DNA methylation and microRNA dysregulation in cancer

Molecular Oncology

Volumn 6, Issue 6, 2012, Pages 567-578

  Suzuki, Hiromu ^a   Maruyama, Reo ^a   Yamamoto, Eiichiro ^a   Kai, Masahiro ^a  

^a SAPPORO MEDICAL UNIVERSITY   (Japan)

Author keywords

DNA methylation; Epigenetic silencing; MicroRNA; Tumor suppressor

Indexed keywords

ANTINEOPLASTIC AGENT; FLUOROURACIL; MICRORNA; MICRORNA 145; MICRORNA 33A; MICRORNA 34A; UNCLASSIFIED DRUG;

ANGIOGENESIS; APOPTOSIS; CANCER INHIBITION; CELL ADHESION; CELL CYCLE CHECKPOINT; CPG ISLAND; DISEASE MARKER; DNA METHYLATION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENOME; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 84869887497     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2012.07.007     Document Type: Review

References (121)

1. Agirre X., Vilas-Zornoza A., Jimenez-Velasco A., Martin-Subero J.I., Cordeu L., Garate L., San Jose-Eneriz E., Abizanda G., Rodriguez-Otero P., Fortes P., Rifon J., Bandres E., Calasanz M.J., Martin V., Heiniger A., Torres A., Siebert R., Roman-Gomez J., Prosper F. Epigenetic silencing of the tumor suppressor microRNA Hsa-miR-124a regulates CDK6 expression and confers a poor prognosis in acute lymphoblastic leukemia. Cancer Res. 2009, 69:4443-4453.
2. Ando T., Yoshida T., Enomoto S., Asada K., Tatematsu M., Ichinose M., Sugiyama T., Ushijima T. DNA methylation of microRNA genes in gastric mucosae of gastric cancer patients: its possible involvement in the formation of epigenetic field defect. Int. J. Cancer 2009, 124:2367-2374.
3. Balaguer F., Link A., Lozano J.J., Cuatrecasas M., Nagasaka T., Boland C.R., Goel A. Epigenetic silencing of miR-137 is an early event in colorectal carcinogenesis. Cancer Res. 2010, 70:6609-6618.
4. Bandres E., Agirre X., Bitarte N., Ramirez N., Zarate R., Roman-Gomez J., Prosper F., Garcia-Foncillas J. Epigenetic regulation of microRNA expression in colorectal cancer. Int. J. Cancer 2009, 125:2737-2743.
5. Bommer G.T., Gerin I., Feng Y., Kaczorowski A.J., Kuick R., Love R.E., Zhai Y., Giordano T.J., Qin Z.S., Moore B.B., MacDougald O.A., Cho K.R., Fearon E.R. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol. 2007, 17:1298-1307.
6. Braconi C., Huang N., Patel T. MicroRNA-dependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes. Hepatology 2010, 51:881-890.
7. Brueckner B., Stresemann C., Kuner R., Mund C., Musch T., Meister M., Sultmann H., Lyko F. The human let-7a-3 locus contains an epigenetically regulated microRNA gene with oncogenic function. Cancer Res. 2007, 67:1419-1423.
8. Bueno M.J., Perez de Castro I., Gomez de Cedron M., Santos J., Calin G.A., Cigudosa J.C., Croce C.M., Fernandez-Piqueras J., Malumbres M. Genetic and epigenetic silencing of microRNA-203 enhances ABL1 and BCR-ABL1 oncogene expression. Cancer Cell 2008, 13:496-506.
9. Calin G.A., Dumitru C.D., Shimizu M., Bichi R., Zupo S., Noch E., Aldler H., Rattan S., Keating M., Rai K., Rassenti L., Kipps T., Negrini M., Bullrich F., Croce C.M. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. U. S. A 2002, 99:15524-15529.
10. Ceppi P., Mudduluru G., Kumarswamy R., Rapa I., Scagliotti G.V., Papotti M., Allgayer H. Loss of miR-200c expression induces an aggressive, invasive, and chemoresistant phenotype in non-small cell lung cancer. Mol. Cancer Res. 2010, 8:1207-1216.
