DNA methylation of tumor suppressor miRNA genes: A lesson from the miR-34 family

Epigenomics

Volumn 3, Issue 1, 2011, Pages 83-92

  Wong, Kwan Yeung ^a   Yu, Li ^b   Chim, Chor Sang ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

cancer; DNA methylation; microRNA; miR 34; tumor suppressor

Indexed keywords

4 PHENYLBUTYRIC ACID; 5 AZA 2' DEOXYCYTIDINE; MICRORNA; PROTEIN P53; TRICHOSTATIN A;

ACUTE LYMPHOBLASTIC LEUKEMIA; BILE DUCT CANCER; BLADDER CANCER; BREAST CANCER; CANCER CELL; CHRONIC MYELOID LEUKEMIA; COLON CANCER; DEREGULATION; DNA METHYLATION; ENDOMETRIUM CANCER; GENE EXPRESSION; GENE INACTIVATION; GENE SILENCING; GENE STRUCTURE; HUMAN; LIVER CANCER; MELANOMA; MOUTH CANCER; PANCREAS CANCER; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; REVIEW; STOMACH CANCER; TUMOR SUPPRESSOR GENE; UTERINE CERVIX CANCER;

DNA METHYLATION; GENES, TUMOR SUPPRESSOR; HUMANS; MICRORNAS; MODELS, BIOLOGICAL; MULTIGENE FAMILY; NEOPLASMS; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P53;

EID: 79951938163     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.10.74     Document Type: Review

References (104)

