Anti-leukemia activity of chaetocin via death receptor-dependent apoptosis and dual modulation of the histone methyl-transferase SUV39H1

Leukemia

Volumn 26, Issue 4, 2012, Pages 662-674

  Chaib, H ^a,b   Nebbioso, A ^c   Prebet, T ^a,b,d   Castellano, R ^a,b,d   Garbit, S ^a,b   Restouin, A ^a,b,d   Vey, N ^a,b,d   Altucci, L ^c,e   Collette, Y ^a,b,d  

^a AIX MARSEILLE UNIVERSITY   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

^d INSTITUT PAOLI CALMETTES   (France)

^e INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

acute myeloid leukemia; apoptosis; chaetocin; epigenetics; reactive oxygen species; SUV39H1

Indexed keywords

ANTILEUKEMIC AGENT; CHETOCIN; DEATH RECEPTOR; HISTONE H3; HISTONE METHYLTRANSFERASE; METHYLTRANSFERASE INHIBITOR; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CLINICAL ARTICLE; DRUG MECHANISM; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL LINE; METHYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASES; HUMANS; LEUKEMIA, MYELOID, ACUTE; METHYLTRANSFERASES; MICE; PIPERAZINES; REACTIVE OXYGEN SPECIES; RECEPTORS, DEATH DOMAIN; REPRESSOR PROTEINS; U937 CELLS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84859643953     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2011.271     Document Type: Article

References (51)