11. Chen Q., Chen X., Zhang M., Fan Q., Luo S., Cao X. miR-137 is frequently down-regulated in gastric cancer and is a negative regulator of Cdc42. Dig. Dis. Sci. 2011, 56:2009-2016.
12. Chen X., Hu H., Guan X., Xiong G., Wang Y., Wang K., Li J., Xu X., Yang K., Bai Y. CpG island methylation status of miRNAs in esophageal squamous cell carcinoma. Int. J. Cancer 2012, 130:1607-1613.
13. Craig V.J., Cogliatti S.B., Rehrauer H., Wundisch T., Muller A. Epigenetic silencing of microRNA-203 dysregulates ABL1 expression and drives Helicobacter-associated gastric lymphomagenesis. Cancer Res. 2011, 71:3616-3624.
14. Croce C.M. Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 2009, 10:704-714.
15. Cummins J.M., He Y., Leary R.J., Pagliarini R., Diaz L.A., Sjoblom T., Barad O., Bentwich Z., Szafranska A.E., Labourier E., Raymond C.K., Roberts B.S., Juhl H., Kinzler K.W., Vogelstein B., Velculescu V.E. The colorectal microRNAome. Proc. Natl. Acad. Sci. U. S. A 2006, 103:3687-3692.
16. Datta J., Kutay H., Nasser M.W., Nuovo G.J., Wang B., Majumder S., Liu C.G., Volinia S., Croce C.M., Schmittgen T.D., Ghoshal K., Jacob S.T. Methylation mediated silencing of microRNA-1 gene and its role in hepatocellular carcinogenesis. Cancer Res. 2008, 68:5049-5058.
17. Davalos V., Moutinho C., Villanueva A., Boque R., Silva P., Carneiro F., Esteller M. Dynamic epigenetic regulation of the microRNA-200 family mediates epithelial and mesenchymal transitions in human tumorigenesis. Oncogene 2012, 31:2062-2074.
18. de Souza Rocha Simonini P., Breiling A., Gupta N., Malekpour M., Youns M., Omranipour R., Malekpour F., Volinia S., Croce C.M., Najmabadi H., Diederichs S., Sahin O., Mayer D., Lyko F., Hoheisel J.D., Riazalhosseini Y. Epigenetically deregulated microRNA-375 is involved in a positive feedback loop with estrogen receptor alpha in breast cancer cells. Cancer Res. 2010, 70:9175-9184.
19. Diaz V.M., Hurtado M., Thomson T.M., Reventos J., Paciucci R. Specific interaction of tissue-type plasminogen activator (t-PA) with annexin II on the membrane of pancreatic cancer cells activates plasminogen and promotes invasion in vitro. Gut 2004, 53:993-1000.
20. Douma S., Van Laar T., Zevenhoven J., Meuwissen R., Van Garderen E., Peeper D.S. Suppression of anoikis and induction of metastasis by the neurotrophic receptor TrkB. Nature 2004, 430:1034-1039.
21. Dudziec E., Miah S., Choudhry H.M., Owen H.C., Blizard S., Glover M., Hamdy F.C., Catto J.W. Hypermethylation of CpG islands and shores around specific microRNAs and mirtrons is associated with the phenotype and presence of bladder cancer. Clin. Cancer Res. 2011, 17:1287-1296.
22. Emoto K., Yamada Y., Sawada H., Fujimoto H., Ueno M., Takayama T., Kamada K., Naito A., Hirao S., Nakajima Y. Annexin II overexpression correlates with stromal tenascin-C overexpression: a prognostic marker in colorectal carcinoma. Cancer 2001, 92:1419-1426.
23. Esquela-Kerscher A., Slack F.J. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 2006, 6:259-269.
24. Esteller M. Non-coding RNAs in human disease. Nat. Rev. Genet. 2011, 12:861-874.
25. Fabbri M., Garzon R., Cimmino A., Liu Z., Zanesi N., Callegari E., Liu S., Alder H., Costinean S., Fernandez-Cymering C., Volinia S., Guler G., Morrison C.D., Chan K.K., Marcucci G., Calin G.A., Huebner K., Croce C.M. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc. Natl. Acad. Sci. U. S. A 2007, 104:15805-15810.
