Methylation of tumor suppressor microRNAs: Lessons from lymphoid malignancies

Expert Review of Molecular Diagnostics

Volumn 12, Issue 7, 2012, Pages 755-765

  Wang, Lu Qian ^a   Liang, Raymond ^a   Chim, Chor Sang ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

acute lymphoblastic leukemia; chronic lymphocytic leukemia; DNA methylation; multiple myeloma; tumor suppressor miRNAs

Indexed keywords

MESSENGER RNA; TUMOR SUPPRESSOR PROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; CARCINOGENESIS; CHRONIC LYMPHATIC LEUKEMIA; DNA METHYLATION; GENE EXPRESSION; GENE SILENCING; HUMAN; LEUKEMIA; LYMPHATIC LEUKEMIA; MULTIPLE MYELOMA; RNA METHYLATION; RNA SEQUENCE; TUMOR SUPPRESSOR GENE;

DNA METHYLATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HEMATOLOGIC NEOPLASMS; HUMANS; LEUKEMIA, LYMPHOID; LYMPHOMA; MICRORNAS;

EID: 84869475176     PISSN: 14737159     EISSN: 17448352     Source Type: Journal    
DOI: 10.1586/erm.12.64     Document Type: Article

References (134)

1. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5), 843-854 (1993). (Pubitemid 24014542)
2. Griffths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res. 36(Suppl. 1), D154-D158 (2008). (Pubitemid 351149713)
3. Ambros V. The functions of animal microRNAs. Nature 431(7006), 350-355 (2004). (Pubitemid 39265675)
4. David PB. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2), 281-297 (2004).
5. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 115(7), 787-798 (2003). (Pubitemid 38058492)
6. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 136(2), 215-233 (2009).
7. Lim LP, Lau NC, Garrett-Engele P et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433(7027), 769-773 (2005). (Pubitemid 40292988)
8. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often fanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120(1), 15-20 (2005). (Pubitemid 40094598)
9. Zhang B, Pan X, Cobb GP, Anderson TA. MicroRNAs as oncogenes and tumor suppressors. Dev. Biol. 302(1), 1-12 (2007). (Pubitemid 46096921)
10. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat. Rev. Cancer 6(4), 259-269 (2006).
11. Chen CZ. MicroRNAs as oncogenes and tumor suppressors. N. Engl. J. Med. 353 (17), 1768-1771 (2005).
12. Laird PW. Cancer epigenetics. Hum. Mol. Genet. 14(Suppl. 1), R65-R76 (2005). (Pubitemid 40542622)
13. Esteller M. Epigenetics in cancer. N. Engl. J. Med. 358 (11), 1148-1159 (2008).
14. Bird AP, Wolffe AP. Methylation-induced repression-belts, braces, and chromatin. Cell 99(5), 451-454 (1999). (Pubitemid 129746827)
15. Shen L, Kondo Y, Guo Y et al. Genome-wide profling of DNA methylation reveals a class of normally methylated CpG-island promoters. PLoS Genet. 3(10), 2023-2036 (2007).
16. Ioshikhes IP, Zhang MQ. Large-scale human promoter mapping using CpG islands. Nat. Genet. 26(1), 61-63 (2000).
17. Kim TH, Barrera LO, Zheng M et al. A high-resolution map of active promoters in the human genome. Nature 436(7052), 876-880 (2005). (Pubitemid 41160649)
18. Chim CS, Liang R, Kwong YL. Hypermethylation of gene promoters in hematological neoplasia. Hematol. Oncol. 20(4), 167-176 (2002). (Pubitemid 36070076)
19. Fazzari MJ, Greally JM. Epigenomics: beyond CpG islands. Nat. Rev. Genet. 5(6), 446-455 (2004). (Pubitemid 38915411)
20. Gardiner-Garden M, Frommer M. CpG islands in vertebrate genomes. J. Mol. Biol. 196 (2), 261-282 (1987). (Pubitemid 17122132)
21. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 16(1), 6-21 (2002). (Pubitemid 34049633)
22. Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9(6), 465-476 (2008). (Pubitemid 351693975)
23. Li E, Beard C, Jaenisch R. Role for DNA methylation in genomic imprinting. Nature 366(6453), 362-365 (1993). (Pubitemid 23349366)
24. Paulsen M, Ferguson-Smith AC. DNA methylation in genomic imprinting, development, and disease. J. Pathol. 195(1), 97-110 (2001).
