Reversible epigenetic fingerprint-mediated glutathione-S-transferase P1 gene silencing in human leukemia cell lines

Biochemical Pharmacology

Volumn 81, Issue 11, 2011, Pages 1329-1342

  Karius, Tommy ^a   Schnekenburger, Michael ^a   Ghelfi, Jenny ^a   Walter, Jörn ^b   Dicato, Mario ^a   Diederich, Marc ^a  

^a LABORATOIRE DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE DU CANCER   (Luxembourg)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

Chromatin; DNA methylation; Epigenetic silencing; GSTP1; Leukemia

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; BISULFITE; CELL PROTEIN; GLUTATHIONE TRANSFERASE; HISTONE;

ARTICLE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; CPG ISLAND; DEACETYLATION; DEMETHYLATION; DNA FINGERPRINTING; DNA METHYLATION; EPIGENETICS; GENE ACTIVATION; GENE REPRESSION; GENE SEQUENCE; GENE SILENCING; HISTONE MODIFICATION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; LEUKEMIA CELL LINE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RESTRICTION MAPPING; TRANSCRIPTION REGULATION;

BASE SEQUENCE; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; DNA METHYLATION; DNA PRIMERS; EPIGENESIS, GENETIC; GENE SILENCING; GLUTATHIONE S-TRANSFERASE PI; HUMANS; LEUKEMIA; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 79955610018     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2011.03.014     Document Type: Article

References (49)