26. Feinberg A.P., Tycko B. The history of cancer epigenetics. Nat. Rev. Cancer 2004, 4:143-153.
27. Furuta M., Kozaki K.I., Tanaka S., Arii S., Imoto I., Inazawa J. miR-124 and miR-203 are epigenetically silenced tumor-suppressive microRNAs in hepatocellular carcinoma. Carcinogenesis 2010, 31:766-776.
28. Fuse M., Nohata N., Kojima S., Sakamoto S., Chiyomaru T., Kawakami K., Enokida H., Nakagawa M., Naya Y., Ichikawa T., Seki N. Restoration of miR-145 expression suppresses cell proliferation, migration and invasion in prostate cancer by targeting FSCN1. Int. J. Oncol. 2011, 38:1093-1101.
29. Gao X.N., Lin J., Li Y.H., Gao L., Wang X.R., Wang W., Kang H.Y., Yan G.T., Wang L.L., Yu L. MicroRNA-193a represses c-kit expression and functions as a methylation-silenced tumor suppressor in acute myeloid leukemia. Oncogene 2011, 30:3416-3428.
30. Giricz O., Reynolds P.A., Ramnauth A., Liu C., Wang T., Stead L., Childs G., Rohan T., Shapiro N., Fineberg S., Kenny P.A., Loudig O. Hsa-miR-375 is differentially expressed during breast lobular neoplasia and promotes loss of mammary acinar polarity. J. Pathol. 2012, 226:108-119.
31. Gregory P.A., Bert A.G., Paterson E.L., Barry S.C., Tsykin A., Farshid G., Vadas M.A., Khew-Goodall Y., Goodall G.J. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 2008, 10:593-601.
32. Hanoun N., Delpu Y., Suriawinata A.A., Bournet B., Bureau C., Selves J., Tsongalis G.J., Dufresne M., Buscail L., Cordelier P., Torrisani J. The silencing of microRNA 148a production by DNA hypermethylation is an early event in pancreatic carcinogenesis. Clin. Chem. 2010, 56:1107-1118.
33. Hashimoto Y., Akiyama Y., Otsubo T., Shimada S., Yuasa Y. Involvement of epigenetically silenced microRNA-181c in gastric carcinogenesis. Carcinogenesis 2010, 31:777-784.
34. He L., He X., Lim L.P., de Stanchina E., Xuan Z., Liang Y., Xue W., Zender L., Magnus J., Ridzon D., Jackson A.L., Linsley P.S., Chen C., Lowe S.W., Cleary M.A., Hannon G.J. A microRNA component of the p53 tumour suppressor network. Nature 2007, 447:1130-1134.
35. He Y., Cui Y., Wang W., Gu J., Guo S., Ma K., Luo X. Hypomethylation of the hsa-miR-191 locus causes high expression of hsa-mir-191 and promotes the epithelial-to-mesenchymal transition in hepatocellular carcinoma. Neoplasia 2011, 13:841-853.
36. Henry J.C., Azevedo-Pouly A.C., Schmittgen T.D. MicroRNA replacement therapy for cancer. Pharm. Res. 2011, 28:3030-3042.
37. Hildebrandt M.A., Gu J., Lin J., Ye Y., Tan W., Tamboli P., Wood C.G., Wu X. Hsa-miR-9 methylation status is associated with cancer development and metastatic recurrence in patients with clear cell renal cell carcinoma. Oncogene 2010, 29:5724-5728.
38. Hsu P.Y., Deatherage D.E., Rodriguez B.A., Liyanarachchi S., Weng Y.I., Zuo T., Liu J., Cheng A.S., Huang T.H. Xenoestrogen-induced epigenetic repression of microRNA-9-3 in breast epithelial cells. Cancer Res. 2009, 69:5936-5945.
39. Huang J., Wang Y., Guo Y., Sun S. Down-regulated microRNA-152 induces aberrant DNA methylation in hepatitis B virus-related hepatocellular carcinoma by targeting DNA methyltransferase 1. Hepatology 2010, 52:60-70.
40. Huang Y.W., Liu J.C., Deatherage D.E., Luo J., Mutch D.G., Goodfellow P.J., Miller D.S., Huang T.H. Epigenetic repression of microRNA-129-2 leads to overexpression of SOX4 oncogene in endometrial cancer. Cancer Res. 2009, 69:9038-9046.
