Predicting response to epigenetic therapy

Journal of Clinical Investigation

Volumn 124, Issue 1, 2014, Pages 47-55

  Treppendahl, Marianne B ^a   Kristensen, Lasse S ^a   Groønb, Kirsten ^a  

^a Rigshospitalet   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; DNA METHYLTRANSFERASE INHIBITOR; HISTONE DEACETYLASE;

CANCER THERAPY; CYTOGENETICS; DNA METHYLATION; DRUG APPROVAL; DRUG EFFICACY; EPIGENETICS; FOOD AND DRUG ADMINISTRATION; GENE EXPRESSION; GENE THERAPY; HUMAN; POINT MUTATION; PRIORITY JOURNAL; REVIEW; TREATMENT RESPONSE;

EID: 84892949766     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI69737     Document Type: Review

References (90)

1. Diamandis M, White NM, Yousef GM. Personalized medicine: marking a new epoch in cancer patient management. Mol Cancer Res. 2010;8(9):1175-1187
2. Milbury CA, Li J, Makrigiorgos GM. PCR-based methods for the enrichment of minority alleles and mutations. Clin Chem. 2009;55(4):632-640
3. Altman DG, McShane LM, Sauerbrei W, Taube SE. Reporting Recommendations for Tumor Marker Prognostic Studies (REMARK): explanation and elaboration. PLoS Med. 2012;9(5):e1001216
4. McShane LM, et al. Reporting recommendations for tumor marker prognostic studies. J Clin Oncol. 2005; 23(36):9067-9072
5. Fenaux P, 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(4):562-569
6. Fenaux P, 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):223-232
7. Kantarjian H, et al. Decitabine improves patient outcomes in myelodysplastic syndromes: results of a phase III randomized study. Cancer. 2006; 106(8):1794-1803
8. Ades L, et al. Predictive factors of response and survival among chronic myelomonocytic leukemia patients treated with azacitidine. Leuk Res. 2013; 37(6):609-613
9. Kantarjian HM et, al. Multicenter, randomized, open-label, phase III trial of decitabine versus patient choice, with physician advice, of either supportive care or low-dose cytarabine for the treatment of older patients with newly diagnosed acute myeloid leukemia. J Clin Oncol. 2012;30(21):2670-2677
10. Lee Y-G, et al. Comparative analysis between azacitidine and decitabine for the treatment of myelodysplastic syndromes. Br J Haematol. 2013; 161(3):339-347
11. Schecter J, Galili N, Raza A. MDS: Refining existing therapy through improved biologic insights. Blood Rev. 2012;26(2):73-80
12. Itzykson R, et al. Prognostic factors for response and overall survival in 282 patients with higherrisk myelodysplastic syndromes treated with azacitidine. Blood. 2011;117(2):403-411
13. Itzykson R, et al. Long-term outcome of higher-risk MDS patients treated with azacitidine: an update of the GFM compassionate program cohort. Blood. 2012;119(25):6172-6173
14. Gore SD, et al. A multivariate analysis of the relationship between response and survival among patients with higher-risk myelodysplastic syndromes treated within azacitidine or conventional care regimens in the randomized AZA-001 trial. Haematologica. 2013;98(7):1067-1072
15. Jones PA, Taylor SM. Cellular differentiation, cytidine analogs and DNA methylation. Cell. 1980; 20(1):85-93
16. Gore SD, et al. Combined DNA methyltransferase and histone deacetylase inhibition in the treatment of myeloid neoplasms. Cancer Res. 2006; 66(12):6361-6369
17. Fandy TE, et al. Early epigenetic changes and DNA damage do not predict clinical response in an overlapping schedule of 5-azacytidine and entinostat in patients with myeloid malignancies. Blood. 2009; 114(13):2764-2773
18. Qiu X, et al. Equitoxic doses of 5-azacytidine and 5-aza- 2′deoxycytidine induce diverse immediate and overlapping heritable changes in the transcriptome. PLoS One. 2010;5(9):e12994
19. Almstedt M, et al. The DNA demethylating agent 5-aza-2′- deoxycytidine induces expression of NYESO- 1 and other cancer/testis antigens in myeloid leukemia cells. Leuk Res. 2010;34(7):899-905
20. Goodyear O, et al. Induction of a CD8+ T-cell response to the MAGE cancer testis antigen by combined treatment with azacitidine and sodium valproate in patients with acute myeloid leukemia and myelodysplasia. Blood. 2010;116(11):1908-1918
