Epigenetic changes by zebularine leading to enhanced differentiation of human promyelocytic leukemia NB4 and KG1 cells

Molecular and Cellular Biochemistry

Volumn 359, Issue 1-2, 2012, Pages 245-261

  Savickiene, Jurate ^a   Treigyte, Grazina ^a   Jonusiene, Violeta ^a   Bruzaite, Renata ^a   Borutinskaite, Veronika Viktorija ^a   Navakauskiene, Ruta ^a  

^a VILNIUS UNIVERSITY   (Lithuania)

Author keywords

Differentiation; DNA methyltransferase inhibitors; E cadherin; Histone; Leukemia; p15

Indexed keywords

CD11B ANTIGEN; DNA METHYLTRANSFERASE 1; HISTONE H3; HISTONE H4; LIPOCORTIN 5; MYELOID DIFFERENTIATION FACTOR 88; PROCASPASE 3; PROPIDIUM IODIDE; PROTEIN P15; PROTEINASE ACTIVATED RECEPTOR 1; RETINOIC ACID; UVOMORULIN; ZEBULARINE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL SURVIVAL; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEMETHYLATION; EPIGENETICS; EVALUATION; GENETIC TRANSCRIPTION; GROWTH INHIBITION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; PROMOTER REGION; PROMYELOCYTIC LEUKEMIA; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TIME;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CYTIDINE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; EPIGENESIS, GENETIC; HUMANS; LEUKEMIA, PROMYELOCYTIC, ACUTE; TRETINOIN;

EID: 83555174910     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-011-1019-7     Document Type: Article

References (59)