1. Esteller M: Epigenetics in cancer. N. Engl. J. Med. 358(11), 1148-1159 (2008).
2. Laird PW: Cancer epigenetics. Hum. Mol. Genet. 14(Suppl. 1), R65-R76 (2005). (Pubitemid 40542622)
3. Robertson KD: DNA methylation and human disease. Nat. Rev. Genet. 6(8), 597-610 (2005). (Pubitemid 41044297)
4. Herman JG, Baylin SB: Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med. 349(21), 2042-2054 (2003). (Pubitemid 37448928)
5. Jones PA, Baylin SB: The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 3(6), 415-428 (2002). (Pubitemid 34587077)
6. Saxonov S, Berg P, Brutlag DL: A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc. Natl Acad. Sci. USA 103(5), 1412-1417 (2006). (Pubitemid 43191179)
7. Das PM, Singal R: DNA methylation and cancer. J. Clin. Oncol. 22(22), 4632-4642 (2004). (Pubitemid 41185132)
8. Fazzari MJ, Greally JM: Epigenomics: Beyond CpG islands. Nat. Rev. Genet. 5(6), 446-455 (2004). (Pubitemid 38915411)
9. Ioshikhes IP, Zhang MQ: Large-scale human promoter mapping using CpG islands. Nat. Genet. 26(1), 61-63 (2000).
10. 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)
11. Chim CS, Liang R, Kwong YL: Hypermethylation of gene promoters in hematological neoplasia. Hematol. Oncol. 20(4), 167-176 (2002). (Pubitemid 36070076)
12. Costello JF, Plass C: Methylation matters. J. Med. Genet. 38(5), 285-303 (2001). (Pubitemid 32433981)
13. Bird A: Molecular biology: DNA methylation de novo. Science 286(5448), 2287-2288 (1999). (Pubitemid 30016879)
14. Singal R, Ginder GD: DNA methylation. Blood 93(12), 4059-4070 (1999). (Pubitemid 29279247)
15. Tuck-Muller CM, Narayan A, Tsien F et al.: DNA hypomethylation and unusual chromosome instability in cell lines from ICF syndrome patients. Cytogenet. Genome. Res. 89(1-2), 121-128 (2000). (Pubitemid 30435274)
16. Rizwana R, Hahn PJ: CpG methylation reduces genomic instability. J. Cell Science 112, 4513-4519 (1999). (Pubitemid 30034801)
17. Knudson AG: Two genetic hits (more or less) to cancer. Nat. Rev. Cancer 1(2), 157-162 (2001). (Pubitemid 33741891)
18. Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2), 281-297 (2004).
19. Calin GA, Croce CM: MicroRNA signatures in human cancers. Nat. Rev. Cancer 6(11), 857-866 (2006). (Pubitemid 44629897)
20. Esquela-Kerscher A, Slack FJ: Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 6(4), 259-269 (2006).
21. Chen CZ: MicroRNAs as oncogenes and tumor suppressors. N. Engl. J. Med. 353(17), 1768-1771 (2005).
22. Guil S, Esteller M: DNA methylomes, histone codes and miRNAs: tying it all together. Int. J. Biochem. Cell Biol. 41(1), 87-95 (2009).
23. Deng S, Calin GA, Croce CM, Coukos G, Zhang L: Mechanisms of microRNA deregulation in human cancer. Cell Cycle 7(17), 2643-2646 (2008).
24. Lujambio A, Esteller M: CpG island hypermethylation of tumor suppressor microRNAs in human cancer. Cell Cycle 6(12), 1455-1459 (2007).
25. Saito Y, Liang G, Egger G et al.: Specific 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)
26. Tarasov V, Jung P, Verdoodt B et al.: Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 6(13), 1586-1593 (2007). (Pubitemid 47327945)
27. Chang TC, Wentzel EA, Kent OA et al.: Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 26(5), 745-752 (2007). (Pubitemid 46856245)
28. Raver-Shapira N, Marciano E, Meiri E et al.: Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell 26(5), 731-743 (2007). (Pubitemid 46856247)
29. He L, He X, Lim LP et al.: A microRNA component of the p53 tumour suppressor network. Nature 447(7148), 1130-1134 (2007). (Pubitemid 47014436)
30. Bommer GT, Gerin I, Feng Y et al.: p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol. 17(15), 1298-1307 (2007). (Pubitemid 47176893)
31. 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)