21. Aimiuwu J, et al. RNA-dependent inhibition of ribonucleotide reductase is a major pathway for 5-azacytidine activity in acute myeloid leukemia. Blood. 2012;119(22):5229-5238
22. Astex Pharmaceuticals. SGI-110 in Patients With Myelodysplastic Syndromes (MDS) or Acute Myelogenous Leukemia (AML). NIH Web site. http://clinicaltrials. gov/ct2/show/NCT01261312. Updated August 14, 2013. Accessed November 5, 2013
23. Astex Pharmaceuticals. SGI-110 in Combination With Carboplatin in Ovarian Cancer. NIH Web site. http://clinicaltrials.gov/ct2/show/NCT01696032. Updated April 14, 2013. Accessed November 5, 2013
24. Astex Pharmaceuticals. SGI-110 in the Treatment of Advanced Hepatocellular Carcinoma (HCC). NIH Web site. http://clinicaltrials.gov/ct2/ show/NCT01752933. Updated April 14, 2013. Accessed November 5, 2013
25. Fahy J, Jeltsch A, Arimondo PB. DNA methyltransferase inhibitors in cancer: a chemical and therapeutic patent overview and selected clinical studies. Expert Opin Ther Pat. 2012;22(12):1427-1442
26. Gros C, et al. DNA methylation inhibitors in cancer: recent and future approaches. Biochimie. 2012; 94(11):2280-2296
27. Rius M, et al. Human concentrative nucleoside transporter 1-mediated uptake of 5-azacytidine enhances DNA demethylation. Mol Cancer Ther. 2009;8(1):225-231
28. Damaraju VL, et al. Role of human nucleoside transporters in the uptake and cytotoxicity of azacitidine and decitabine. Nucleosides Nucleotides Nucleic Acids. 2012;31(3):236-255
29. Qin T, Jelinek J, Si J, Shu J, Issa J-PJ. Mechanisms of resistance to 5-aza-2′-deoxycytidine in human cancer cell lines. Blood. 2009;113(3):659-667
30. van den Heuvel-Eibrink MM, Wiemer EA, Kuijpers M, Pieters R, Sonneveld P. Absence of mutations in the deoxycytidine kinase (dCK) gene in patients with relapsed and/or refractory acute myeloid leukemia (AML). Leukemia. 2001;15(5):855-856
31. Qin T, et al. Mechanisms of resistance to decitabine in the myelodysplastic syndrome. PLoS One. 2011; 6(8):e23372
32. Mahfouz RZ, et al. Increased CDA expression/activity in males contributes to decreased cytidine analog half-life and likely contributes to worse outcomes with 5-azacytidine or decitabine therapy. Clin Cancer Res. 2013;19(4):938-948
33. Bally C, et al. Azacitidine in the treatment of therapy related myelodysplastic syndrome and acute myeloid leukemia (tMDS/AML): A report on 54 patients by the Groupe Francophone Des Myelodysplasies (GFM). Leuk Res. 2013;37(6):637-640
34. Shen L, et al. DNA methylation predicts survival and response to therapy in patients with myelodysplastic syndromes. J Clin Oncol. 2010;28(4):605-613
35. Raj K, et al. CDKN2B methylation status and isolated chromosome 7 abnormalities predict responses to treatment with 5-azacytidine. Leukemia. 2007;21(9):1937-1944
36. Yoo CB, et al. Delivery of 5-aza-2′-deoxycytidine to cells using oligodeoxynucleotides. Cancer Res. 2007; 67(13):6400-6408
37. Greenberg P, et al. International scoring system for evaluating prognosis in myelodysplastic syndromes. Blood. 1997;89(6):2079-2088
38. Breccia M, et al. Application of French prognostic score to patients with International Prognostic Scoring System intermediate-2 or high risk myelodysplastic syndromes treated with 5-azacitidine is able to predict overall survival and rate of response. Leuk Lymphoma. 2012;53(5):985-986
39. Van der Helm LH, et al. Platelet doubling after the first azacitidine cycle is a promising predictor for response in myelodysplastic syndromes (MDS), chronic myelomonocytic leukaemia (CMML) and acute myeloid leukaemia (AML) patients in the Dutch azacitidine compassionate named p. Br J Haematol. 2011;155(5):599-606
40. Lubbert M, et al. Cytogenetic responses in highrisk myelodysplastic syndrome following low-dose treatment with the DNA methylation inhibitor 5-aza-2′-deoxycytidine. Br J Haematol. 2001; 114(2):349-357
41. Garzon R, et al. MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood. 2009;113(25):6411-6418