1. H de The C Chomienne M Lanotte L Degos A Dejean 1990 The t (15;17) translocation of acute promyelocytic leukemia fuses the retinoic acid receptor α gene to a novel transcribed locus Nature 347 559 561
2. L-Z He E Guidez C Tribioli, et al. 1998 Distinct interactions of PML-RAR alpha and PLZF-RAR alpha with co-repressors determine differential responses to RA in APL Nat Genet 18 126 135 9462740 10.1038/ng0298-126 1:CAS:528: DyaK1cXosFOrsw%3D%3D (Pubitemid 28082458)
3. RJ Lin I Nagy S Inoque, et al. 1998 Role of histone deacetylase complex in acute promyelocytic leukemia Nature 391 811 814 9486654 10.1038/35895 1:CAS:528:DyaK1cXhtlCisr4%3D (Pubitemid 28099682)
4. F Grignani V Gelmetti M Fanelli, et al. 1999 Formation of PML/RAR alpha high molecular weight nuclear complexes through the PML coiled-coil region is essential for the PML/RAR alpha-mediated retinoic acid response Oncogene 18 6313 6321 10597230 10.1038/sj.onc.1203029 1:CAS:528:DyaK1MXnslKrtrs%3D
5. F Grignani PF Ferrucci U Testa, et al. 1993 The acute promyelocytic leukemia-specific PML- RARα fusion protein inhibits differentiation and promotes survival of myeloid precursor cells Cell 74 423 431 8394219 10.1016/0092-8674(93)80044-F 1:CAS:528:DyaK3sXmtVSkurk%3D (Pubitemid 23244608)
6. JA Dyck GG Maul WH Miller, et al. 1994 A novel macromolecular structure is a target of the promyelocytic-retinoic acid receptor Cell 76 333 343 8293467 10.1016/0092-8674(94)90340-9 1:CAS:528:DyaK2cXhs1Sgs7g%3D
7. Z Chen NJ Brand A Chen, et al. 1993 Fusion between a novel Kruppel-like zinc finger gene and the retinoic acid receptor-α locus due to a variant t (11; 17) translocation associated with acute promyelocytic leukemia EMBO J 12 1161 1167 8384553 1:CAS:528:DyaK3sXisFagtLc%3D (Pubitemid 23095865)
8. RL Redner J Wang JM Liu 1999 Chromatin remodeling and leukemia: new therapeutic paradigms Blood 94 417 428 10397708 1:CAS:528:DyaK1MXksVemt7o%3D (Pubitemid 29323855)
9. PG Lo Coco F Nervi C Look 2001 Histone deacetylase-targeted treatment restores retinoic acid signalling and differentiation in acute myeloid leukemia Cancer Res 61 2 7 11196162
10. SB Baylin JG Herman JR Graff PM Vertino JP Issa 1998 Alterations in DNA methylation: a fundamental aspect of neoplasia Adv Cancer Res 72 141 196 9338076 10.1016/S0065-230X(08)60702-2 1:CAS:528:DyaK2sXotVyktr8%3D (Pubitemid 27435555)
11. M Toyota KJ Kopecky MO Toyota, et al. 2001 Methylation profiling in acute myeloid leukemia Blood 97 2823 2829 11313277 10.1182/blood.V97.9.2823 1:CAS:528:DC%2BD3MXjtlShsro%3D
12. MF Paz MF Fraga S Avila, et al. 2003 A systematic profile of DNA methylation in human cancer cell lines Cancer Res 63 1114 1121 12615730 1:CAS:528:DC%2BD3sXhs1agtLo%3D (Pubitemid 36278446)
13. L Teofilini M Martini M Luongo, et al. 2003 Hypermethylation of CpG islands in the promoter region of p15 (INK4b) in acute promyelocytic leukemia represses p15 (INK4b) expression and correlates with poor prognosis Leukemia 17 919 924 10.1038/sj.leu.2402907 (Pubitemid 36626320)
14. CG Ekmekci MI Gutierrez AK Siraj, et al. 2004 Aberrant methylation of multiple tumor suppressor genes in acute myeloid leukemia Am J Hematol 77 233 240 15495254 10.1002/ajh.20186 1:CAS:528:DC%2BD2cXhtVenurrP (Pubitemid 39430701)
15. INK4b Cancer Res 56 722 727 8631003 1:CAS:528:DyaK28XhtVCls7Y%3D
