Epigenetic aspects of MDS and its molecular targeted therapy

International Journal of Hematology

Volumn 97, Issue 2, 2013, Pages 175-182

  Yamazaki, Jumpei ^a,b   Issa, Jean Pierre J ^a,b  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Dna methylation; Epigenetics; Histone modification; Mds; Mutation

Indexed keywords

ARTICLE; CELL DIFFERENTIATION; DNA METHYLATION; EMBRYO DEVELOPMENT; EPIGENETICS; GENE EXPRESSION; HISTONE MODIFICATION; HUMAN; MOLECULARLY TARGETED THERAPY; MYELODYSPLASTIC SYNDROME; NEOPLASM; GENETIC EPIGENESIS; GENETICS; REVIEW;

ANTINEOPLASTIC AGENT;

ANTINEOPLASTIC AGENTS; EPIGENESIS, GENETIC; HUMANS; MOLECULAR TARGETED THERAPY; MYELODYSPLASTIC SYNDROMES;

EID: 84885834757     PISSN: 09255710     EISSN: 18653774     Source Type: Journal    
DOI: 10.1007/s12185-012-1197-4     Document Type: Article

References (86)

1. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007; 128(4):683-92.
2. Baylin SB, Herman JG, Graff JR, Vertino PM, Issa JP. Alterations in DNA methylation: A fundamental aspect of neoplasia. Adv Cancer Res. 1998;72:141-96.
3. Jones PA, Laird PW. Cancer epigenetics comes of age. Nat Genet. 1999;21(2):163-7.
4. Klose RJ, Bird AP. Genomic DNA methylation: The mark and its mediators. Trends Biochem Sci. 2006;31(2):89-97.
5. Illingworth RS, Bird AP. CpG islands-'a rough guide'. FEBS Lett. 2009;583(11):1713-20.
6. Heard E, Clerc P, Avner P. X-chromosome inactivation in mammals. Annu Rev Genet. 1997;31:571-610.
7. Barlow DP. Gametic imprinting in mammals. Science. 1995;270(5242):1610-3.
8. Ferguson-Smith AC. Genomic imprinting: The emergence of an epigenetic paradigm. Nat Rev Genet. 2011;12(8):565-75.
9. Jones PL, Wolffe AP. Relationships between chromatin organization and DNA methylation in determining gene expression. Semin Cancer Biol. 1999;9(5):339-47.
10. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature. 1998;393(6683):386-9.
11. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell selfrenewal and inner cell mass specification. Nature. 2010;466 (7310):1129-33.
12. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009;324(5929):930-5.
13. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science. 2011;333(6047):1300-3.
14. Nestor CE, Ottaviano R, Reddington J, Sproul D, Reinhardt D, Dunican D, et al. Tissue type is a major modifier of the 5-hydroxymethylcytosine content of human genes. Genome Res. 2012;22(3):467-77.
15. Khorasanizadeh S. The nucleosome: from genomic organization to genomic regulation. Cell. 2004;116(2):259-72.
16. Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403(6765):41-5.
17. Lachner M, Jenuwein T. The many faces of histone lysine methylation. Curr Opin Cell Biol. 2002;14(3):286-98.
18. Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293(5532):1074-80.
19. Rice JC, Allis CD. Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr Opin Cell Biol. 2001;13(3):263-73.
20. Taby R, Issa JP. Cancer epigenetics. CA Cancer J Clin. 2010;60(6):376-92.
21. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature. 1983;301(5895):89-92.
22. Feinberg AP, Gehrke CW, Kuo KC, Ehrlich M. Reduced genomic 5-methylcytosine content in human colonic neoplasia. Cancer Res. 1988;48(5):1159-61.
23. Estecio MR, Gharibyan V, Shen L, Ibrahim AE, Doshi K, He R, et al. LINE-1 hypomethylation in cancer is highly variable and inversely correlated with microsatellite instability. PLoS ONE. 2007;2(5):e399.
24. Dunn BK. Hypomethylation: one side of a larger picture. Ann N Y Acad Sci. 2003;983:28-42.
