Epigenetic silencing of BIM in glucocorticoid poor-responsive pediatric acute lymphoblastic leukemia, and its reversal by histone deacetylase inhibition

Blood

Volumn 116, Issue 16, 2010, Pages 3013-3022

  Bachmann, Petra S ^a   Piazza, Rocco G ^b   Janes, Mary E ^c   Wong, Nicholas C ^d   Davies, Carwyn ^a   Mogavero, Angela ^b   Bhadri, Vivek A ^a,e   Szymanska, Barbara ^a   Geninson, Greta ^a   Magistroni, Vera ^b   Cazzaniga, Giovanni ^b   Biondi, Andrea ^b   Miranda Saavedra, Diego ^f   Göttgens, Berthold ^f   Saffery, Richard ^d   Craig, Jeffrey M ^d   Marshall, Glenn M ^a,e   Gambacorti Passerini, Carlo ^b   Pimanda, John E ^c   Lock, Richard B ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e SYDNEY CHILDREN'S HOSPITAL   (Australia)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; DEXAMETHASONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HISTONE DEACETYLASE; HISTONE H3; PREDNISOLONE; VORINOSTAT;

ACETYLATION; ACUTE LYMPHOBLASTIC LEUKEMIA; ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLAST CELL; CHILD; CONTROLLED STUDY; CPG ISLAND; DEACETYLATION; DNA METHYLATION; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; ENZYME INHIBITION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE LOCUS; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; TUMOR BIOPSY; TUMOR XENOGRAFT; UPREGULATION;

EID: 77958196417     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-05-284968     Document Type: Article

References (50)

