572:184-188.
30. Olney JW. 1994. New mechanisms of excitatory transmitter neurotoxicity. J Neural Transm Suppl 43:47-51.
31. Pawlak J, Brito V, Kuppers E, Beyer C. 2005. Regulation of glutamate transporter GLAST and GLT-1 expression in astrocytes by estrogen. Brain Res Mol Brain Res 138:1-7.
32. Rein T, Zorbas H, DePamphilis ML. 1997. Active mammalian replication origins are associated with a high-density cluster of mCpG dinucleotides. Mol Cell Biol 17:416-426.
33. Robertson KD, Wolffe AP. 2000. DNA methylation in health and disease. Nat Rev Genet 1:11-19.
34. Rothstein JD. 2002. Paving new pathways. Nat Med 8:938-940.
35. Rothstein JD, Jin L, Dykes-Hoberg M, Kuncl RW. 1993. Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc Natl Acad Sci USA 90:6591-6595.
36. Rothstein JD, Van Kammen M, Levey AI, Martin LJ, Kuncl RW. 1995. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol 38:73-84.
37. Scarpa S, Cavallaro RA, D'Anselmi F, Fuso A. 2006. Gene silencing through methylation: An epigenetic intervention on Alzheimer disease. J Alzheimers Dis 9:407-414.
38. Schlag BD, Vondrasek JR, Munir M, Kalandadze A, Zelenaia OA, Rothstein JD, Robinson MB. 1998. Regulation of the glial Na+-dependent glutamate transporters by cyclic AMP analogs and neurons. Mol Pharmacol 53:355-369.
39. Schluter K, Figiel M, Rozyczka J, Engele J. 2002. CNS region-specific regulation of glial glutamate transporter expression. Eur J Neurosci 16:836-842.
40. Seal RP, Amara SG. 1999. Excitatory amino acid transporters: A family in flux. Annu Rev Pharmacol Toxicol 39:431-456.
41. Sontheimer H. 2003. Malignant gliomas: Perverting glutamate and ion homeostasis for selective advantage. Trends Neurosci 26:543-549.
42. Su ZZ, Leszczyniecka M, Kang DC, Sarkar D, Chao W, Volsky DJ, Fisher PB. 2003. Insights into glutamate transport regulation in human astrocytes: Cloning of the promoter for excitatory amino acid transporter 2 (EAAT2). Proc Natl Acad Sci USA 100:1955-1960.
43. Takai D, Jones PA. 2002. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci USA 99:3740-3745.
44. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M, Taga T. 2001. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1:749-758.
45. 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.
46. Trotti D, Rolfs A, Danbolt NC, Brown RHJ, Hediger MA. 1999. SOD1 mutants linked to amyotrophic lateral sclerosis selectively inactivate a glial glutamate transporter. Nat Neurosci 2:427-433.
47. 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.
48. Ye ZC, Sontheimer H. 1999. Glioma cells release excitotoxic concentrations of glutamate. Cancer Res 59:4383-4391.
49. Yoshida M, Kijima M, Akita M, Beppu T. 1990. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J Biol Chem 265:17174-17179.
50. Zelenaia O, Schlag BD, Gochenauer GE, Ganel R, Song W, Beesley JS, Grinspan JB, Rothstein JD, Robinson MB. 2000. Epidermal growth factor receptor agonists increase expression of glutamate transporter GLT-1 in astrocytes through pathways dependent on phosphatidylinositol 3-kinase and transcription factor NF-kappaB. Mol Pharmacol 57:667-678.
51. Zhu Y, Parada LF. 2002. The molecular and genetic basis of neurological tumours. Nat Rev Cancer 2:616-626.
52. Zschocke J, Bayatti N, Behl C. 2005a. Caveolin and GLT-1 gene expression is reciprocally regulated in primary astrocytes: Association of GLT-1 with non-caveolar lipid rafts. Glia 49:275-287.
53. Zschocke J, Bayatti N, Clement AM, Witan H, Figiel M, Engele J, Behl C. 2005b. Differential promotion of glutamate transporter expression and function by glucocorticoids in astrocytes from various brain regions. J Biol Chem 280:34924-34932.