25. Chen RZ, Pettersson U, Beard C, Jackson-Grusby L, Jaenisch R. DNA hypomethylation leads to elevated mutation rates. Nature. 1998;395(6697):89-93.
26. Issa JP. Epigenetic changes in the myelodysplastic syndrome. Hematol Oncol Clin N Am. 2010;24(2):317-30.
27. 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(4):391-400.
28. Esteller M. Cancer epigenomics: DNA methylomes and histonemodification maps. Nat Rev Genet. 2007;8(4):286-98.
29. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C, et al. Epigenetic stem cell signature in cancer. Nat Genet. 2007;39(2):157-8.
30. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet. 2007;39(2):237-42.
31. Chi P, Allis CD, Wang GG. Covalent histone modifications- miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer. 2010;10(7):457-69.
32. Armstrong SA, Golub TR, Korsmeyer SJ. MLL-rearranged leukemias: insights from gene expression profiling. Semin Hematol. 2003;40(4):268-73.
33. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar- Sinha C, Sanda MG, et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature. 2002;419(6907):624-9.
34. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet. 2008;40(6):741-50.
35. van Haaften G, Dalgliesh GL, Davies H, Chen L, Bignell G, Greenman C, et al. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat Genet. 2009;41(5):521-3.
36. Mistry AR, Pedersen EW, Solomon E, Grimwade D. The molecular pathogenesis of acute promyelocytic leukaemia: implications for the clinical management of the disease. Blood Rev. 2003;17(2):71-97.
37. Schwartzentruber J, Korshunov A, Liu XY, Jones DT, Pfaff E, Jacob K, et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature. 2012;482(7384):226-31.
38. Wu G, Broniscer A, McEachron TA, Lu C, Paugh BS, Becksfort J, et al. Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet. 2012;44(3):251-3.
39. Voso MT, D'Alo F, Greco M, Fabiani E, Criscuolo M, Migliara G, et al. Epigenetic changes in therapy-related MDS/AML. Chem Biol Interact. 2010;184(1-2):46-9.
40. Tien HF, Tang JH, Tsay W, Liu MC, Lee FY, Wang CH, et al. Methylation of the p15(INK4B) gene in myelodysplastic syndrome: it can be detected early at diagnosis or during disease progression and is highly associated with leukaemic transformation. Br J Haematol. 2001;112(1):148-54.
41. Christiansen DH, Andersen MK, Pedersen-Bjergaard J. Methylation of p15INK4B is common, is associated with deletion of genes on chromosome arm 7q and predicts a poor prognosis in therapy-related myelodysplasia and acute myeloid leukemia. Leukemia. 2003;17(9):1813-9.
42. 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(8):2985-90.
43. 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(4):605-13.
44. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA. 1999;96(15):8681-6.
45. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell. 2010;17(5):510-22.
46. 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(16):3448-58.
47. 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(6):1315-25.
48. Romermann D, Hasemeier B, Metzig K, Schlegelberger B, Langer F, Kreipe H, et al. Methylation status of LINE-1 sequences in patients with MDS or secondary AML. Verh Dtsch Ges Pathol. 2007;91:338-42.
49. Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS, et al. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature. 2010;468(7325):839-43.
50. Yamazaki J, Taby R, Vasanthakumar A, Macrae T, Ostler KR, Shen L, et al. Effects of TET2 mutations on DNA methylation in chronic myelomonocytic leukemia. Epigenetics. 2012;7(2):201-7.