25. Knudson AG. Karnofsky Memorial Lecture. Hereditary cancer: theme and variations. J. Clin. Oncol. 15(10), 3280-3287 (1997). (Pubitemid 27419342)
26. Weinberg RA. Tumor suppressor genes. Science 254(5035), 1138-1146 (1991). (Pubitemid 21917438)
27. + primary effusion lymphomas (body cavity-based lymphomas). Leukemia 12 (10), 1507-1517 (1998). (Pubitemid 28470432)
28. Siegfried Z, Eden S, Mendelsohn M, Feng X, Tsuberi BZ, Cedar H. DNA methylation represses transcription in vivo. Nat. Genet. 22(2), 203-206 (1999). (Pubitemid 29264820)
29. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med. 349(21), 2042-2054 (2003). (Pubitemid 37448928)
30. Berger AH, Knudson AG, Pandolf PP. A continuum model for tumour suppression. Nature 476 (7359), 163-169 (2011).
31. Feinberg A P, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 301(5895), 89-92 (1983). (Pubitemid 13154475)
32. Esteller M, Fraga MF, Guo M et al. DNA methylation patterns in hereditary human cancers mimic sporadic tumorigenesis. Hum. Mol. Genet. 10(26), 3001-3007 (2001). (Pubitemid 34083486)
33. Costello JF, Frühwald MC, Smiraglia DJ et al. Aberrant CpG-island methylation has nonrandom and tumour-type-specifc patterns. Nat. Genet. 24(2), 132-138 (2000). (Pubitemid 30094712)
34. Greger V, Passarge E, Höpping W, Messmer E, Horsthemke B. Epigenetic changes may contribute to the formation and spontaneous regression of retinoblastoma. Hum. Genet. 83(2), 155-158 (1989).
35. Herman JG, Latif F, Weng Y et al. Silencing of the VHL tumor suppressor gene by DNA methylation in renal carcinoma. Proc. Natl Acad. Sci. USA 91(21), 9700-9704 (1994). (Pubitemid 24311875)
36. Kane MF, Loda M, Gaida GM et al. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res. 57(5), 808-811 (1997). (Pubitemid 27097998)
37. Esteller M, Silva JM, Dominguez G et al. Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors. J. Natl Cancer Inst. 92(7), 564-569 (2000). (Pubitemid 30212318)
38. Gonzalez-Zulueta M, Bender CM, Yang AS et al. Methylation of the 5́ CpG island of the p16/CDKN2 tumor suppressor gene in normal and transformed human tissues correlates with gene silencing. Cancer Res. 55(20), 4531-4535 (1995).
39. Chim CS, Pang R, Fung TK, Choi CL, Liang R. Epigenetic dysregulation of Wnt signaling pathway in multiple myeloma. Leukemia 21(12), 2527-2536 (2007). (Pubitemid 350148897)
40. Raval A, Tanner SM, Byrd JC et al. Downregulation of death-associated protein kinase 1 (DAPK1) in chronic lymphocytic leukemia. Cell 129(5), 879-890 (2007). (Pubitemid 46813150)
41. Chim CS, Fung TK, Cheung WC, Liang R, Kwong YL. SOCS1 and SHP1 hypermethylation in multiple myeloma: implications for epigenetic activation of the JAK/STAT pathway. Blood 103(12), 4630-4635 (2004). (Pubitemid 38745995)
42. Chim CS, Kwong YL, Fung TK, Liang R. Methylation profling in multiple myeloma. Leuk. Res. 28(4), 379-385 (2004).
43. De Carvalho DD, Sharma S, You JS et al. DNA methylation screening identifes driver epigenetic events of cancer cell survival. Cancer Cell 21(5), 655-667 (2012).