41. Hui A.B., Bruce J.P., Alajez N.M., Shi W., Yue S., Perez-Ordonez B., Xu W., O'Sullivan B., Waldron J., Cummings B., Gullane P., Siu L., Liu F.F. Significance of dysregulated metadherin and microRNA-375 in head and neck cancer. Clin. Cancer Res. 2011, 17:7539-7550.
42. Ibrahim A.F., Weirauch U., Thomas M., Grunweller A., Hartmann R.K., Aigner A. MicroRNA replacement therapy for miR-145 and miR-33a is efficacious in a model of colon carcinoma. Cancer Res. 2011, 71:5214-5224.
43. Iorio M.V., Ferracin M., Liu C.G., Veronese A., Spizzo R., Sabbioni S., Magri E., Pedriali M., Fabbri M., Campiglio M., Menard S., Palazzo J.P., Rosenberg A., Musiani P., Volinia S., Nenci I., Calin G.A., Querzoli P., Negrini M., Croce C.M. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005, 65:7065-7070.
44. Iorio M.V., Visone R., Di Leva G., Donati V., Petrocca F., Casalini P., Taccioli C., Volinia S., Liu C.G., Alder H., Calin G.A., Menard S., Croce C.M. MicroRNA signatures in human ovarian cancer. Cancer Res. 2007, 67:8699-8707.
45. Irizarry R.A., Ladd-Acosta C., Wen B., Wu Z., Montano C., Onyango P., Cui H., Gabo K., Rongione M., Webster M., Ji H., Potash J.B., Sabunciyan S., Feinberg A.P. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet. 2009, 41:178-186.
46. Ji Q., Hao X., Zhang M., Tang W., Yang M., Li L., Xiang D., Desano J.T., Bommer G.T., Fan D., Fearon E.R., Lawrence T.S., Xu L. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One 2009, 4:e6816.
47. Johnson S.M., Grosshans H., Shingara J., Byrom M., Jarvis R., Cheng A., Labourier E., Reinert K.L., Brown D., Slack F.J. RAS is regulated by the let-7 microRNA family. Cell 2005, 120:635-647.
48. Jones P.A., Baylin S.B. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 2002, 3:415-428.
49. Jones P.A., Baylin S.B. The epigenomics of cancer. Cell 2007, 128:683-692.
50. Kalimutho M., Di Cecilia S., Del Vecchio Blanco G., Roviello F., Sileri P., Cretella M., Formosa A., Corso G., Marrelli D., Pallone F., Federici G., Bernardini S. Epigenetically silenced miR-34b/c as a novel faecal-based screening marker for colorectal cancer. Br. J. Cancer 2011, 104:1770-1778.
51. Kamimae S., Yamamoto E., Yamano H.O., Nojima M., Suzuki H., Ashida M., Hatahira T., Sato A., Kimura T., Yoshikawa K., Harada T., Hayashi S., Takamaru H., Maruyama R., Kai M., Nishiwaki M., Sugai T., Sasaki Y., Tokino T., Shinomura Y., Imai K., Toyota M. Epigenetic alteration of DNA in mucosal wash fluid predicts invasiveness of colorectal tumors. Cancer Prev. Res. 2011, 4:674-683.
52. Ke X.S., Qu Y., Rostad K., Li W.C., Lin B., Halvorsen O.J., Haukaas S.A., Jonassen I., Petersen K., Goldfinger N., Rotter V., Akslen L.A., Oyan A.M., Kalland K.H. Genome-wide profiling of histone h3 lysine 4 and lysine 27 trimethylation reveals an epigenetic signature in prostate carcinogenesis. PLoS One 2009, 4:e4687.
53. Kitano K., Watanabe K., Emoto N., Kage H., Hamano E., Nagase T., Sano A., Murakawa T., Nakajima J., Goto A., Fukayama M., Yatomi Y., Ohishi N., Takai D. CpG island methylation of microRNAs is associated with tumor size and recurrence of non-small-cell lung cancer. Cancer Sci. 2011, 102:2126-2131.