16. JG Herman CI Civin JP Issa, et al. 1997 Distinct patterns of inactivation of p15INK4B and p16INK4A characterize the major types of hematological malignancies Cancer Res 57 837 841 9041182 1:CAS:528:DyaK2sXhs1Kisrc%3D (Pubitemid 27098005)
17. INK4B CpG island methylation in primary acute leukemia is heterogeneous and suggests density as a critical factor for transcriptional silencing Blood 94 2445 2451 10498617 1:CAS:528:DyaK1MXmsVCitrs%3D (Pubitemid 29467693)
18. CS Chim R Liang CYY Ram YL Kwong 2002 Methylation of p15 and p16 genes in acute promyelocytic leukemia: potential diagnostic and prognostic significance J Clin Oncol 19 2033 2040 (Pubitemid 32702548)
19. S Agrawal M Utenberg S Koschmieder, et al. 2007 DNA methylation of tumour suppressor genes in clinical remission predicts the relapse risk in acute myeloid leukaemia Cancer Res 67 1370 1377 17283175 10.1158/0008-5472.CAN-06-1681 1:CAS:528:DC%2BD2sXht1ynt70%3D
20. JE Dodge C Minson AF List 2001 KG-1 and KG1a model the p15 CpG island methylation observed in acute myeloid leukaemia patients Leuk Res 25 917 925 11532526 10.1016/S0145-2126(01)00053-4 1:CAS:528:DC%2BD3MXmsFWrtrg%3D (Pubitemid 32776583)
21. H Nayera MD Shakankiry I Ghada MD Mossallam 2006 p15 (INK4B) and E-cadherin island methylation is frequent in Egyptian acute myeloid leukemia J Egypt Nat Cancer Inst 18 227 232
22. T Berg Y Guo M Abdekkarim M Fliegauft M Lubbert 2007 Reversal of p15/Ink4b hypermethylation in AML1/ETO-positive and-negative myeloid leukemia cell lines Leuk Res 31 496 506 10.1016/j.leukres.2006.08.008 (Pubitemid 46206089)
23. LA Ribeiro-Filho J Franks M Sasaki, et al. 2002 CpG hypermethylation of promoter region and inactivation of E-cadherin gene in human bladder cancer Mol Carcinog 34 187 198 12203370 10.1002/mc.10064 1:CAS:528:DC%2BD38Xmtlertr0%3D (Pubitemid 34840002)
24. PG Corn BD Smith ES Rukdeschel, et al. 2000 E-cadherin expression is silenced by 5′ CpG island methylation in acute myeloid leukemia Clin Cancer Res 6 4243 4248 11106238 1:CAS:528:DC%2BD3cXovVSgtbk%3D
25. JR Melki PC Vincent RD Brown SJ Clark 2000 Hypermethylation of E-cadherin in leukemia Blood 95 3208 3213 10807790 1:CAS:528:DC%2BD3cXjt1Cjs78%3D (Pubitemid 30321175)
26. T Shimamoto JH Ohyashiki K Ohyashiki 2005 Methylation of p15 (INK4b) and E-cadherin genes is independently correlated with poor prognosis in acute myeloid leukemia Leuk Res 6 653 659 10.1016/j.leukres.2004.11.014 (Pubitemid 40603565)
27. NJ Farinha S Shaker M Lemaire, et al. 2004 Activation of expression of p15, p73 and E-cadherin in leukemic cells by different concentrations of 5-aza-2′-deoxycytidine (decitabine) Anticancer Res 24 75 78 15015578 1:CAS:528:DC%2BD2cXisFGntb8%3D (Pubitemid 38279690)
28. C Mund B Brueckner F Lyko 2006 Reactivation of epigenetically silenced genes by DNA methyltransferase inhibitors: basic concepts and clinical applications Epigenetics 1 7 13 17998812 10.4161/epi.1.1.2375
29. JK Christman 2002 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy Oncogene 21 5483 5495 12154409 10.1038/sj.onc.1205699 1:CAS:528:DC%2BD38XlslSqtLw%3D (Pubitemid 34983483)
30. M Lubbert 2000 DNA methylation inhibitors in the treatment of leukemias, myelodisplastic syndromes and hemoglobinopathies: clinical results and possible mechanisms of action Curr Top Microbiol Immunol 249 135 164 10802943 10.1007/978-3-642-59696-4-9 1:CAS:528:DC%2BD3cXis1ykurg%3D (Pubitemid 30134342)
31. C Stresemann B Brueckner T Musch, et al. 2006 Functional diversity of DNA methyltransferase inhibitors in human cancer cell lines Cancer Res 66 2080 2794 10.1158/0008-5472.CAN-05-2821
