The CpG island shore of the GLT-1 gene acts as a methylation-sensitive enhancer

GLIA

Volumn 60, Issue 9, 2012, Pages 1345-1355

  Perisic, Tatjana ^a   Holsboer, Florian ^a   Rein, Theo ^a   Zschocke, Jürgen ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Astrocytes; DNA methylation; EAAT2; Epigenetics; Histones

Indexed keywords

DEXAMETHASONE; DNA; GLUTAMIC ACID; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; HISTONE H4; SODIUM GLUCOSE COTRANSPORTER 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN REGION; CEREBELLUM; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ENHANCER REGION; EPIGENETICS; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM;

ANIMALS; ASTROCYTES; BRAIN; CELLS, CULTURED; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; EXCITATORY AMINO ACID TRANSPORTER 2; HISTONES; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84863996658     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22353     Document Type: Article

References (55)

1. Allritz C, Bette S, Figiel M, Engele J. 2009. Endothelin-1 reverses the histone deacetylase inhibitor-induced increase in glial glutamate transporter transcription without affecting histone acetylation levels. Neurochem Int 55: 22-27.
2. Allritz C, Bette S, Figiel M, Engele J. 2010. Comparative structural and functional analysis of the GLT-1/EAAT-2 promoter from man and rat. J Neurosci Res 88: 1234-1241.
3. Anderson CM, Swanson RA. 2000. Astrocyte glutamate transport: Review of properties, regulation, and physiological functions. Glia 32: 1-14.
4. Banine F, Matagne V, Sherman LS, Ojeda SR. 2011. Brain region-specific expression of Fxyd1, an Mecp2 target gene, is regulated by epigenetic mechanisms. J Neurosci Res 89: 840-851.
5. Bernstein BE, Mikkelsen TS, Xie XH, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
6. Bird AP. 1986. CpG-rich islands and the function of DNA methylation. Nature 321: 209-213.
7. Bose R, Moors M, Tofighi R, Cascante A, Hermanson O, Ceccatelli S. 2010. Glucocorticoids induce long-lasting effects in neural stem cells resulting in senescence-related alterations. Cell Death Dis 1: e92.
8. Brandeis M, Frank D, Keshet I, Siegfried Z, Mendelsohn M, Nemes A, Temper V, Razin A, Cedar H. 1994. Sp1 elements protect a CpG island from de novo methylation. Nature 371: 435-438.
9. Buira SP, Dentesano G, Albasanz JL, Moreno J, Martin M, Ferrer I, Barrachina M. 2010. DNA methylation and Yin Yang-1 repress adenosine A(2A) receptor levels in human brain. J Neurochem 115: 283-295.
10. Campanero MR, Armstrong MI, Flemington EK. 2000. CpG methylation as a mechanism for the regulation of E2F activity. Proc Natl Acad Sci USA 97: 6481-6486.
11. Chen W, Aoki C, Mahadomrongkul V, Gruber CE, Wang GJ, Blitzblau R, Irwin N, Rosenberg PA. 2002. Expression of a variant form of the glutamate transporter GLT1 in neuronal cultures and in neurons and astrocytes in the rat brain. J Neurosci 22: 2142-2152.
12. D'Alessio AC, Szyf M. 2006. Epigenetic tete-a-tete: The bilateral relationship between chromatin modifications and DNA methylation. Biochem Cell Biol 84: 463-476.
13. Doi A, Park IH, Wen B, Murakami P, Aryee MJ, Irizarry R, Herb B, Ladd-Acosta C, Rho JS, Loewer S, Miller J, Schlaeger T, Daley GQ, Feinberg AP. 2009. Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet 41: 1350-U123.
14. Espinas ML, Roux J, Ghysdael J, Pictet R, Grange T. 1994. Participation of ETS transcription factors in the glucocorticoid response of the rat tyrosine aminotransferase gene. Mol Cell Biol 14: 4116-4125.
15. Feber A, Wilson GA, Zhang L, Presneau N, Idowu B, Down TA, Rakyan VK, Noon LA, Lloyd AC, Stupka E, Schiza V, Teschendorff AE, Schroth GP, Flanagan A, Beck S. 2011. Comparative methylome analysis of benign and malignant peripheral nerve sheath tumors. Genome Res 21: 515-524.
16. Franchimont DP, Galon J, Gadina M, Visconti R, Chrousos GP, O'Shea JJ. 2000. Inhibition of Th1 immune response by glucocorticoids: Dexamethasone inhibits IL-12-induced Stat4 phosphorylation in T lymphocytes. Gastroenterology 118: A790-A791.
17. Franke B, Figiel M, Engele J. 1998. CNS glia are targets for GDNF and neurturin. Histochem Cell Biol 110: 595-601.
18. Freeman MR. 2010. Specification and morphogenesis of astrocytes. Science 330: 774-778.
19. Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T. 2000. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 24: 88-91.
20. Furuta A, Rothstein JD, Martin LJ. 1997. Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17: 8363-8375.
21. 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.
22. Iguchiariga SMM, Schaffner W. 1989. CpG methylation of the cAMP-responsive enhancer promoter sequence TGACGTCA abolishes specific factor binding as well as transcriptional activation. Gene Dev 3: 612-619.
23. Irizarry RA, Ladd-Acosta C, Wen B, Wu ZJ, Montano C, Onyango P, Cui HM, Gabo K, Rongione M, Webster M, Ji H, Potash JB, Sabunciyan S, Feinberg AP. 2009. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 41: 178-186.
24. Johnson LM, Cao XF, Jacobsen SE. 2002. Interplay between two epigenetic marks: DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12: 1360-1367.
25. Jones PL, Veenstra GJC, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP. 1998. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19: 187-191.
26. Klug M, Rehli M. 2006. Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics 1: 127-130.