54. Kong K.L., Kwong D.L., Chan T.H., Law S.Y., Chen L., Li Y., Qin Y.R., Guan X.Y. MicroRNA-375 inhibits tumour growth and metastasis in oesophageal squamous cell carcinoma through repressing insulin-like growth factor 1 receptor. Gut 2012, 61:33-42.
55. Korpal M., Lee E.S., Hu G., Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 2008, 283:14910-14914.
56. Kozaki K., Imoto I., Mogi S., Omura K., Inazawa J. Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res. 2008, 68:2094-2105.
57. Kubo T., Toyooka S., Tsukuda K., Sakaguchi M., Fukazawa T., Soh J., Asano H., Ueno T., Muraoka T., Yamamoto H., Nasu Y., Kishimoto T., Pass H.I., Matsui H., Huh N.H., Miyoshi S. Epigenetic silencing of microRNA-34b/c plays an important role in the pathogenesis of malignant pleural mesothelioma. Clin. Cancer Res. 2011, 17:4965-4974.
58. Langevin S.M., Stone R.A., Bunker C.H., Grandis J.R., Sobol R.W., Taioli E. MicroRNA-137 promoter methylation in oral rinses from patients with squamous cell carcinoma of the head and neck is associated with gender and body mass index. Carcinogenesis 2010, 31:864-870.
59. Langevin S.M., Stone R.A., Bunker C.H., Lyons-Weiler M.A., Laframboise W.A., Kelly L., Seethala R.R., Grandis J.R., Sobol R.W., Taioli E. MicroRNA-137 promoter methylation is associated with poorer overall survival in patients with squamous cell carcinoma of the head and neck. Cancer 2011, 117:1454-1462.
60. Lehmann U., Hasemeier B., Christgen M., Muller M., Romermann D., Langer F., Kreipe H. Epigenetic inactivation of microRNA gene hsa-mir-9-1 in human breast cancer. J. Pathol. 2008, 214:17-24.
61. Li A., Omura N., Hong S.M., Vincent A., Walter K., Griffith M., Borges M., Goggins M. Pancreatic cancers epigenetically silence SIP1 and hypomethylate and overexpress miR-200a/200b in association with elevated circulating miR-200a and miR-200b levels. Cancer Res. 2010, 70:5226-5237.
62. Li X., Lin R., Li J. Epigenetic silencing of microRNA-375 regulates PDK1 expression in esophageal cancer. Dig. Dis. Sci. 2011, 56:2849-2856.
63. Liu C., Kelnar K., Liu B., Chen X., Calhoun-Davis T., Li H., Patrawala L., Yan H., Jeter C., Honorio S., Wiggins J.F., Bader A.G., Fagin R., Brown D., Tang D.G. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat. Med. 2011, 17:211-215.
64. Liu M., Lang N., Qiu M., Xu F., Li Q., Tang Q., Chen J., Chen X., Zhang S., Liu Z., Zhou J., Zhu Y., Deng Y., Zheng Y., Bi F. miR-137 targets Cdc42 expression, induces cell cycle G1 arrest and inhibits invasion in colorectal cancer cells. Int. J. Cancer 2011, 128:1269-1279.
65. Lodygin D., Tarasov V., Epanchintsev A., Berking C., Knyazeva T., Korner H., Knyazev P., Diebold J., Hermeking H. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 2008, 7:2591-2600.
66. Lopez-Serra P., Esteller M. DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer. Oncogene 2012, 31:1609-1622.
67. Lujambio A., Calin G.A., Villanueva A., Ropero S., Sanchez-Cespedes M., Blanco D., Montuenga L.M., Rossi S., Nicoloso M.S., Faller W.J., Gallagher W.M., Eccles S.A., Croce C.M., Esteller M. A microRNA DNA methylation signature for human cancer metastasis. Proc. Natl. Acad. Sci. U. S. A 2008, 105:13556-13561.
68. Lujambio A., Ropero S., Ballestar E., Fraga M.F., Cerrato C., Setien F., Casado S., Suarez-Gauthier A., Sanchez-Cespedes M., Git A., Spiteri I., Das P.P., Caldas C., Miska E., Esteller M. Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res. 2007, 67:1424-1429.