42. Blum W, et al. Clinical response and miR-29b predictive significance in older AML patients treated with a 10-day schedule of decitabine. Proc Natl Acad Sci U S A. 2010;107(16):7473-7478
43. Vire E, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature. 2006; 439(7078):871-874
44. Itzykson R, et al. Impact of TET2 mutations on response rate to azacitidine in myelodysplastic syndromes and low blast count acute myeloid leukemias. Leukemia. 2011;25(7):1147-1152
45. Voso MT, et al. Role of BCL2L10 methylation and TET2 mutations in higher risk myelodysplastic syndromes treated with 5-azacytidine. Leukemia. 2011; 25(12):1910-1913
46. Braun T, et al. Molecular predictors of response to decitabine in advanced chronic myelomonocytic leukemia: a phase 2 trial. Blood. 2011; 118(14):3824-3831
47. Metzeler KH, et al. DNMT3A mutations and response to the hypomethylating agent decitabine in acute myeloid leukemia. Leukemia. 2012; 26(5):1106-1107
48. Traina F, et al. Impact of molecular mutations on treatment response to DNMT inhibitors in myelodysplasia and related neoplasms [published online ahead of print September 18, 2013]. Leukemia. doi:10.1038/leu.2013.269
49. Daskalakis M, et al. Demethylation of a hypermethylated P15/INK4B gene in patients with myelodysplastic syndrome by 5-Aza-2′-deoxycytidine (decitabine) treatment. Blood. 2002;100(8):2957-2964
50. Garcia-Manero G, et al. Phase 1/2 study of the combination of 5-aza-2′-deoxycytidine with valproic acid in patients with leukemia. Blood. 2006; 108(10):3271-3279
51. Yang AS, et al. DNA methylation changes after 5-aza-2′- deoxycytidine therapy in patients with leukemia. Cancer Res. 2006;66(10):5495-5503
52. Kantarjian H, et al. Results of a randomized study of 3 schedules of low-dose decitabine in higherrisk myelodysplastic syndrome and chronic myelomonocytic leukemia. Blood. 2007;109(1):52-57
53. Issa J-PJ, et al. Phase 1 study of low-dose prolonged exposure schedules of the hypomethylating agent 5-aza-2′-deoxycytidine (decitabine) in hematopoietic malignancies. Blood. 2004;103(5):1635-1640
54. Cluzeau T, et al. BCL2L10 is a predictive factor for resistance to azacitidine in MDS and AML patients. Oncotarget. 2012;3(4):490-501
55. Juergens R, a et al. Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer. Cancer Discov. 2011; 1(7):598-607
56. Abaigar M, et al. Prognostic impact of the number of methylated genes in myelodysplastic syndromes and acute myeloid leukemias treated with azacytidine. Ann Hematol. 2013;92(11):1543-1552
57. Yan P, et al. Genome-wide methylation profiling in decitabine-treated patients with acute myeloid leukemia. Blood. 2012;120(12):2466-2474
58. Simo-Riudalbas L, Melo SA, Esteller M. DNMT3B gene amplification predicts resistance to DNA demethylating drugs. Genes Chromosomes Cancer. 2011;50(7):527-534
59. Yang Z, et al. Increased c-Jun expression and reduced GATA2 expression promote aberrant monocytic differentiation induced by activating PTPN11 mutants. Mol Cell Biol. 2009; 29(16):4376-4393
60. Ramsay RG, Gonda TJ. MYB function in normal and cancer cells. Nat Rev Cancer. 2008;8(7):523-534
61. Ettou S, et al. Fas expression at diagnosis as a biomarker of azacitidine activity in high-risk MDS and secondary AML. Leukemia. 2012;26(10):2297-2299
62. Follo MY, et al. Synergistic induction of PI-PLC®1 signaling by azacitidine and valproic acid in highrisk myelodysplastic syndromes. Leukemia. 2011; 25(2):271-280
63. Follo MY, et al. Reduction of phosphoinositidephospholipase C ®1 methylation predicts the responsiveness to azacitidine in high-risk MDS. Proc Natl Acad Sci U S A. 2009;106(39):16811-16816
64. Fili C, et al. Prospective phase II Study on 5-days azacitidine for treatment of symptomatic and/or erythropoietin unresponsive patients with low/INT- 1-risk myelodysplastic syndromes. Clin Cancer Res. 2013;19(12):3297- 3308
65. Follo MY, et al. Epigenetic regulation of nuclear PI-PLC®1 signaling pathway in low-risk MDS patients during azacitidine treatment. Leukemia. 2012;26(5):943-950
66. Fabbri M, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A. 2007;104(40):15805-15810