27. Lachner M, Jenuwein T. 2002. The many faces of histone lysine methylation. Curr Opin Cell Biol 14: 286-298.
28. Ladd-Acosta C, Pevsner J, Sabunciyan S, Yolken RH, Webster MJ, Dinkins T, Callinan PA, Fan JB, Potash JB, Feinberg AP. 2007. DNA methylation signatures within the human brain. Am J Hum Genet 81: 1304-1315.
29. Lee RS, Tamashiro KLK, Yang XJ, Purcell RH, Harvey A, Willour VL, Huo YQ, Rongione M, Wand GS, Potash JB. 2010. Chronic corticosterone exposure increases expression and decreases deoxyribonucleic acid methylation of Fkbp5 in mice. Endocrinology 151: 4332-4343.
30. Letwin NE, Kafkafi N, Benjamini Y, Mayo C, Frank BC, Luu T, Lee NH, Elmer GI. 2006. Combined application of behavior genetics and microarray analysis to identify regional expression themes and gene-behavior associations. J Neurosci 26: 5277-5287.
31. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408.
32. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, Johnson BE, Hong CB, Nielsen C, Zhao YJ, Turecki G, Delaney A, Varhol R, Thiessen N, Shchors K, Heine VM, Rowitch DH, Xing XY, Fiore C, Schillebeeckx M, Jones SJM, Haussler D, Marra MA, Hirst M, Wang T, Costello JF. 2010. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466: 253-U131.
33. Meaney MJ. 2010. Epigenetics and the biological definition of gene x environment interactions. Child Dev 81: 41-79.
34. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, Bibel M, Schubeler D. 2008. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30: 755-766.
35. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmuhl Y, Fischer D, Holsboer F, Wotjak CT, Almeida OFX, Spengler D. 2009. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 12: 1559-U108.
36. 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.
37. Nan XS, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386-389.
38. Perisic T, Zimmermann N, Kirmeier T, Asmus M, Tuorto F, Uhr M, Holsboer F, Rein T, Zschocke J. 2010. Valproate and amitriptyline exert common and divergent influences on global and gene promoter-specific chromatin modifications in rat primary astrocytes. Neuropsychopharmacology 35: 792-805.
39. Plachez C, Danbolt NC, Récasens M. 2000. Transient expression of the glial glutamate transporters GLAST and GLT in hippocampal neurons in primary culture. J Neurosci Res 59: 587-593.
40. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, Bell GW, Walker K, Rolfe PA, Herbolsheimer E, Zeitlinger J, Lewitter F, Gifford DK, Young RA. 2005. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517-527.
41. Schluter K, Figiel M, Rozyczka J, Engele J. 2002. CNS region-specific regulation of glial glutamate transporter expression. Eur J Neurosci 16: 836-842.
42. Schmidl C, Klug M, Boeld TJ, Andreesen R, Hoffmann P, Edinger M, Rehli M. 2009. Lineage-specific DNA methylation in T cells correlates with histone methylation and enhancer activity. Genome Res 19: 1165-1174.
43. Schülke JP, Wochnik GM, Lang-Rollin I, Gassen NC, Knapp RT, Berning B, Yassouridis A, Rein T. 2010. Differential impact of tetratricopeptide repeat proteins on the steroid hormone receptors. PloS ONE 5:e11717.
44. Song MR, Ghosh A. 2004. FGF2-induced chromatin remodeling regulates CNTF-mediated gene expression and astrocyte differentiation. Nat Neurosci 7: 229-235.
45. Stadler F, Kolb G, Rubusch L, Baker SP, Jones EG, Akbarian S. 2005. Histone methylation at gene promoters is associated with developmental regulation and region-specific expression of ionotropic and metabotropic glutamate receptors in human brain. J Neurochem 94: 324-336.
46. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M. 2001. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1: 749-758.
47. Tao YZ, Neppl RL, Huang ZP, Chen JF, Tang RH, Cao R, Zhang Y, Jin SW, Wang DZ. 2011. The histone methyltransferase Set7/9 promotes myoblast differentiation and myofibril assembly. J Cell Biol 194: 551-565.
48. van der Laan S, de Kloet ER, Meijer OC. 2009. Timing is critical for effective glucocorticoid receptor mediated repression of the cAMP-induced CRH gene. PloS ONE 4
49. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM, Bollen M, Esteller M, Di Croce L, de Launoit Y, Fuks F. 2006. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439: 871-874.
50. Wochnik GM, Ruegg J, Abel GA, Schmidt U, Holsboer F, Rein T. 2005. FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. J Biol Chem 280: 4609-4616.
51. Wong CM, Wong CCL, Ng YL, Au SLK, Ko FCF, Ng IOL. 2011. Transcriptional repressive H3K9 and H3K27 methylations contribute to DNMT1-mediated DNA methylation recovery. PloS ONE 6:e16702.
52. Xiong ZG, Laird PW. 1997. COBRA: A sensitive and quantitative DNA methylation assay. Nucleic Acids Res 25: 2532-2534.
53. Yang YJ, Gozen O, Vidensky S, Robinson MB, Rothstein JD. 2010. Epigenetic regulation of neuron-dependent induction of astroglial synaptic protein GLT1. Glia 58: 277-286.
54. Zschocke J, Allritz C, Engele J, Rein T. 2007. DNA methylation dependent silencing of the human glutamate transporter EAAT2 gene in glial cells. Glia 55: 663-674.
55. Zschocke J, Bayatti N, Clement AM, Witan H, Figiel M, Engele J, Behl C. 2005. Differential promotion of glutamate transporter expression and function by glucocorticoids in astrocytes from various brain regions. J Biol Chem 280: 34924-34932.