69. Ma K., He Y., Zhang H., Fei Q., Niu D., Wang D., Ding X., Xu H., Chen X., Zhu J. DNA methylation-regulated miR-193a-3p dictates resistance of hepatocellular carcinoma to 5-fluorouracil via repression of SRSF2 expression. J. Biol. Chem. 2012, 287:5639-5649.
70. Ma L., Young J., Prabhala H., Pan E., Mestdagh P., Muth D., Teruya-Feldstein J., Reinhardt F., Onder T.T., Valastyan S., Westermann F., Speleman F., Vandesompele J., Weinberg R.A. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell. Biol. 2010, 12:247-256.
71. Marson A., Levine S.S., Cole M.F., Frampton G.M., Brambrink T., Johnstone S., Guenther M.G., Johnston W.K., Wernig M., Newman J., Calabrese J.M., Dennis L.M., Volkert T.L., Gupta S., Love J., Hannett N., Sharp P.A., Bartel D.P., Jaenisch R., Young R.A. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008, 134:521-533.
72. Mazar J., DeBlasio D., Govindarajan S.S., Zhang S., Perera R.J. Epigenetic regulation of microRNA-375 and its role in melanoma development in humans. FEBS Lett. 2011, 585:2467-2476.
73. Mazar J., Khaitan D., DeBlasio D., Zhong C., Govindarajan S.S., Kopanathi S., Zhang S., Ray A., Perera R.J. Epigenetic regulation of microRNA genes and the role of miR-34b in cell invasion and motility in human melanoma. PLoS One 2011, 6:e24922.
74. Michael M.Z., SM O.C., van Holst Pellekaan N.G., Young G.P., James R.J. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol. Cancer Res. 2003, 1:882-891.
75. Nasser M.W., Datta J., Nuovo G., Kutay H., Motiwala T., Majumder S., Wang B., Suster S., Jacob S.T., Ghoshal K. Down-regulation of micro-RNA-1 (miR-1) in lung cancer. Suppression of tumorigenic property of lung cancer cells and their sensitization to doxorubicin-induced apoptosis by miR-1. J. Biol. Chem. 2008, 283:33394-33405.
76. Neves R., Scheel C., Weinhold S., Honisch E., Iwaniuk K.M., Trompeter H.I., Niederacher D., Wernet P., Santourlidis S., Uhrberg M. Role of DNA methylation in miR-200c/141 cluster silencing in invasive breast cancer cells. BMC Res. Notes 2010, 3:219.
77. Ng E.K., Tsang W.P., Ng S.S., Jin H.C., Yu J., Li J.J., Rocken C., Ebert M.P., Kwok T.T., Sung J.J. MicroRNA-143 targets DNA methyltransferases 3A in colorectal cancer. Br. J. Cancer 2009, 101:699-706.
78. Omura N., Li C.P., Li A., Hong S.M., Walter K., Jimeno A., Hidalgo M., Goggins M. Genome-wide profiling of methylated promoters in pancreatic adenocarcinoma. Cancer Biol. Ther. 2008, 7:1146-1156.
79. Ozsolak F., Poling L.L., Wang Z., Liu H., Liu X.S., Roeder R.G., Zhang X., Song J.S., Fisher D.E. Chromatin structure analyses identify miRNA promoters. Genes Dev. 2008, 22:3172-3183.
80. Park S.M., Gaur A.B., Lengyel E., Peter M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 2008, 22:894-907.
81. Popovic R., Riesbeck L.E., Velu C.S., Chaubey A., Zhang J., Achille N.J., Erfurth F.E., Eaton K., Lu J., Grimes H.L., Chen J., Rowley J.D., Zeleznik-Le N.J. Regulation of mir-196b by MLL and its overexpression by MLL fusions contributes to immortalization. Blood 2009, 113:3314-3322.
82. Rao P.K., Missiaglia E., Shields L., Hyde G., Yuan B., Shepherd C.J., Shipley J., Lodish H.F. Distinct roles for miR-1 and miR-133a in the proliferation and differentiation of rhabdomyosarcoma cells. FASEB J. 2010, 24:3427-3437.