51. Nikoloski G, van der Reijden BA, Jansen JH. Mutations in epigenetic regulators in myelodysplastic syndromes. Int J Hematol. 2012;95(1):8-16.
52. Kosmider O, Gelsi-Boyer V, Ciudad M, Racoeur C, Jooste V, Vey N, et al. TET2 gene mutation is a frequent and adverse event in chronic myelomonocytic leukemia. Haematologica. 2009;94(12):1676-81.
53. Jankowska AM, Szpurka H, Tiu RV, Makishima H, Afable M, Huh J, et al. Loss of heterozygosity 4q24 and TET2 mutations associated with myelodysplastic/myeloproliferative neoplasms. Blood. 2009;113(25):6403-10.
54. Abdel-Wahab O, Mullally A, Hedvat C, Garcia-Manero G, Patel J, Wadleigh M, et al. Genetic characterization of TET1, TET2, and TET3 alterations in myeloid malignancies. Blood. 2009;114(1):144-7.
55. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A, et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell. 2010;18(6):553-67.
56. Moran-Crusio K, Reavie L, Shih A, Abdel-Wahab O, Ndiaye-Lobry D, Lobry C, et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell. 2011;20(1):11-24.
57. Quivoron C, Couronne L, Della Valle V, Lopez CK, Plo I, Wagner-Ballon O, et al. TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell. 2011;20(1):25-38.
58. Egger G, Liang GN, Aparicio A, Jones PA. Epigenetics in human disease and prospects for epigenetic therapy. Nature. 2004;429(6990):457-63.
59. Issa JP, Kantarjian HM. Targeting DNA methylation. Clin Cancer Res. 2009;15(12):3938-46.
60. Yoo CB, Jones PA. Epigenetic therapy of cancer: past, present and future. Nat Rev Drug Discov. 2006;5(1):37-50.
61. Jones PA, Taylor SM. Cellular differentiation, cytidine analogs and DNA methylation. Cell. 1980;20(1):85-93.
62. Santini V, Kantarjian HM, Issa JP. Changes in DNA methylation in neoplasia: pathophysiology and therapeutic implications. Ann Intern Med. 2001;134(7):573-86.
63. Tsai HC, Li H, Van Neste L, Cai Y, Robert C, Rassool FV, et al. Transient low doses of DNA-demethylating agents exert durable antitumor effects on hematological and epithelial tumor cells. Cancer Cell. 2012;21(3):430-46.
64. Wijermans P, Lubbert M, Verhoef G, Bosly A, Ravoet C, Andre M, et al. Low-dose 5-aza-20-deoxycytidine, a DNA hypomethylating agent, for the treatment of high-risk myelodysplastic syndrome: A multicenter phase II study in elderly patients. J Clin Oncol. 2000;18(5):956-62.
65. Issa JP, Garcia-Manero G, Giles FJ, Mannari R, Thomas D, Faderl S, et al. Phase 1 study of low-dose prolonged exposure schedules of the hypomethylating agent 5-aza-20-deoxycytidine (decitabine) in hematopoietic malignancies. Blood. 2004;103(5):1635-40.
66. Silverman LR, Demakos EP, Peterson BL, Kornblith AB, Holland JC, Odchimar-Reissig R, et al. Randomized controlled trial of azacitidine in patients with the myelodysplastic syndrome: A study of the cancer and leukemia group B. J Clin Oncol. 2002;20(10):2429-40.
67. Fenaux P, Mufti GJ, Hellstrom-Lindberg E, Santini V, Finelli C, Giagounidis A, et al. Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: A randomised, open-label, phase III study. Lancet Oncol. 2009;10(3):223-32.
68. Kantarjian H, Issa JP, Rosenfeld CS, Bennett JM, Albitar M, DiPersio J, et al. Decitabine improves patient outcomes in myelodysplastic syndromes: results of a phase III randomized study. Cancer. 2006;106(8):1794-803.
69. Kantarjian H, Oki Y, Garcia-Manero G, Huang X, O'Brien S, Cortes J, et al. Results of a randomized study of 3 schedules of low-dose decitabine in higher-risk myelodysplastic syndrome and chronic myelomonocytic leukemia. Blood. 2007;109(1):52-7.