44. Bozic I, Antal T, Ohtsuki H et al. Accumulation of driver and passenger mutations during tumor progression. Proc. Natl Acad. Sci. USA 107(43), 18545-18550 (2010).
45. Klein U, Lia M, Crespo M et al. The DLEU2/miR-15a/16-1 cluster controls B-cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 17(1), 28-40 (2010).
46. Tommasi S, Karm DL, Wu X, Yen Y, Pfeifer GP. Methylation of homeobox genes is a frequent and early epigenetic event in breast cancer. Breast Cancer Res. 11(1), R14 (2009).
47. Kalari S, Pfeifer GP. Identifcation of driver and passenger DNA methylation in cancer by epigenomic analysis. Adv. Genet. 70, 277-308 (2010).
48. Clark SJ, Harrison J, Paul CL, Frommer M. High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 22(15), 2990-2997 (1994). (Pubitemid 24260626)
49. Herman JG, Graff JR, Myöhänen S, Nelkin BD, Baylin SB. Methylation-specifc PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl Acad. Sci. USA 93(18), 9821-9826 (1996). (Pubitemid 26296693)
50. Tost J, Gut IG. DNA methylation analysis by pyrosequencing. Nat. Protoc. 2(9), 2265-2275 (2007). (Pubitemid 351575045)
51. Colella S, Shen L, Baggerly KA, Issa JP, Krahe R. Sensitive and quantitative universal pyrosequencing methylation analysis of CpG sites. BioTechniques 35(1), 146-150 (2003). (Pubitemid 36828724)
52. Cokus SJ, Feng S, Zhang X et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452 (7184), 215-219 (2008). (Pubitemid 351380251)
53. Lister R, Pelizzola M, Dowen RH et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462(7271), 315-322 (2009).
54. Weber M, Davies JJ, Wittig D et al. Chromosome-wide and promoter-specifc analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet. 37(8), 853-862 (2005). (Pubitemid 41077111)
55. Mohn F, Weber M, Schübeler D, Roloff TC. Methylated DNA immunoprecipitation (MeDIP). Methods Mol. Biol. 507, 55-64 (2009).
56. Jacinto FV, Ballestar E, Esteller M. Methyl-DNA immunoprecipitation (MeDIP): hunting down the DNA methylome. BioTechniques 44(1), 35, 37, 39 passim (2008).
57. Weber M, Hellmann I, Stadler MB et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet. 39(4), 457-466 (2007). (Pubitemid 46514772)
58. ® assay. Epigenomics 1(1), 177-200 (2009).
59. Bibikova M, Barnes B, Tsan C et al. High density DNA methylation array with single-CpG-site resolution. Genomics 98(4), 288-295 (2011).
60. Li Y, Zhu J, Tian G et al. The DNA methylome of human peripheral blood mononuclear cells. PLoS Biol. 8(11), e1000533 (2010).
61. Yang AS, Doshi KD, Choi SW et al. DNA methylation changes after 5-aza-2́-deoxycytidine therapy in patients with leukemia. Cancer Res. 66(10), 5495-5503 (2006). (Pubitemid 43844978)
62. Christman JK. 5-Azacytidine and 5-aza-2́-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 21(35), 5483-5495 (2002). (Pubitemid 34983483)
63. Suzuki H, Gabrielson E, Chen W et al. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat. Genet. 31(2), 141-149 (2002).
64. Laird PW. Principles and challenges of genome-wide DNA methylation analysis. Nat. Rev. Genet. 11(3), 191-203 (2010).
65. Krueger F, Kreck B, Franke A, Andrews SR. DNA methylome analysis using short bisulfte sequencing data. Nat. Methods 9(2), 145-151 (2012).
66. Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A. Preparation of reduced representation bisulfte sequencing libraries for genome-scale DNA methylation profling. Nat. Protoc. 6(4), 468-481 (2011).
67. Lister R, Ecker Jr. Finding the ffth base: genome-wide sequencing of cytosine methylation. Genome Res. 19(6), 959-966 (2009).
68. Saito Y, Liang G, Egger G et al. Specifc activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 9(6), 435-443 (2006). (Pubitemid 43832188)
69. Lujambio A, Ropero S, Ballestar E et al. Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res. 67(4), 1424-1429 (2007). (Pubitemid 46383366)
70. Wilting SM, van Boerdonk RA, Henken FE et al. Methylation-mediated silencing and tumour suppressive function of Hsa-miR-124 in cervical cancer. Mol. Cancer 9, 167 (2010).
71. Furuta M, Kozaki KI, Tanaka S, Arii S, Imoto I, Inazawa J. miR-124 and miR-203 are epigenetically silenced tumor suppressive microRNAs in hepatocellular carcinoma. Carcinogenesis 31(5), 766-776 (2010).
72. Craig VJ, Cogliatti SB, Rehrauer H, Wündisch T, Müller A. Epigenetic silencing of microRNA-203 dysregulates ABL1 expression and drives Helicobacter-associated gastric lymphomagenesis. Cancer Res. 71(10), 3616-3624 (2011).
73. Tsai KW, Wu CW, Hu LY et al. Epigenetic regulation of miR-34b and miR-129 expression in gastric cancer. Int. J. Cancer 129(11), 2600-2610 (2011).
74. Chen X, Hu H, Guan X et al. CpG-island methylation status of miRNAs in esophageal squamous cell carcinoma. Int. J. Cancer 130(7), 1607-1613 (2012).
75. Huang YW, Liu JC, Deatherage DE et al. Epigenetic repression of microRNA-129-2 leads to overexpression of SOX4 oncogene in endometrial cancer. Cancer Res. 69(23), 9038-9046 (2009).
76. Bandres E, Agirre X, Bitarte N et al. Epigenetic regulation of microRNA expression in colorectal cancer. Int. J. Cancer 125(11), 2737-2743 (2009).
77. Cheung HH, Davis AJ, Lee TL et al. Methylation of an intronic region regulates miR-199a in testicular tumor malignancy. Oncogene 30(31), 3404-3415 (2011).
78. Toyota M, Suzuki H, Sasaki Y et al. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG-island methylation in colorectal cancer. Cancer Res. 68(11), 4123-4132 (2008).
79. Dores GM, Anderson WF, Curtis RE et al. Chronic lymphocytic leukaemia and small lymphocytic lymphoma: overview of the descriptive epidemiology. Br. J. Haematol. 139(5), 809-819 (2007). (Pubitemid 350115721)
80. Fais F, Ghiotto F, Hashimoto S et al. Chronic lymphocytic leukemia B-cells express restricted sets of mutated and unmutated antigen receptors. J. Clin. Invest. 102 (8), 1515-1525 (1998). (Pubitemid 28492218)
81. Oscier DG, Gardiner AC, Mould SJ et al. Multivariate analysis of prognostic factors in CLL: clinical stage, IgVH gene mutational status, and loss or mutation of the p53 gene are independent prognostic factors. Blood 100(4), 1177-1184 (2002). (Pubitemid 34864269)
82. Damle RN, Wasil T, Fais F et al. IgV gene mutation status and CD38 expression as novel prognostic indicators in chronic lymphocytic leukemia. Blood 94(6), 1840-1847 (1999). (Pubitemid 29430399)
83. Hamblin TJ, Davis Z, Gardiner A, Oscier DG, Stevenson FK. Unmutated Ig V(H) genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood 94(6), 1848-1854 (1999). (Pubitemid 29430400)
84. Döhner H, Stilgenbauer S, Benner A et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N. Engl. J. Med. 343(26), 1910-1916 (2000). (Pubitemid 32064784)