1. Goldstone AH, Burnett AK, Wheatley K, Smith AG, Hutchinson RM, Clark RE. Attempts to improve treatment outcomes in acute myeloid leukemia (AML) in older patients: the results of the United Kingdom Medical Research Council AML11 trial. Blood 2001; 98: 1302-1311.
2. Rowe JM, Neuberg D, Friedenberg W, Bennett JM, Paietta E, Makary AZ et al. A phase 3 study of three induction regimens and of priming with GM-CSF in older adults with acute myeloid leukemia: a trial by the Eastern Cooperative Oncology Group. Blood 2004; 103: 479-485. (Pubitemid 38140076)
3. Sanz M, Burnett A, Lo-Coco F, Lowenberg B. FLT3 inhibition as a targeted therapy for acute myeloid leukemia. Curr Opin Oncol 2009; 21: 594-600.
4. Eden A, Gaudet F, Waghmare A, Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 2003; 300: 455. (Pubitemid 36444319)
5. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW et al. Induction of tumors in mice by genomic hypomethylation. Science 2003; 300: 489-492. (Pubitemid 36444330)
6. Fraga MF, Ballestar E, Villar-Garea A, Boix-Chornet M, Espada J, Schotta G et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet 2005; 37: 391-400.
7. Jiang Y, Dunbar A, Gondek LP, Mohan S, Rataul M, O'Keefe C et al. Aberrant DNA methylation is a dominant mechanism in MDS progression to AML. Blood 2009; 113: 1315-1325.
8. Figueroa ME, Skrabanek L, Li Y, Jiemjit A, Fandy TE, Paietta E et al. MDS and secondary AML display unique patterns and abundance of aberrant DNA methylation. Blood 2009; 114: 3448-3458.
9. Shen L, Kantarjian H, Guo Y, Lin E, Shan J, Huang X et al. DNA methylation predicts survival and response to therapy in patients with myelodysplastic syndromes. J Clin Oncol 2010; 28: 605-613.
10. Boultwood J, Wainscoat JS. Gene silencing by DNA methylation in haematological malignancies. Br J Haematol 2007; 138: 3-11. (Pubitemid 46889779)
11. Gurion R, Vidal L, Gafter-Gvili A, Belnik Y, Yeshurun M, Raanani P et al. 5-Azacitidine prolongs overall survival in patients with myelodysplastic syndromeFsystematic review and meta-analysis. Haematologica 2010; 95: 303-310.
12. Fenaux P, Mufti GJ, Hellstrom-Lindberg E, Santini V, Gattermann N, Germing U et al. Azacitidine prolongs overall survival compared with conventional care regimens in elderly patients with low bone marrow blast count acute myeloid leukemia. J Clin Oncol 2010; 28: 562-569.
13. Altucci L, Clarke N, Nebbioso A, Scognamiglio A, Gronemeyer H. Acute myeloid leukemia: therapeutic impact of epigenetic drugs. Int J Biochem Cell Biol 2005; 37: 1752-1762. (Pubitemid 40961660)
14. Insinga A, Monestiroli S, Ronzoni S, Gelmetti V, Marchesi F, Viale A et al. Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nat Med 2005; 11: 71-76. (Pubitemid 40215840)
15. Nebbioso A, Clarke N, Voltz E, Germain E, Ambrosino C, Bontempo P et al. Tumor-selective action of HDAC inhibitors involves TRAIL induction in acute myeloid leukemia cells. Nat Med 2005; 11: 77-84. (Pubitemid 40215841)
16. Okada Y, Feng Q, Lin Y, Jiang Q, Li Y, Coffield VM et al. hDOT1L links histone methylation to leukemogenesis. Cell 2005; 121: 167-178. (Pubitemid 40546386)
17. Cole PA. Chemical probes for histone-modifying enzymes. Nat Chem Biol 2008; 4: 590-597.
18. Greiner D, Bonaldi T, Eskeland R, Roemer E, Imhof A. Identification of a specific inhibitor of the histone methyltransferase SU(VAR)3-9. Nat Chem Biol 2005; 1: 143-145.
19. Isham CR, Tibodeau JD, Jin W, Xu R, Timm MM, Bible KC. Chaetocin: a promising new antimyeloma agent with in vitro and in vivo activity mediated via imposition of oxidative stress. Blood 2007; 109: 2579-2588. (Pubitemid 46425905)
20. Goyama S, Nitta E, Yoshino T, Kako S, Watanabe-Okochi N, Shimabe M et al. EVI-1 interacts with histone methyltransferases SUV39H1 and G9a for transcriptional repression and bone marrow immortalization. Leukemia 2010; 24: 81-88.
21. Vire B, de Walque S, Restouin A, Olive D, Van Lint C, Collette Y. Anti-leukemia activity of MS-275 histone deacetylase inhibitor implicates 4-1BBL/4-1BB immunomodulatory functions. PLoS One 2009; 4: e7085.
22. Chou TC, Talalay P. Quantitative analysis of doseeffect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984; 22: 27-55.
23. Lakshmikuttyamma A, Scott SA, DeCoteau JF, Geyer CR. Reexpression of epigenetically silenced AML tumor suppressor genes by SUV39H1 inhibition. Oncogene 2010; 29: 576-588.
24. Castellano R, Vire B, Pion M, Quivy V, Olive D, Hirsch I et al. Active transcription of the human FASL/CD95L/TNFSF6 promoter region in T lymphocytes involves chromatin remodeling: role of DNA methylation and protein acetylation suggest distinct mechanisms of transcriptional repression. J Biol Chem 2006; 281: 14719-14728. (Pubitemid 43855177)
25. Cherrier T, Suzanne S, Redel L, Calao M, Marban C, Samah B et al. p21(WAF1) gene promoter is epigenetically silenced by CTIP2 and SUV39H1. Oncogene 2009; 28: 3380-3389.
26. Marks PA, Breslow R. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol 2007; 25: 84-90. (Pubitemid 46087907)