83. Reid J.F., Sokolova V., Zoni E., Lampis A., Pizzamiglio S., Bertan C., Zanutto S., Perrone F., Camerini T., Gallino G., Verderio P., Leo E., Pilotti S., Gariboldi M., Pierotti M.A. miRNA profiling in colorectal cancer highlights miR-1 involvement in MET-dependent proliferation. Mol. Cancer Res. 2012, 10:504-515.
84. Rodriguez-Otero P., Roman-Gomez J., Vilas-Zornoza A., Jose-Eneriz E.S., Martin-Palanco V., Rifon J., Torres A., Calasanz M.J., Agirre X., Prosper F. Deregulation of FGFR1 and CDK6 oncogenic pathways in acute lymphoblastic leukaemia harbouring epigenetic modifications of the MIR9 family. Br. J. Haematol. 2011, 155:73-83.
85. Roman-Gomez J., Agirre X., Jimenez-Velasco A., Arqueros V., Vilas-Zornoza A., Rodriguez-Otero P., Martin-Subero I., Garate L., Cordeu L., San Jose-Eneriz E., Martin V., Castillejo J.A., Bandres E., Calasanz M.J., Siebert R., Heiniger A., Torres A., Prosper F. Epigenetic regulation of microRNAs in acute lymphoblastic leukemia. J. Clin. Oncol. 2009, 27:1316-1322.
86. Rotkrua P., Akiyama Y., Hashimoto Y., Otsubo T., Yuasa Y. MiR-9 downregulates CDX2 expression in gastric cancer cells. Int. J. Cancer 2011, 129:2611-2620.
87. Sachdeva M., Mo Y.Y. MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1. Cancer Res. 2010, 70:378-387.
88. Saito Y., Liang G., Egger G., Friedman J.M., Chuang J.C., Coetzee G.A., Jones P.A. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 2006, 9:435-443.
89. Saito Y., Suzuki H., Tsugawa H., Nakagawa I., Matsuzaki J., Kanai Y., Hibi T. Chromatin remodeling at Alu repeats by epigenetic treatment activates silenced microRNA-512-5p with downregulation of Mcl-1 in human gastric cancer cells. Oncogene 2009, 28:2738-2744.
90. 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. 2010, 394:1047-1052.
91. Shi B., Sepp-Lorenzino L., Prisco M., Linsley P., deAngelis T., Baserga R. Micro RNA 145 targets the insulin receptor substrate-1 and inhibits the growth of colon cancer cells. J. Biol. Chem. 2007, 282:32582-32590.
92. Smrt R.D., Szulwach K.E., Pfeiffer R.L., Li X., Guo W., Pathania M., Teng Z.Q., Luo Y., Peng J., Bordey A., Jin P., Zhao X. MicroRNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1. Stem Cells 2010, 28:1060-1070.
93. Suh S.O., Chen Y., Zaman M.S., Hirata H., Yamamura S., Shahryari V., Liu J., Tabatabai Z.L., Kakar S., Deng G., Tanaka Y., Dahiya R. MicroRNA-145 is regulated by DNA methylation and p53 gene mutation in prostate cancer. Carcinogenesis 2011, 32:772-778.
94. Suzuki H., Takatsuka S., Akashi H., Yamamoto E., Nojima M., Maruyama R., Kai M., Yamano H.O., Sasaki Y., Tokino T., Shinomura Y., Imai K., Toyota M. Genome-wide profiling of chromatin signatures reveals epigenetic regulation of MicroRNA genes in colorectal cancer. Cancer Res. 2011, 71:5646-5658.
95. Suzuki H., Tokino T., Shinomura Y., Imai K., Toyota M. DNA methylation and cancer pathways in gastrointestinal tumors. Pharmacogenomics 2008, 9:1917-1928.
96. Suzuki H., Yamamoto E., Nojima M., Kai M., Yamano H.O., Yoshikawa K., Kimura T., Kudo T., Harada E., Sugai T., Takamaru H., Niinuma T., Maruyama R., Yamamoto H., Tokino T., Imai K., Toyota M., Shinomura Y. Methylation-associated silencing of microRNA-34b/c in gastric cancer and its involvement in an epigenetic field defect. Carcinogenesis 2010, 31:2066-2073.