1. Iacobuzio-Donahue CA. Epigenetic changes in cancer. Annu Rev Pathol. 2009;4:229-249.
2. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med. 2003;349(21):2042-2054. (Pubitemid 37448928)
3. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693-705.
4. Garzon R, Calin GA, Croce CM. MicroRNAs in Cancer. Annu Rev Med. 2009;60:167-179.
5. Feinberg AP. The epigenetics of cancer etiology. Semin Cancer Biol. 2004;14(6):427-432.
6. Bouillet P, Metcalf D, Huang DC, et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science. 1999;286(5445):1735-1738.
7. Egle A, Harris AW, Bouillet P, Cory S. Bim is a suppressor of Myc-induced mouse B-cell leukemia. Proc Natl Acad Sci U S A. 2004;101(16):6164-6169.
8. Erlacher M, Michalak EM, Kelly PN, et al. BH3-only proteins Puma and Bim are rate-limiting for gamma-radiation- and glucocorticoid-induced apoptosis of lymphoid cells in vivo. Blood. 2005;106(13):4131-4138.
9. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ. Expression of the proapoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol. 2000;10(19):1201-1204.
10. Hershko T, Ginsberg D. Up-regulation of Bcl-2 homology 3 (BH3)-only proteins by E2F1 mediates apoptosis. J Biol Chem. 2004;279(10):8627-8634. (Pubitemid 38295917)
11. Xiao C, Srinivasan L, Calado DP, et al. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol. 2008;9(4):405-414.
12. Gilley J, Ham J. Evidence for increased complexity in the regulation of Bim expression in sympathetic neurons: involvement of novel transcriptional and translational mechanisms. DNA Cell Biol. 2005;24(9):563-573.
13. Mestre-Escorihuela C, Rubio-Moscardo F, Richter JA, et al. Homozygous deletions localize novel tumor suppressor genes in B-cell lymphomas. Blood. 2007;109(1):271-280.
14. Dördelmann M, Reiter A, Borkhardt A, et al. Prednisone response is the strongest predictor of treatment outcome in infant acute lymphoblastic leukemia. Blood. 1999;94(4):1209-1217.
15. Schmidt S, Rainer J, Riml S, et al. Identification of glucocorticoid-response genes in children with acute lymphoblastic leukemia. Blood. 2006;107(5):2061-2069.
16. Wang Z, Malone MH, He H, McColl KS, Distelhorst CW. Microarray analysis uncovers the induction of the proapoptotic BH3-only protein Bim in multiple models of glucocorticoid-induced apoptosis. J Biol Chem. 2003;278(26):23861- 23867. (Pubitemid 36830212)
17. Bhojwani D, Kang H, Menezes RX, et al. Gene expression signatures predictive of early response and outcome in high-risk childhood acute lymphoblastic leukemia: a Children's Oncology Group Study [corrected]. J Clin Oncol. 2008;26(27):4376-4384.
18. Bachmann PS, Gorman R, Mackenzie KL, Lutze-Mann L, Lock RB. Dexamethasone resistance in B-cell precursor childhood acute lymphoblastic leukemia occurs downstream of ligand-induced nuclear translocation of the glucocorticoid receptor. Blood. 2005;105(6):2519-2526.
19. Bachmann PS, Gorman R, Papa RA, et al. Divergent mechanisms of glucocorticoid resistance in experimental models of pediatric acute lymphoblastic leukemia. Cancer Res. 2007;67(9):4482-4490.
20. Hillmann AG, Ramdas J, Multanen K, Norman MR, Harmon JM. Glucocorticoid receptor gene mutations in leukemic cells acquired in vitro and in vivo. Cancer Res. 2000;60(7):2056-2062.
21. Tissing WJ, Meijerink JP, Brinkhof B, et al. Glucocorticoid-induced glucocorticoid-receptor expression and promoter usage is not linked to glucocorticoid resistance in childhood ALL. Blood. 2006;108(3):1045-1049.
22. Lock RB, Liem N, Farnsworth ML, et al. The nonobese diabetic/severe combined immunodeficient (NOD/SCID) mouse model of childhood acute lymphoblastic leukemia reveals intrinsic differences in biologic characteristics at diagnosis and relapse. Blood. 2002;99(11):4100-4108.
23. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul. 1984;22:27-55.
24. Pimanda JE, Chan WY, Wilson NK, et al. Endoglin expression in blood and endothelium is differentially regulated by modular assembly of the Ets/Gata hemangioblast code. Blood. 2008;112(12):4512-4522.
25. Liem NL, Papa RA, Milross CG, et al. Characterization of childhood acute lymphoblastic leukemia xenograft models for the preclinical evaluation of new therapies. Blood. 2004;103(10):3905-3914.
26. Lindemann RK, Newbold A, Whitecross KF, et al. Analysis of the apoptotic and therapeutic activities of histone deacetylase inhibitors by using a mouse model of B-cell lymphoma. Proc Natl Acad Sci U S A. 2007;104(19):8071-8076.