32. 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).
33. Corney DC, Hwang C-I, Matoso A et al.: Frequent downregulation of miR-34 family in human ovarian cancers. Clin. Cancer Res. 16(4), 1119-1128 (2010).
34. Dalgard Cl, Gonzalez M, Deniro JE, O'Brien JM: Differential microRNA-34a expression and tumor suppressor function in retinoblastoma cells. Invest. Ophthalmol. Vis. Sci. 50(10), 4542-4551 (2009).
35. Duan W, Gao L, Wu X et al.: MicroRNA- 34a is an important component of prima-1-induced apoptotic network in human lung cancer cells. Int. J. Cancer 127(2), 313-320 (2010).
36. Kumamoto K, Spillare EA, Fujita K et al.: Nutlin-3a activates p53 to both down-regulate inhibitor of growth 2 and up-regulate miR-34a, miR-34b, and miR-34c expression, and induce senescence. Cancer Res. 68(9), 3193 (2008).
37. Luan S, Sun L, Huang F: MicroRNA-34a: a novel tumor suppressor in p53-mutant glioma cell line u251. Arch. Med. Res. 41(2), 67-74 (2010).
38. Zenz T, Habe S, Denzel T et al.: Detailed analysis of p53 pathway defects in fludarabine-refractory chronic lymphocytic leukemia (CLL): Dissecting the contribution of 17p deletion, TP53 mutation, p53-p21 dysfunction, and miR34a in a prospective clinical trial. Blood 114(13), 2589-2597 (2009).
39. Mraz M, Pospisilova S, Malinova K, Slapak I, Mayer J: MicroRNAs in chronic lymphocytic leukemia pathogenesis and disease subtypes. Leuk. Lymphoma 50(3), 506-509 (2009).
40. 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).
41. Zenz T, Mohr J, Eldering E et al.: MiR-34a as part of the resistance network in chronic lymphocytic leukemia. Blood 113(16), 3801-3808 (2009).
42. Dijkstra MK, Van Lom K, Tielemans D et al.: 17p13/TP53 deletion in B-CLL patients is associated with microRNA-34a downregulation. Leukemia 23(3), 625-627 (2008).
43. Ji Q, Hao X, Meng Y et al.: Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer 8(1), 266 (2008).
44. Asslaber D, Pinon JD, Seyfried I et al.: MicroRNA-34a expression correlates with MDM2 SNP309 polymorphism and treatment-free survival in chronic lymphocytic leukemia. Blood 115(21), 4191-4197 (2010).
45. Wang X, Wang HK, McCoy JP et al.: Oncogenic HPV infection interrupts the expression of tumor-suppressive miR-34a through viral oncoprotein E6. RNA 15(4), 637 (2009).
46. Ito T, Yagi S, Yamakuchi M: MicroRNA-34a regulation of endothelial senescence. Biochem. Biophys. Res. Commun. 398(4), 735-740 (2010).
47. Fujita Y, Kojima K, Hamada N et al.: Effects of miR-34a on cell growth and chemoresistance in prostate cancer PC3 cells. Biochem. Biophys. Res. Commun. 377(1), 114-119 (2008).
48. Yamakuchi M, Ferlito M, Lowenstein CJ: MiR-34a repression of SIRT1 regulates apoptosis. Proc. Natl Acad. Sci. 105(36), 13421-13426 (2008).
49. Welch C, Chen Y, Stallings RL: MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 26(34), 5017-5022 (2007). (Pubitemid 47172643)
50. Stallings RL, Nair P, Maris JM et al.: High-resolution analysis of chromosomal breakpoints and genomic instability identifies PTPRD as a candidate tumor suppressor gene in neuroblastoma. Cancer Res. 66(7), 3673 (2006).
51. Wei JS, Song YK, Durinck S et al.: The MYCN oncogene is a direct target of miR-34a. Oncogene 27(39), 5204-5213 (2008).
52. Cole KA, Attiyeh EF, Mosse YP et al.: A functional screen identifies miR-34a as a candidate neuroblastoma tumor suppressor gene. Mol. Cancer Res. 6(5), 735 (2008).
53. Tazawa H, Tsuchiya N, Izumiya M, Nakagama H: Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the e2f pathway in human colon cancer cells. Proc. Natl Acad. Sci. 104(39), 15472-15477 (2007). (Pubitemid 47502941)
54. Cheng J, Zhou L, Xie QF et al.: The impact of miR-34a on protein output in hepatocellular carcinoma HEPG2 cells. Proteomics 10(8), 1557-1572 (2010).