85. Haferlach C, Dicker F, Schnittger S, Kern W, Haferlach T. Comprehensive genetic characterization of CLL: a study on 506 cases analysed with chromosome banding analysis, interphase FISH, IgV(H) status and immunophenotyping. Leukemia 21(12), 2442-2451 (2007). (Pubitemid 350148886)
86. Dighiero G, Hamblin TJ. Chronic lymphocytic leukaemia. Lancet 371(9617), 1017-1029 (2008). (Pubitemid 351389535)
87. Crespo M, Bosch F, Villamor N et al. ZAP70 expression as a surrogate for immunoglobulin-variable-region mutations in chronic lymphocytic leukemia. N. Engl. J. Med. 348(18), 1764-1775 (2003). (Pubitemid 36514707)
88. Wiestner A, Rosenwald A, Barry TS et al. ZAP70 expression identifes a chronic lymphocytic leukemia subtype with unmutated immunoglobulin genes, inferior clinical outcome, and distinct gene expression profle. Blood 101(12), 4944-4951 (2003). (Pubitemid 36857758)
89. Rai KR, Sawitsky A, Cronkite EP, Chanana AD, Levy RN, Pasternack BS. Clinical staging of chronic lymphocytic leukemia. Blood 46(2), 219-234 (1975).
90. Rassenti LZ, Huynh L, Toy TL et al. ZAP70 compared with immunoglobulin heavy-chain gene mutation status as a predictor of disease progression in chronic lymphocytic leukemia. N. Engl. J. Med. 351(9), 893-901 (2004). (Pubitemid 39096916)
91. Binet JL, Auquier A, Dighiero G et al. A new prognostic classifcation of chronic lymphocytic leukemia derived from a multivariate survival analysis. Cancer 48(1), 198-206 (1981). (Pubitemid 11064396)
92. Calin GA, Dumitru CD, Shimizu M et al. Frequent deletions and downregulation of micro-RNA genes miR15 and miR-16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl Acad. Sci. USA 99(24), 15524-15529 (2002). (Pubitemid 35403967)
93. Calin GA, Cimmino A, Fabbri M et al. MiR-15a and miR-16-1 cluster functions in human leukemia. Proc. Natl Acad. Sci. USA 105(13), 5166-5171 (2008). (Pubitemid 351738528)
94. Auer RL, Riaz S, Cotter FE. The 13q and 11q B-cell chronic lymphocytic leukaemia-associated regions derive from a common ancestral region in the zebrafsh. Br. J. Haematol. 137(5), 443-453 (2007). (Pubitemid 46698292)
95. Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY. MicroRNA-34b and microRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res. 67(18), 8433-8438 (2007). (Pubitemid 47437414)
96. Fabbri M, Bottoni A, Shimizu M et al. Association of a microRNA/TP53 feedback circuitry with pathogenesis and outcome of B-cell chronic lymphocytic leukemia. JAMA 305(1), 59-67 (2011).
97. Calin GA, Liu CG, Sevignani C et al. MicroRNA profling reveals distinct signatures in B-cell chronic lymphocytic leukemias. Proc. Natl Acad. Sci. USA 101(32), 11755-11760 (2004). (Pubitemid 39095368)
98. Marton S, Garcia MR, Robello C et al. Small RNAs analysis in CLL reveals a deregulation of miRNA expression and novel miRNA candidates of putative relevance in CLL pathogenesis. Leukemia 22(2), 330-338 (2008). (Pubitemid 351250538)
99. Calin GA, Ferracin M, Cimmino A et al. A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med. 353(17), 1793-1801 (2005). (Pubitemid 41549891)
100. Fulci V, Chiaretti S, Goldoni M et al. Quantitative technologies establish a novel microRNA profle of chronic lymphocytic leukemia. Blood 109(11), 4944-4951 (2007). (Pubitemid 46827793)
101. Visone R, Rassenti LZ, Veronese A et al. Karyotype-specifc microRNA signature in chronic lymphocytic leukemia. Blood 114(18), 3872-3879 (2009).