27. Tissing WJ, den Boer ML, Meijerink JP, et al. Genomewide identification of prednisolone-responsive genes in acute lymphoblastic leukemia cells. Blood. 2007;109(9):3929-3935.
28. Hubler TR, Scammell JG. Intronic hormone response elements mediate regulation of FKBP5 by progestins and glucocorticoids. Cell Stress Chaperones. 2004;9(3):243-252.
29. U M, Shen L, Oshida T, Miyauchi J, Yamada M, Miyashita T. Identification of novel direct transcriptional targets of glucocorticoid receptor. Leukemia. 2004;18(11):1850-1856. (Pubitemid 39534321)
30. Barski A, Cuddapah S, Cui K, et al. High-resolution profiling of histone methylations in the human genome. Cell. 2007;129(4):823-837.
31. Jacinto FV, Ballestar E, Esteller M. Methyl-DNA immunoprecipitation (MeDIP): hunting down the DNA methylome. Biotechniques. 2008;44(1):35-43.
32. Fraga MF, Esteller M. DNA methylation: a profile of methods and applications. Biotechniques. 2002;33(3):632-649.
33. Thompson RF, Suzuki M, Lau KW, Greally JM. A pipeline for the quantitative analysis of CG dinucleotide methylation using mass spectrometry. Bioinformatics. 2009;25(17):2164-2170.
34. Duvic M, Talpur R, Ni X, et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood. 2007;109(1):31-39. (Pubitemid 46053039)
35. Mann BS, Johnson JR, He K, et al. Vorinostat for treatment of cutaneous manifestations of advanced primary cutaneous T-cell lymphoma. Clin Cancer Res. 2007;13(8):2318-2322.
36. Haarman EG, Kaspers GJ, Pieters R, Rottier MM, Veerman AJ. Glucocorticoid receptor alpha, beta and gamma expression vs in vitro glucocorticod resistance in childhood leukemia. Leukemia. 2004;18(3):530-537. (Pubitemid 38425868)
37. Tagawa H, Karnan S, Suzuki R, et al. Genome-wide array-based CGH for mantle cell lymphoma: identification of homozygous deletions of the proapoptotic gene BIM. Oncogene. 2005;24(8):1348-1358.
38. Mullighan CG, Goorha S, Radtke I, et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature. 2007;446(7137):758-764.
39. Nowak D, Akagi T, Papa R, et al. High density SNP array allelokaryotyping of human acute lymphoblastic leukemia (ALL) xenografts in immunodeficient mice reveals genomic changes upon in vivo induction of chemoresistance [abstract]. In: Proceedings of the 100th Annual Meeting of the American Association for Cancer Research, April 18-22, 2009, Denver, CO. 2009;434. Abstract 5198.
40. De Bruyne E, Bos TJ, Schuit F, et al. IGF-1 suppresses Bim expression in multiple myeloma via epigenetic and posttranslational mechanisms. Blood. 2010;115(12):2430-2440.
41. Webb MS, Miller AL, Johnson BH, et al. Gene networks in glucocorticoid-evoked apoptosis of leukemic cells. J Steroid Biochem Mol Biol. 2003;85(2-5):183-193.
42. Barreyro FJ, Kobayashi S, Bronk SF, Werneburg NW, Malhi H, Gores GJ. Transcriptional regulation of Bim by FoxO3A mediates hepatocyte lipoapoptosis. J Biol Chem. 2007;282(37):27141-27154.
43. Ellis L, Atadja PW, Johnstone RW. Epigenetics in cancer: targeting chromatin modifications. Mol Cancer Ther. 2009;8(6):1409-1420.
44. Gibbons RJ. Histone modifying and chromatin remodelling enzymes in cancer and dysplastic syndromes. Hum Mol Genet. 2005;14(Spec No 1):R85-92.
45. Pottier N, Yang W, Assem M, et al. The SWI/SNF chromatin-remodeling complex and glucocorticoid resistance in acute lymphoblastic leukemia. J Natl Cancer Inst. 2008;100(24):1792-1803.
46. Enders A, Bouillet P, Puthalakath H, Xu Y, Tarlinton DM, Strasser A. Loss of the proapoptotic BH3-only Bcl-2 family member Bim inhibits BCR stimulation-induced apoptosis and deletion of autoreactive B cells. J Exp Med. 2003;198(7):1119-1126. (Pubitemid 37248627)
47. Flotho C, Coustan-Smith E, Pei D, et al. A set of genes that regulate cell proliferation predicts treatment outcome in childhood acute lymphoblastic leukemia. Blood. 2007;110(4):1271-1277.
48. Wei G, Twomey D, Lamb J, et al. Gene expression-based chemical genomics identifies rapamycin as a modulator of MCL1 and glucocorticoid resistance. Cancer Cell. 2006;10(4):331-342.
49. Ploner C, Rainer J, Niederegger H, et al. The BCL2 rheostat in glucocorticoid-induced apoptosis of acute lymphoblastic leukemia. Leukemia. 2008;22(2):370-377.
50. Keshelava N, Houghton PJ, Morton CL, et al. Initial testing (stage 1) of vorinostat (SAHA) by the pediatric preclinical testing program. Pediatr Blood Cancer. 2009;53(3):505-508.