32. CH Kim VE Marquez DT Mao, et al. 1986 Synthesis of pyrimidin-2-one nucleosides as acid-stable inhibitors of cytidine deaminase J Med Chem 29 1374 1380 3735306 10.1021/jm00158a009 1:CAS:528:DyaL28Xks1Sru70%3D (Pubitemid 16034624)
33. PJ Hurd AJ Whistmatsh GS Baldwin, et al. 1999 Mechanism-based inhibition of C5-cytosine DNA methyltransferases by 2-H pyrimidone J Mol Biol 286 389 401 9973559 10.1006/jmbi.1998.2491 1:CAS:528:DyaK1MXhtV2gs7s%3D (Pubitemid 29090158)
34. L Zhou X Cheng BA Connolly, et al. 2002 Zebularine: a novel DNA methylation inhibitor that forms a covalent complex with DNA methyltransferases J Mol Biol 23 581 599
35. JC Cheng CB Matsen FA Gonzales, et al. 2003 Inhibition of DNA methylation and reactivation of silenced genes by zebularine J Natl Cancer Inst 95 399 409 12618505 10.1093/jnci/95.5.399 1:CAS:528:DC%2BD3sXivVeqs74%3D (Pubitemid 36395260)
36. VE Marquez JA Kelly R Agbaria, et al. 2005 Zebularine: a unique molecule for an epigenetically based strategy in cancer chemotherapy Ann N Y Acad Sci 1008 246 254 10.1196/annals.1359.037
37. JC Cheng DJ Weisenberger FA Gonzales, et al. 2004 Continuous zebularine treatment effectively sustains demethylation in human bladder cancer cells Mol Cell Biol 24 1270 1278 14729971 10.1128/MCB.24.3.1270-1278.2004 1:CAS:528:DC%2BD2cXmsFWmsw%3D%3D (Pubitemid 38112188)
38. SA Scott A Lakshimikuttysamma DP Sheridan, et al. 2007 Zebularine inhibits human myeloid leukemia cell growth in vitro in association with p15INK4B demethylation and reexpression Exp Hematol 35 263 273 17258075 10.1016/j.exphem.2006.10.005 1:CAS:528:DC%2BD2sXhtVarsrc%3D (Pubitemid 46135814)
39. S Veerla I Panagopoulos Y Jin, et al. 2008 Promoter analysis of epigenetically controlled genes in bladder cancer Genes Chromosom Cancer 47 358 378 10.1002/gcc.20542 (Pubitemid 351451791)
40. S Collins 1987 The HL-60 promyelocytic leukemia cell line: proliferation, differentiation and cellular oncogene expression Blood 70 1233 1244 3311197 1:CAS:528:DyaL1cXjsFGmtg%3D%3D (Pubitemid 18026122)
41. AL Clayton S Rose MJ Barrat LC Mahadevan 2000 Phosphoacetylation of histone H3 on c-fos- and c-jun-associated nucleosomes upon gene activation EMBO J 19 3714 3726 10899125 10.1093/emboj/19.14.3714 1:CAS:528:DC%2BD3cXmtlegs7k%3D (Pubitemid 30462129)
42. A El-Osta P Kandharidis JR Zalcberg AP Wolffe 2002 Precipitous release of methyl-CpG binding protein 2 and histone deacetylase 1 from the methylated human multidrug resistance gene (MDR1) on activation Mol Cell Biol 22 1844 1857 11865062 10.1128/MCB.22.6.1844-1857.2002 1:CAS:528:DC%2BD38XitVWjtbo%3D (Pubitemid 34175000)
43. J Savickiene V-V Borutinskaite G Treigyte, et al. 2006 The novel histone deacetylase inhibitor BML-210 exerts growth inhibitory, proapoptotic and differentiation stimulating effects on human leukemia cell lines Europ J Pharmacol 549 9 18 10.1016/j.ejphar.2006.08.010 1:CAS:528:DC%2BD28XhtVWqu7zN (Pubitemid 44441256)
44. J Savickiene G Treigyte K-E Magnusson R Navakauskiene 2009 Response of retinoic acid-resistant KG1 cells to combination of retinoic acid with diverse histone deacetylase inhibitors Ann NY Acad Sci 1171 321 333 19723072 10.1111/j.1749-6632.2009.04718.x 1:CAS:528:DC%2BD1MXht1SntbjJ
45. JC Cheng CB Yoo DJ Weisenberger J Chuang, et al. 2004 Preferential response of cancer cells to zebularine Cancer Cell 6 151 158 15324698 10.1016/j.ccr.2004.06.023 1:CAS:528:DC%2BD2cXns1arsro%3D (Pubitemid 39485687)