70. Oki Y, Jelinek J, Shen L, Kantarjian HM, Issa JP. Induction of hypomethylation and molecular response after decitabine therapy in patients with chronic myelomonocytic leukemia. Blood. 2008;111(4):2382-4.
71. Faderl S, Ravandi F, Huang X, Wang X, Jabbour E, Garcia- Manero G, et al. Clofarabine plus low-dose cytarabine followed by clofarabine plus low-dose cytarabine alternating with decitabine in acute myeloid leukemia frontline therapy for older patients. Cancer. 2012;118(18):4471-7.
72. Sekeres MA, List AF, Cuthbertson D, Paquette R, Ganetzky R, Latham D, et al. Phase I combination trial of lenalidomide and azacitidine in patients with higher-risk myelodysplastic syndromes. J Clin Oncol. 2010;28(13):2253-8.
73. Garcia-Manero G, Gore SD, Cogle C, Ward R, Shi T, Macbeth KJ, et al. Phase I study of oral azacitidine in myelodysplastic syndromes, chronic myelomonocytic leukemia, and acute myeloid leukemia. J Clin Oncol. 2011;29(18):2521-7.
74. Datta J, Ghoshal K, Denny WA, Gamage SA, Brooke DG, Phiasivongsa P, et al. A new class of quinoline-based DNA hypomethylating agents reactivates tumor suppressor genes by blocking DNA methyltransferase 1 activity and inducing its degradation. Cancer Res. 2009;69(10):4277-85.
75. 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(3):1060-6.
76. Raynal NJ, Si J, Taby RF, Gharibyan V, Ahmed S, Jelinek J, et al. DNA methylation does not stably lock gene expression but instead serves as a molecular mark for gene silencing memory. Cancer Res. 2012;72(5):1170-81.
77. Si J, Boumber YA, Shu J, Qin T, Ahmed S, He R, et al. Chromatin remodeling is required for gene reactivation after decitabine- mediated DNA hypomethylation. Cancer Res. 2010;70(17):6968-77.
78. Garcia-Manero G, Kantarjian HM, Sanchez-Gonzalez B, Yang H, Rosner G, Verstovsek S, et al. Phase 1/2 study of the combination of 5-aza-20- deoxycytidine with valproic acid in patients with leukemia. Blood. 2006;108(10):3271-9.
79. Voso MT, Santini V, Finelli C, Musto P, Pogliani E, Angelucci E, et al. Valproic acid at therapeutic plasma levels may increase 5-azacytidine efficacy in higher risk myelodysplastic syndromes. Clin Cancer Res. 2009;15(15):5002-7.
80. Kubicek S, O'Sullivan RJ, August EM, Hickey ER, Zhang Q, Teodoro ML, et al. Reversal of H3K9me2 by a small-molecule inhibitor for the G9a histone methyltransferase. Mol Cell. 2007;25(3):473-81.
81. Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL, et al. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev. 2007;21(9):1050-63.
82. Kosmider O, Gelsi-Boyer V, Cheok M, Grabar S, Della-Valle V, Picard F, et al. TET2 mutation is an independent favorable prognostic factor in myelodysplastic syndromes (MDSs). Blood. 2009;114(15):3285-91.
83. Kosmider O, Gelsi-Boyer V, Slama L, Dreyfus F, Beyne-Rauzy O, Quesnel B, et al. Mutations of IDH1 and IDH2 genes in early and accelerated phases of myelodysplastic syndromes and MDS/myeloproliferative neoplasms. Leukemia. 2010;24(5):1094-6.
84. Walter MJ, Ding L, Shen D, Shao J, Grillot M, McLellan M, et al. Recurrent DNMT3A mutations in patients with myelodysplastic syndromes. Leukemia. 2011;25(7):1153-8.
85. Thol F, Friesen I, Damm F, Yun H, Weissinger EM, Krauter J, et al. Prognostic significance of ASXL1 mutations in patients with myelodysplastic syndromes. J Clin Oncol. 2011; 29(18):2499-506.
86. Bejar R, Levine R, Ebert BL. Unraveling the molecular pathophysiology of myelodysplastic syndromes. J Clin Oncol. 2011;29(5):504-15.