55. Li N, Fu H, Tie Y et al.: MiR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett. 275(1), 44-53 (2009).
56. Pang RT, Leung CO, Ye TM et al.: MicroRNA-34a suppresses invasion through downregulation of NOTCH1 and jagged1 in cervical carcinoma and choriocarcinoma cells. Carcinogenesis 31(6), 1037-1044 (2010).
57. Ichimura A, Ruike Y, Terasawa K, Shimizu K, Tsujimoto G: MicroRNA-34a inhibits cell proliferation by repressing mitogen-activated protein kinase kinase 1 during megakaryocytic differentiation of k562 cells. Mol. Pharmacol. 77(6), 1016-1024 (2010).
58. Navarro F, Gutman D, Meire E et al.: MiR-34a contributes to megakaryocytic differentiation of k562 cells independently of p53. Blood 114(10), 2181-2192 (2009).
59. Hashimi ST, Fulcher JA, Chang MH, Gov L, Wang S, Lee B: MicroRNA profiling identifies miR-34a and miR-21 and their target genes JAG1 and WNT1 in the coordinate regulation of dendritic cell differentiation. Blood 114(2), 404-414 (2009).
60. Witwer KW, Sisk JM, Gama L, Clements JE: MicroRNA regulation of IFN-{b} protein expression: rapid and sensitive modulation of the innate immune response. J. Immunol. 184(5), 2369-2376 (2010).
61. Hermeking H: The miR-34 family in cancer and apoptosis. Cell Death Differ. 17(2), 193-199 (2010).
62. 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).
63. Gallardo E, Navarro A, Vinolas N et al.: MiR-34a as a prognostic marker of relapse in surgically resected non-small-cell lung cancer. Carcinogenesis 30(11), 1903-1909 (2009).
64. Chim CS, Wong KY, Qi Y et al.: Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 31(4), 745-750 (2010).
65. Peller S, Rotter V: TP53 in hematological cancer: low incidence of mutations with significant clinical relevance. Hum. Mutat. 21(3), 277-284 (2003). (Pubitemid 36292969)
66. Lowe SW, Cepero E, Evan G: Intrinsic tumour suppression. Nature 432(7015), 307-315 (2004). (Pubitemid 39551658)
67. Kozaki K-I, Imoto I, Mogi S, Omura K, Inazawa J: Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res. 68(7), 2094-2105 (2008). (Pubitemid 351521781)
68. Roman-Gomez J, Agirre X, Jimenez- Velasco A et al.: Epigenetic regulation of microRNAs in acute lymphoblastic leukemia. J. Clin. Oncol. 27, 1316-1322 (2009).
69. Meek DW: Tumour suppression by p53: a role for the DNA damage response? Nat. Rev. Cancer 9(10), 714-723 (2009).
70. Soussi T, Beroud C: Assessing TP53 status in human tumours to evaluate clinical outcome. Nat. Rev. Cancer 1(3), 233-239 (2001).
71. Kastan MB, Bartek J: Cell-cycle checkpoints and cancer. Nature 432(7015), 316-323 (2004). (Pubitemid 39551659)
72. Moll UM, Petrenko O: The MDM2-p53 interaction. Mol. Cancer Res. 1(14), 1001-1008 (2003). (Pubitemid 38044975)
73. 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)
74. Chim CS, Liang R, Tam CYY, Kwong YL: Methylation of p15 and p16 genes in acute promyelocytic leukemia: potential diagnostic and prognostic significance. J. Clin. Oncol. 19(7), 2033-2040 (2001). (Pubitemid 32702548)
75. Chim CS, Wong ASY, Kwong YL: Epigenetic dysregulation of the JAK/STAT pathway by frequent aberrant methylation of SHP1 but not SOCS1 in acute leukaemias. Ann. Hematol. 83(8), 527-532 (2004). (Pubitemid 39144754)
76. Chim CS, Wong KY, Loong F, Lam WW, Srivastava G: Frequent epigenetic inactivation of Rb1 in addition to p15 and p16 in mantle cell and follicular lymphoma. Hum. Pathol. 38(12), 1849-1857 (2007). (Pubitemid 350179934)
77. 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)
78. Chim CS, Kwong YL: Adverse prognostic impact of CDKN2B hyper-methylation in acute promyelocytic leukemia. Leuk. Lymphoma 47(5), 815-825 (2006).
79. 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 (2005).
80. 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). (Pubitemid 43797324)
81. 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).