102. Stamatopoulos B, Meuleman N, Haibe-Kains B et al. MicroRNA-29c and microRNA-223 downregulation has in vivo signifcance in chronic lymphocytic leukemia and improves disease risk stratifcation. Blood 113(21), 5237-5245 (2009).
103. Garzon R, Liu S, Fabbri M et al. MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene re-expression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood 113(25), 6411-6418 (2009).
104. Pallasch CP, Patz M, Park YJ et al. miRNA deregulation by epigenetic silencing disrupts suppression of the oncogene PLAG1 in chronic lymphocytic leukemia. Blood 114(15), 3255-3264 (2009).
105. Ward BP, Tsongalis GJ, Kaur P. MicroRNAs in chronic lymphocytic leukemia. Exp. Mol. Pathol. 90(2), 173-178 (2011).
106. Wong KY, Yu L, Chim CS. DNA methylation of tumor suppressor miRNA genes: a lesson from the miR-34 family. Epigenomics 3(1), 83-92 (2011).
107. Mraz M, Malinova K, Kotaskova J et al. miR-34a, miR-29c and miR-17-5p are downregulated in CLL patients with TP53 abnormalities. Leukemia 23 (6), 1159-1163 (2009).
108. Rossi D, Cerri M, Deambrogi C et al. The prognostic value of TP53 mutations in chronic lymphocytic leukemia is independent of del17p13: implications for overall survival and chemorefractoriness. Clin. Cancer Res. 15(3), 995-1004 (2009).
109. Cordone I, Masi S, Mauro FR et al. p53 expression in B-cell chronic lymphocytic leukemia: a marker of disease progression and poor prognosis. Blood 91(11), 4342-4349 (1998). (Pubitemid 28261999)
110. Lodygin D, Tarasov V, Epanchintsev A et al. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 7(16), 2591-2600 (2008).
111. Chim CS, Wong KY, Qi Y et al. Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 31(4), 745-750 (2010).
112. Wong KY, So CC, Loong F et al. Epigenetic inactivation of the miR-124-1 in haematological malignancies. PLoS ONE 6(4), e19027 (2011).
113. Bueno MJ, Pérez de Castro I, Gómez de Cedrón M et al. Genetic and epigenetic silencing of microRNA-203 enhances ABL1 and BCR-ABL1 oncogene expression. Cancer Cell 13(6), 496-506 (2008). (Pubitemid 351763902)
114. Chim CS, Wong KY, Leung CY et al. Epigenetic inactivation of the Hsa-miR-203 in haematological malignancies. J. Cell. Mol. Med. 15(12), 2760-2767 (2011).
115. Palamarchuk A, Yan PS, Zanesi N et al. Tcl1 protein functions as an inhibitor of de novo DNA methylation in B-cell chronic lymphocytic leukemia (CLL). Proc. Natl Acad. Sci. USA 109 (7), 2555-2560 (2012).
116. Kuehl WM, Bergsagel PL. Multiple myeloma: evolving genetic events and host interactions. Nat. Rev. Cancer 2(3), 175-187 (2002). (Pubitemid 37328787)
117. Hideshima T, Mitsiades C, Tonon G, Richardson PG, Anderson KC. Understanding multiple myeloma pathogenesis in the bone marrow to identify new therapeutic targets. Nat. Rev. Cancer 7(8), 585-598 (2007). (Pubitemid 47106630)
118. Kyle RA, Therneau TM, Rajkumar SV et al. A long-term study of prognosis in monoclonal gammopathy of undetermined signifcance. N. Engl. J. Med. 346(8), 564-569 (2002). (Pubitemid 34438817)
119. Bergsagel PL, Kuehl WM. Molecular pathogenesis and a consequent classifcation of multiple myeloma. J. Clin. Oncol. 23(26), 6333-6338 (2005). (Pubitemid 46218843)
120. Chim CS, Liang R, Leung MH, Yip SF, Kwong YL. Aberrant gene promoter methylation marking disease progression in multiple myeloma. Leukemia 20(6), 1190-1192 (2006).