67. Mims A, et al. Increased anti-leukemic activity of decitabine via AR-42-induced upregulation of miR- 29b: a novel epigenetic-targeting approach in acute myeloid leukemia. Leukemia. 2013;27(4):871-878
68. Yang H, et al. Levels of miR-29b do not predict for response in patients with acute myelogenous leukemia treated with the combination of 5-azacytidine, valproic acid, and ATRA. Am J Hematol. 2011; 86(2):237-238
69. New M, Olzscha H, La Thangue NB. HDAC inhibitor- based therapies: can we interpret the code? Mol Oncol. 2012;6(6):637-656
70. Stimson L, La Thangue NB. Biomarkers for predicting clinical responses to HDAC inhibitors. Cancer Lett. 2009;280(2):177-183
71. Wagner JM, Hackanson B, Lubbert M, Jung M. Histone deacetylase (HDAC) inhibitors in recent clinical trials for cancer therapy. Clin Epigenetics. 2010;1(3-4):117-136
72. Haigentz M, et al. Phase II trial of the histone deacetylase inhibitor romidepsin in patients with recurrent/metastatic head and neck cancer. Oral Oncol. 2012;48(12):1281-1288
73. Ellis L, et al. Histone deacetylase inhibitor panobinostat induces clinical responses with associated alterations in gene expression profiles in cutaneous T-cell lymphoma. Clin Cancer Res. 2008;14(14):4500-4510
74. Garcia-Manero G, 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):1060-1066
75. Glaser KB, et al. Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines. Mol Cancer Ther. 2003;2(2):151-163
76. Arts J, et al. R306465 is a novel potent inhibitor of class I histone deacetylases with broadspectrum antitumoral activity against solid and haematological malignancies. Br J Cancer. 2007;97(10):1344-1353
77. Noro R, et al. Histone deacetylase inhibitor enhances sensitivity of non-small-cell lung cancer cells to 5-FU/S-1 via down-regulation of thymidylate synthase expression and up-regulation of p21(waf1/cip1) expression. Cancer Sci. 2010;101(6):1424-1430
78. Galanis E, et al. Phase II trial of vorinostat in recurrent glioblastoma multiforme: a north central cancer treatment group study. J Clin Oncol. 2009;27(12):2052-2058
79. Khan O, La Thangue NB. HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol Cell Biol. 2012;90(1):85-94
80. Marquard L, et al. Prognostic significance of the therapeutic targets histone deacetylase 1, 2, 6 and acetylated histone H4 in cutaneous T-cell lymphoma. Histopathology. 2008;53(3):267-277
81. Munster PN, et al. Phase I trial of vorinostat and doxorubicin in solid tumours: histone deacetylase 2 expression as a predictive marker. Br J Cancer. 2009; 101(7):1044-1050
82. Munster P, et al. Clinical and biological effects of valproic acid as a histone deacetylase inhibitor on tumor and surrogate tissues: phase I/II trial of valproic acid and epirubicin/FEC. Clin Cancer Res. 2009; 15(7):2488-2496
83. Fotheringham S, et al. Genome-wide loss-offunction screen reveals an important role for the proteasome in HDAC inhibitor-induced apoptosis. Cancer Cell. 2009;15(1):57-66
84. Khan O, et al. HR23B is a biomarker for tumor sensitivity to HDAC inhibitor-based therapy. Proc Natl Acad Sci U S A. 2010;107(14):6532-6537
85. Hurwitz JL, et al. Vorinostat/SAHA-induced apoptosis in malignant mesothelioma is FLIP/caspase 8-dependent and HR23B-independent. Eur J Cancer. 2012;48(7):1096-1107
86. Fantin VR, et al. Constitutive activation of signal transducers and activators of transcription predicts vorinostat resistance in cutaneous T-cell lymphoma. Cancer Res. 2008;68(10):3785-3794
87. Hu Y, et al. Overcoming resistance to histone deacetylase inhibitors in human leukemia with the redox modulating compound ®-phenylethyl isothiocyanate. Blood. 2010;116(15):2732-2741
88. Flotho C, et al. The DNA methyltransferase inhibitors azacitidine, decitabine and zebularine exert differential effects on cancer gene expression in acute myeloid leukemia cells. Leukemia. 2009;23(6):1019-1028
89. Bennett JM, et al. Proposals for the classification of the myelodysplastic syndromes. Br J Haematol. 1982;51(2):189-199
90. Swerdlow SH, et al. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. 4th ed. Lyon, France: IARC Press; 2008.