82. Chim CS, Tam CYY, Liang R, Kwong Yl: Methylation of p15 and p16 genes in adult acute leukemia. Cancer 91(12), 2222-2229 (2001).
83. Chim CS, Wong SY, Kwong YL: Aberrant gene promoter methylation in acute promyelocytic leukaemia: profile and prognostic significance. Br. J. Haematol. 122(4), 571-578 (2003). (Pubitemid 36995212)
84. Chim CS, Wong ASY, Kwong YL: Infrequent hypermethylation of cebpa promotor in acute myeloid leukaemia. Br. J. Haematol 119(4), 988-990 (2002). (Pubitemid 35463824)
85. Chim CS, Chan WWL, Pang A, Kwong YL: Preferential methylation of Wnt inhibitory factor-1 in acute promyelocytic leukemia: an independent poor prognostic factor. Leukemia 20(5), 907-909 (2006).
86. Chim CS, Liang R, Fung TK, Choi CL, Kwong YL: Epigenetic dysregulation of the death-associated protein kinase/p14/hdm2/ p53/apaf-1 apoptosis pathway in multiple myeloma. J. Clin. Pathol. 60(6), 664-669 (2007). (Pubitemid 46975222)
87. Zenz T, Dohner H, Stilgenbauer S: Genetics and risk-stratified approach to therapy in chronic lymphocytic leukemia. Best Pract. Res. Clin. Haematol. 20(3), 439-453 (2007). (Pubitemid 47250492)
88. Meng F, Wehbe-Janek H, Henson R, Smith H, Patel T: Epigenetic regulation of microRNA-370 by interleukin-6 in malignant human cholangiocytes. Oncogene 27(3), 378-386 (2007).
89. Lehmann U, Hasemeier B, Christgen M et al.: Epigenetic inactivation of microRNA gene hsa-miR-9-1 in human breast cancer. J. Path. 214(1), 17-24 (2008).
90. Wilting S, Van Boerdonk R, Henken F et al.: Methylation-mediated silencing and tumour suppressive function of hsa-mir-124 in cervical cancer. Mol. Cancer 9(1), 167 (2010).
91. Bandres E, Agirre X, Bitarte N et al.: Epigenetic regulation of microRNA expression in colorectal cancer. Int. J. Cancer 125(11), 2737-2743 (2009).
92. 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)
93. Balaguer F, Link A, Lozano JJ et al.: Epigenetic silencing of miR-137 is an early event in colorectal carcinogenesis. Cancer Res. 70(16), 6609-6618 (2010).
94. Grady WM, Parkin RK, Mitchell PS et al.: Epigenetic silencing of the intronic microRNA hsa-miR-342 and its host gene EVL in colorectal cancer. Oncogene 27(27), 3880-3888 (2008). (Pubitemid 351862055)
95. Huang Y-W, 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).
96. Vrba L, Jensen TJ, Garbe JC et al.: Role for DNA methylation in the regulation of miR-200c and miR-141 expression in normal and cancer cells. PLoS ONE 5(1), e8697 (2010).
97. Shen R, Pan S, Qi S, Lin X, Cheng S: Epigenetic repression of microRNA-129-2 leads to overexpression of SOX4 in gastric cancer. Biochem. Biophys. Res. Commun.394(4), 1047-1052 (2010).
98. Tsai K-W, Hu L-Y, Wu C-W et al.: Epigenetic regulation of miR-196b expression in gastric cancer. Genes Chromosomes Cancer 49(11), 969-980 (2010).
99. Saito Y, Suzuki H, Tsugawa H et al.: Chromatin remodeling at ALU repeats by epigenetic treatment activates silenced microRNA-512-5p with downregulation of Mcl-1 in human gastric cancer cells. Oncogene 28(30), 2738-2744 (2009).
100. Datta J, Kutay H, Nasser MW et al.: Methylation mediated silencing of microRNA-1 gene and its role in hepatocellular carcinogenesis. Cancer Res. 68(13), 5049-5058 (2008).
101. Lee KH, Lotterman C, Karikari C et al.: Epigenetic silencing of microRNA miR-107 regulates cyclin-dependent kinase 6 expression in pancreatic cancer. Pancreatology 9(3), 293-301 (2009).
102. Rauhala HE, Jalava SE, Isotalo J et al.: MiR-193b is an epigenetically regulated putative tumor suppressor in prostate cancer. Int. J. Cancer 127(6), 1363-1372 (2010).
103. Agirre X, Vilas-Zornoza A, Jimenez-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).
104. Bueno MJ, Perez De Castro I, Gomez De Cedron 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)