27. Robak T, Wierzbowska A. Current and emerging therapies for acute myeloid leukemia. Clin Ther 2009; 31: 2349-2370.
28. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996; 93: 9821-9826. (Pubitemid 26296693)
29. Quesnel B, Guillerm G, Vereecque R, Wattel E, Preudhomme C, Bauters F et al. Methylation of the p15(INK4b) gene in myelodysplastic syndromes is frequent and acquired during disease progression. Blood 1998; 91: 2985-2990. (Pubitemid 28227550)
30. Garcia-Manero G, Assouline S, Cortes J, Estrov Z, Kantarjian H, Yang H et al. Phase 1 study of the oral isotype specific histone deacetylase inhibitor MGCD0103 in leukemia. Blood 2008; 112: 981-989.
31. Garcia-Manero G, Yang H, Bueso-Ramos C, Ferrajoli A, Cortes J, Wierda WG et al. Phase 1 study of the histone deacetylase inhibitor vorinostat (suberoylanilide hydroxamic acid [SAHA]) in patients with advanced leukemias and myelodysplastic syndromes. Blood 2008; 111: 1060-1066. (Pubitemid 351213383)
32. Gore SD, Baylin S, Sugar E, Carraway H, Miller CB, Carducci M et al. Combined DNA methyltransferase and histone deacetylase inhibition in the treatment of myeloid neoplasms. Cancer Res 2006; 66: 6361-6369.
33. Silverman LR, Verma A, Odchimar-Reissig R, Cozza A, Najfeld V, Licht JD et al. A phase I/II study of vorinostat, an oral histone deacetylase inhibitor, in combination with azacitidine in patients with the myelodysplastic syndrome (MDS) and acute myeloid leukemia (AML). Initial results of the phase I trial: A New York Cancer Consortium. J Clin Oncol 2008; 26(Suppl): abstract 7000.
34. Raffoux E, Labarthe A, Cras A, Recher C, Turlure P, Marolleau JP et al. Epigenetic therapy with 5-azacitidine, valproic acid, and ATRA in patients with high-risk AML or MDS: results of the French VIVEDEP Phase II study. 50th ASH Annual Meeting 2008.
35. Qian C, Zhou MM. SET domain protein lysine methyltransferases: structure, specificity and catalysis. Cell Mol Life Sci 2006; 63: 2755-2763. (Pubitemid 44913316)
36. Krause CD, Yang ZH, Kim YS, Lee JH, Cook JR, Pestka S. Protein arginine methyltransferases: evolution and assessment of their pharmacological and therapeutic potential. Pharmacol Ther 2007; 113: 50-87. (Pubitemid 46017068)
37. Kleer CG, Cao Q, Varambally S, Shen R, Ota I, Tomlins SA et al. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 2003; 100: 11606-11611. (Pubitemid 37205983)
38. Krivtsov AV, Feng Z, Lemieux ME, Faber J, Vempati S, Sinha AU et al. H3K79 methylation profiles define murine and human MLL-AF4 leukemias. Cancer Cell 2008; 14: 355-368.
39. Jansson M, Durant ST, Cho EC, Sheahan S, Edelmann M, Kessler B et al. Arginine methylation regulates the p53 response. Nat Cell Biol 2008; 10: 1431-1439.
40. Cattaneo F, Nucifora G. EVI1 recruits the histone methyltransferase SUV39H1 for transcription repression. J Cell Biochem 2008; 105: 344-352.
41. Carbone R, Botrugno OA, Ronzoni S, Insinga A, Di Croce L, Pelicci PG et al. Recruitment of the histone methyltransferase SUV39H1 and its role in the oncogenic properties of the leukemia-associated PML-retinoic acid receptor fusion protein. Mol Cell Biol 2006; 26: 1288-1296. (Pubitemid 43202556)
42. Chakraborty S, Sinha KK, Senyuk V, Nucifora G. SUV39H1 interacts with AML1 and abrogates AML1 transactivity. AML1 is methylated in vivo. Oncogene 2003; 22: 5229-5237. (Pubitemid 37056085)
43. Tibodeau J, Benson L, Isham C, Owen W, Bible K. The anticancer agent chaetocin is a competitive substrate and inhibitor of thioredoxin reductase. Antioxid Redox Signal 2009; 11: 1097-1106.
44. Cook KM, Hilton ST, Mecinovic J, Motherwell WB, Figg WD, Schofield CJ. Epidithiodiketopiperazines block the interaction between hypoxia-inducible factor-1alpha (HIF-1alpha) and p300 by a zinc ejection mechanism. J Biol Chem 2009; 284: 26831-26838.
45. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, Schmid M et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000; 406: 593-599. (Pubitemid 30641039)
46. Zhang X, Tamaru H, Khan SI, Horton JR, Keefe LJ, Selker EU et al. Structure of the neurospora SET domain protein DIM-5, a histone H3 lysine methyltransferase. Cell 2002; 111: 117-127.
47. Zhang X, Yang Z, Khan SI, Horton JR, Tamaru H, Selker EU et al. Structural basis for the product specificity of histone lysine methyltransferases. Mol Cell 2003; 12: 177-185. (Pubitemid 36957834)
48. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 2009; 8: 579-591.
49. Ward PS, Patel J, Wise DR, Abdel-Wahab O, Bennett BD, Coller HA et al. The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 2010; 17: 225-234.
50. Chou WC, Hou HA, Chen CY, Tang JL, Yao M, Tsay W et al. Distinct clinical and biologic characteristics in adult acute myeloid leukemia bearing the isocitrate dehydrogenase 1 mutation. Blood 2010; 115: 2749-2754.
51. Callens C, Coulon S, Naudin J, Radford-Weiss I, Boissel N, Raffoux E et al. Targeting iron homeostasis induces cellular differentiation and synergizes with differentiating agents in acute myeloid leukemia. J Exp Med 2010; 207: 731-750.