46. F Fazi L Travaglini D Carotti F Palitti, et al. 2005 Retinoic acid targets DNA-methyltransferases and histone deacetylases during APL blast differentiation in vitro and in vivo Oncogene 24 1820 1830 15688037 10.1038/sj.onc.1208286 1:CAS:528:DC%2BD2MXitV2nsrs%3D (Pubitemid 40462785)
47. M Serrano GJ Hannon D Beach 1993 A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4 Nature 366 704 707 8259215 10.1038/366704a0 1:CAS:528:DyaK2cXhsFOgu7Y%3D (Pubitemid 24036021)
48. HG Drexler 1998 Review of alterations of the cyclin-dependent kinase inhibitor INK4 family genes, p15, p16, p18 and p19 in human leukemia-lymphoma cells Leukemia 12 845 859 9639410 10.1038/sj.leu.2401043 1:CAS:528: DyaK1cXkt1Kiuro%3D (Pubitemid 28287205)
49. JE Dodge AF List BW Fitscher 1998 Selective variegated methylation of the p15 island in acute myeloid leukemia Int J Cancer 78 561 567 9808523 10.1002/(SICI)1097-0215(19981123)78:5<561::AID-IJC6>3.0.CO;2-R 1:CAS:528:DyaK1cXns1Cgsb4%3D (Pubitemid 28507178)
50. PR Solomon AK Munirajan N Tsuchida, et al. 2008 Promoter hypermethylation analysis in myeloplastic syndromes: diagnostic and prognostic implication Indian J Med Res 127 52 57 18316853 1:CAS:528:DC%2BD1cXksFKis74%3D (Pubitemid 351663566)
51. JM Halbleib WJ Nelson 2006 Cadherins in development: cell adhesion, sorting, and tissue morphogenesis Genes Dev 20 3199 3214 17158740 10.1101/gad.1486806 1:CAS:528:DC%2BD28XhtlSmt7vJ (Pubitemid 44904842)
52. M Grunstein 1997 Histone acetylation in chromatin structure and transcription Nature 389 349 352 9311776 10.1038/38664 1:CAS:528: DyaK2sXmsVWntLk%3D (Pubitemid 27415209)
53. T Kouzarides 2002 Histone methylation in transcriptional control Curr Opin Genet Dev 12 198 209 11893494 10.1016/S0959-437X(02)00287-3 1:CAS:528:DC%2BD38XhvVCnsbY%3D (Pubitemid 34219493)
54. MD Litt M Simpson M Gaszner, et al. 2001 Correlation between histone lysine methylation and development changes at the chicken beta-globin locus Science 28 2453 24555 10.1126/science.1064413 (Pubitemid 32917326)
55. J Nakayama JC Rice BD Strahl, et al. 2001 Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly Science 292 110 113 11283354 10.1126/science.1060118 1:CAS:528:DC%2BD3MXis1Grt78%3D (Pubitemid 32289138)
56. PL Jones GJ Veenstra PA Wade, et al. 1998 Methylated DNA and MecP2 recruit histone deacetylase to repress transcription Nat Genet 19 181 187 10.1038/561 (Pubitemid 28248804)
57. CT Nguyen DJ Weisenberger M Valicescu, et al. 2002 Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-Aza-2′-deoxycytidine Cancer Res 62 6456 6461 12438235 1:CAS:528:DC%2BD38XovFOlu7o%3D (Pubitemid 35364106)
58. G Lagger A Doetzlhofer B Scuettengruber, et al. 2003 The tumor suppressor p53 and histone deacetylase 1 are antagonistic regulators of the cyclin-dependent kinase inhibitor p21/WAF1/CIP1 gene Mol Cell Biol 23 2669 2679 12665570 10.1128/MCB.23.8.2669-2679.2003 1:CAS:528:DC%2BD3sXktV2lsbo%3D (Pubitemid 36403069)
59. SA Scott WF Dong R Ichinohasama, et al. 2006 5-Aza-2′-deoxycytidine (decitabine) can relieve p21WAF1 repression in human acute myeloid leukemia by a mechanism involving release of histone deacetylase 1 (HDAC1) without requiring p21WAF1 promoter demethylation Leuk Res 30 69 76 16043219 10.1016/j.leukres. 2005.05.010 1:CAS:528:DC%2BD2MXht1GnsL3K (Pubitemid 41654707)