1. S.B. Baylin, M. Esteller, M.R. Rountree, K.E. Bachman, K. Schuebel, and J.G. Herman Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer Hum Mol Genet 10 2001 687 692 (Pubitemid 32331576)
2. M. Esteller Aberrant DNA methylation as a cancer-inducing mechanism Annu Rev Pharmacol Toxicol 45 2005 629 656 (Pubitemid 40261820)
3. M. Esteller CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future Oncogene 21 2002 5427 5440 (Pubitemid 34983479)
4. G.A. Garinis, G.P. Patrinos, N.E. Spanakis, and P.G. Menounos DNA hypermethylation: when tumour suppressor genes go silent Hum Genet 111 2002 115 127 (Pubitemid 36075029)
5. S.M. Iguchi-Ariga, and W. Schaffner CpG methylation of the cAMP-responsive enhancer/promoter sequence TGACGTCA abolishes specific factor binding as well as transcriptional activation Genes Dev 3 1989 612 619
6. M.R. Rountree, and E.U. Selker DNA methylation inhibits elongation but not initiation of transcription in Neurospora crassa Genes Dev 11 1997 2383 2395 (Pubitemid 27408535)
7. J.M. Craig Heterochromatin - many flavours, common themes Bioessays 27 2005 17 28 (Pubitemid 40128619)
8. K.D. Robertson, and A.P. Wolffe DNA methylation in health and disease Nat Rev Genet 1 2000 11 19
9. E. Heard, C. Rougeulle, D. Arnaud, P. Avner, C.D. Allis, and D.L. Spector Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation Cell 107 2001 727 738 (Pubitemid 34033666)
10. M.R. Rountree, K.E. Bachman, J.G. Herman, and S.B. Baylin DNA methylation, chromatin inheritance, and cancer Oncogene 20 2001 3156 3165 (Pubitemid 32553571)
11. J. Tazi, and A. Bird Alternative chromatin structure at CpG islands Cell 60 1990 909 920
12. D. Schubeler, D.M. MacAlpine, D. Scalzo, C. Wirbelauer, C. Kooperberg, and F. van Leeuwen The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote Genes Dev 18 2004 1263 1271 (Pubitemid 38720594)
13. S.L. Berger The complex language of chromatin regulation during transcription Nature 447 2007 407 412 (Pubitemid 46816746)
14. J.L. Wright, and P.H. Lange Newer potential biomarkers in prostate cancer Rev Urol 9 2007 207 213
15. P. Cairns, M. Esteller, J.G. Herman, M. Schoenberg, C. Jeronimo, and M. Sanchez-Cespedes Molecular detection of prostate cancer in urine by GSTP1 hypermethylation Clin Cancer Res 7 2001 2727 2730 (Pubitemid 32911377)
16. W.B. Jakoby The glutathione S-transferases: a group of multifunctional detoxification proteins Adv Enzymol Relat Areas Mol Biol 46 1978 383 414
17. N.W. Chow, J. Whang-Peng, C.S. Kao-Shan, M.F. Tam, H.C. Lai, and C.P. Tu Human glutathione S-transferases. The Ha multigene family encodes products of different but overlapping substrate specificities J Biol Chem 263 1988 12797 12800
18. F. Morceau, A. Duvoix, S. Delhalle, M. Schnekenburger, M. Dicato, and M. Diederich Regulation of glutathione S-transferase P1-1 gene expression by NF-kappaB in tumor necrosis factor alpha-treated K562 leukemia cells Biochem Pharmacol 67 2004 1227 1238 (Pubitemid 38315088)
19. G.J. Moffat, A.W. McLaren, and C.R. Wolf Sp1-mediated transcriptional activation of the human Pi class glutathione S-transferase promoter J Biol Chem 271 1996 1054 1060
20. A. Duvoix, M. Schnekenburger, S. Delhalle, R. Blasius, P. Borde-Chiche, and F. Morceau Expression of glutathione S-transferase P1-1 in leukemic cells is regulated by inducible AP-1 binding Cancer Lett 216 2004 207 219 (Pubitemid 39463325)
21. W.H. Lee, R.A. Morton, J.I. Epstein, J.D. Brooks, P.A. Campbell, and G.S. Bova Cytidine methylation of regulatory sequences near the pi-class glutathione S-transferase gene accompanies human prostatic carcinogenesis Proc Natl Acad Sci USA 91 1994 11733 11737 (Pubitemid 24356419)
22. R. Singal, J. van Wert, and M. Bashambu Cytosine methylation represses glutathione S-transferase P1 (GSTP1) gene expression in human prostate cancer cells Cancer Res 61 2001 4820 4826 (Pubitemid 32691897)
23. P. Borde-Chiche, M. Diederich, F. Morceau, A. Puga, M. Wellman, and M. Dicato Regulation of transcription of the glutathione S-transferase P1 gene by methylation of the minimal promoter in human leukemia cells Biochem Pharmacol 61 2001 605 612 (Pubitemid 32178495)
24. X. Lin, and W.G. Nelson Methyl-CpG-binding domain protein-2 mediates transcriptional repression associated with hypermethylated GSTP1 CpG islands in MCF-7 breast cancer cells Cancer Res 63 2003 498 504 (Pubitemid 36152513)
25. W.H. Lee, W.B. Isaacs, G.S. Bova, and W.G. Nelson CG island methylation changes near the GSTP1 gene in prostatic carcinoma cells detected using the polymerase chain reaction: a new prostate cancer biomarker Cancer Epidemiol Biomarkers Prev 6 1997 443 450 (Pubitemid 27270550)