121. Wong KY, Yim RL, So CC, Jin DY, Liang R, Chim CS. Epigenetic inactivation of the MIR34B/C in multiple myeloma. Blood 118(22), 5901-5904 (2011).
122. Wong KY, Liang R, So CC, Jin DY, Costello JF, Chim CS. Epigenetic silencing of MIR203 in multiple myeloma. Br. J. Haematol. 154(5), 569-578 (2011).
123. Ribera JM, Oriol A, Bethencourt C et al.; PETHEMA Group, Spain. Comparison of intensive chemotherapy, allogeneic or autologous stem cell transplantation as post-remission treatment for adult patients with high-risk acute lymphoblastic leukemia. Results of the PETHEMA ALL-93 trial. Haematologica 90(10), 1346-1356 (2005). (Pubitemid 41503650)
124. Agirre X, Vilas-Zornoza A, Jiménez-Velasco A et al. Epigenetic silencing of the tumor suppressor microRNA Hsa-miR-124a regulates CDK6 expression and confers a poor prognosis in acute lymphoblastic leukemia. Cancer Res. 69(10), 4443-4453 (2009).
125. Calin GA, Croce CM. Chronic lymphocytic leukemia: interplay between noncoding RNAs and protein-coding genes. Blood 114(23), 4761-4770 (2009).
126. Chim CS, Liang R, Tam CY, Kwong YL. Methylation of p15 and p16 genes in acute promyelocytic leukemia: potential diagnostic and prognostic signifcance. J. Clin. Oncol. 19(7), 2033-2040 (2001). (Pubitemid 32702548)
127. Chim CS, Wong SY, Pang A et al. Aberrant promoter methylation of the retinoic acid receptor a gene in acute promyelocytic leukemia. Leukemia 19(12), 2241-2246 (2005). (Pubitemid 41741620)
128. Chim CS, Lau JS, Wong KF, Kwong YL. CDKN2B methylation is an independent poor prognostic factor in newly diagnosed acute promyelocytic leukemia. Leukemia 20(1), 149-151 (2006).
129. Chim CS, Ma SY, Au WY et al. Primary nasal natural killer cell lymphoma: long-term treatment outcome and relationship with the International Prognostic Index. Blood 103(1), 216-221 (2004).
130. Chim CS, Tam CY, Liang R, Kwong YL. Methylation of p15 and p16 genes in adult acute leukemia: lack of prognostic signifcance. Cancer 91(12), 2222-2229 (2001). (Pubitemid 32552806)
131. Chim CS, Wong SY, Kwong YL. Aberrant gene promoter methylation in acute promyelocytic leukaemia: profle and prognostic signifcance. Br. J. Haematol. 122(4), 571-578 (2003). (Pubitemid 36995212)
132. Chim CS, Wong AS, Kwong YL. Infrequent hypermethylation of CEBPA promotor in acute myeloid leukaemia. Br. J. Haematol. 119 (4), 988-990 (2002). (Pubitemid 35463824)
133. Zhang YJ, Wu HC, Shen J et al. Predicting hepatocellular carcinoma by detection of aberrant promoter methylation in serum DNA. Clin. Cancer Res. 13(8), 2378-2384 (2007). (Pubitemid 46698587)
134. Mori T, O'Day SJ, Umetani N et al. Predictive utility of circulating methylated DNA in serum of melanoma patients receiving biochemotherapy. J. Clin. Oncol. 23(36), 9351-9358 (2005).