26. J.C. Tchou, X. Lin, D. Freije, W.B. Isaacs, J.D. Brooks, and A. Rashid GSTP1 CpG island DNA hypermethylation in hepatocellular carcinomas Int J Oncol 16 2000 663 676
27. M. Esteller, P.G. Corn, J.M. Urena, E. Gabrielson, S.B. Baylin, and J.G. Herman Inactivation of glutathione S-transferase P1 gene by promoter hypermethylation in human neoplasia Cancer Res 58 1998 4515 4518 (Pubitemid 28480605)
28. M.S. Jhaveri, and C.S. Morrow Methylation-mediated regulation of the glutathione S-transferase P1 gene in human breast cancer cells Gene 210 1998 1 7 (Pubitemid 28156380)
29. M. Schnekenburger, F. Morceau, A. Duvoix, S. Delhalle, C. Trentesaux, and M. Dicato Expression of glutathione S-transferase P1-1 in differentiating K562: role of GATA-1 Biochem Biophys Res Commun 311 2003 815 821 (Pubitemid 37393391)
30. R.M. Brena, H. Auer, K. Kornacker, and C. Plass Quantification of DNA methylation in electrofluidics chips (Bio-COBRA) Nat Protoc 1 2006 52 58
31. J.E. Ruscoe, L.A. Rosario, T. Wang, L. Gate, P. Arifoglu, and C.R. Wolf Pharmacologic or genetic manipulation of glutathione S-transferase P1-1 (GSTpi) influences cell proliferation pathways J Pharmacol Exp Ther 298 2001 339 345 (Pubitemid 32574545)
32. V. Greger, E. Passarge, W. Hopping, E. Messmer, and B. Horsthemke Epigenetic changes may contribute to the formation and spontaneous regression of retinoblastoma Hum Genet 83 1989 155 158 (Pubitemid 19234564)
33. M. Esteller, P.G. Corn, S.B. Baylin, and J.G. Herman A gene hypermethylation profile of human cancer Cancer Res 61 2001 3225 3229 (Pubitemid 32695003)
34. M. Nakayama, M.L. Gonzalgo, S. Yegnasubramanian, X. Lin, A.M. De Marzo, and W.G. Nelson GSTP1 CpG island hypermethylation as a molecular biomarker for prostate cancer J Cell Biochem 91 2004 540 552
35. T.C. Shea, S.L. Kelley, and W.D. Henner Identification of an anionic form of glutathione transferase present in many human tumors and human tumor cell lines Cancer Res 48 1988 527 533 (Pubitemid 18056516)
36. C. Goessl, H. Krause, M. Muller, R. Heicappell, M. Schrader, and J. Sachsinger Fluorescent methylation-specific polymerase chain reaction for DNA-based detection of prostate cancer in bodily fluids Cancer Res 60 2000 5941 5945
37. M. Esteller, M. Sanchez-Cespedes, R. Rosell, D. Sidransky, S.B. Baylin, and J.G. Herman Detection of aberrant promoter hypermethylation of tumor suppressor genes in serum DNA from non-small cell lung cancer patients Cancer Res 59 1999 67 70 (Pubitemid 29062958)
38. W.M. Grady, A. Rajput, J.D. Lutterbaugh, and S.D. Markowitz Detection of aberrantly methylated hMLH1 promoter DNA in the serum of patients with microsatellite unstable colon cancer Cancer Res 61 2001 900 902 (Pubitemid 32174399)
39. C. Goessl, M. Muller, R. Heicappell, H. Krause, and K. Miller DNA-based detection of prostate cancer in blood, urine, and ejaculates Ann NY Acad Sci 945 2001 51 58 (Pubitemid 33022431)
40. N.R. dos Santos, R. Torensma, T.J. de Vries, M.W. Schreurs, D.R. de Bruijn, and E. Kater-Baats Heterogeneous expression of the SSX cancer/testis antigens in human melanoma lesions and cell lines Cancer Res 60 2000 1654 1662 (Pubitemid 30183438)
41. E.E. Cameron, K.E. Bachman, S. Myohanen, J.G. Herman, and S.B. Baylin Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer Nat Genet 21 1999 103 107 (Pubitemid 29036293)
42. M.A. Harrington, P.A. Jones, M. Imagawa, and M. Karin Cytosine methylation does not affect binding of transcription factor Sp1 Proc Natl Acad Sci USA 85 1988 2066 2070 (Pubitemid 24315829)
43. M. Holler, G. Westin, J. Jiricny, and W. Schaffner Sp1 transcription factor binds DNA and activates transcription even when the binding site is CpG methylated Genes Dev 2 1988 1127 1135
44. X. Nan, H.H. Ng, C.A. Johnson, C.D. Laherty, B.M. Turner, and R.N. Eisenman Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex Nature 393 1998 386 389 (Pubitemid 28269714)
45. P.L. Jones, G.J. Veenstra, P.A. Wade, D. Vermaak, S.U. Kass, and N. Landsberger Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription Nat Genet 19 1998 187 191 (Pubitemid 28248804)
46. P.A. Jones, and S.B. Baylin The fundamental role of epigenetic events in cancer Nat Rev Genet 3 2002 415 428 (Pubitemid 34587077)
47. X. Lin, M. Tascilar, W.H. Lee, W.J. Vles, B.H. Lee, and R. Veeraswamy GSTP1 CpG island hypermethylation is responsible for the absence of GSTP1 expression in human prostate cancer cells Am J Pathol 159 2001 1815 1826 (Pubitemid 33062524)
48. K.W. Kinzler, and B. Vogelstein Cancer-susceptibility genes. Gatekeepers and caretakers Nature 386 1997 761 763
49. B. Ketterer Glutathione S-transferases and prevention of cellular free radical damage Free Radic Res 28 1998 647 658 (Pubitemid 28454257)