97. Szulwach K.E., Li X., Smrt R.D., Li Y., Luo Y., Lin L., Santistevan N.J., Li W., Zhao X., Jin P. Cross talk between microRNA and epigenetic regulation in adult neurogenesis. J. Cell Biol. 2010, 189:127-141.
98. Tellez C.S., Juri D.E., Do K., Bernauer A.M., Thomas C.L., Damiani L.A., Tessema M., Leng S., Belinsky S.A. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res. 2011, 71:3087-3097.
99. Ting A.H., Suzuki H., Cope L., Schuebel K.E., Lee B.H., Toyota M., Imai K., Shinomura Y., Tokino T., Baylin S.B. A requirement for DICER to maintain full promoter CpG island hypermethylation in human cancer cells. Cancer Res. 2008, 68:2570-2575.
100. Toyota M., Suzuki H., Sasaki Y., Maruyama R., Imai K., Shinomura Y., Tokino T. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res. 2008, 68:4123-4132.
101. Tsai K.W., Hu L.Y., Wu C.W., Li S.C., Lai C.H., Kao H.W., Fang W.L., Lin W.C. Epigenetic regulation of miR-196b expression in gastric cancer. Genes Chromosomes Cancer 2010, 49:969-980.
102. Tsai K.W., Liao Y.L., Wu C.W., Hu L.Y., Li S.C., Chan W.C., Ho M.R., Lai C.H., Kao H.W., Fang W.L., Huang K.H., Lin W.C. Aberrant hypermethylation of miR-9 genes in gastric cancer. Epigenetics 2011, 6:1189-1197.
103. Tsai K.W., Wu C.W., Hu L.Y., Li S.C., Liao Y.L., Lai C.H., Kao H.W., Fang W.L., Huang K.H., Chan W.C., Lin W.C. Epigenetic regulation of miR-34b and miR-129 expression in gastric cancer. Int. J. Cancer 2011, 129:2600-2610.
104. Tsukamoto Y., Nakada C., Noguchi T., Tanigawa M., Nguyen L.T., Uchida T., Hijiya N., Matsuura K., Fujioka T., Seto M., Moriyama M. MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res. 2010, 70:2339-2349.
105. Tsuruta T., Kozaki K., Uesugi A., Furuta M., Hirasawa A., Imoto I., Susumu N., Aoki D., Inazawa J. miR-152 is a tumor suppressor microRNA that is silenced by DNA hypermethylation in endometrial cancer. Cancer Res. 2011, 71:6450-6462.
106. Uesugi A., Kozaki K., Tsuruta T., Furuta M., Morita K., Imoto I., Omura K., Inazawa J. The tumor suppressive microRNA miR-218 targets the mTOR component Rictor and inhibits AKT phosphorylation in oral cancer. Cancer Res. 2011, 71:5765-5778.
107. Vogt M., Munding J., Gruner M., Liffers S.T., Verdoodt B., Hauk J., Steinstraesser L., Tannapfel A., Hermeking H. Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch. 2011, 458:313-322.
108. Vrba L., Jensen T.J., Garbe J.C., Heimark R.L., Cress A.E., Dickinson S., Stampfer M.R., Futscher B.W. Role for DNA methylation in the regulation of miR-200c and miR-141 expression in normal and cancer cells. PLoS One 2010, 5:e8697.
109. Wang H., Wu J., Meng X., Ying X., Zuo Y., Liu R., Pan Z., Kang T., Huang W. MicroRNA-342 inhibits colorectal cancer cell proliferation and invasion by directly targeting DNA methyltransferase 1. Carcinogenesis 2011, 32:1033-1042.
110. Wang Z., Chen Z., Gao Y., Li N., Li B., Tan F., Tan X., Lu N., Sun Y., Sun J., Sun N., He J. DNA hypermethylation of microRNA-34b/c has prognostic value for stage non-small cell lung cancer. Cancer Biol. Ther. 2011, 11:490-496.
111. Watanabe K., Emoto N., Hamano E., Sunohara M., Kawakami M., Kage H., Kitano K., Nakajima J., Goto A., Fukayama M., Nagase T., Yatomi Y., Ohishi N., Takai D. Genome structure-based screening identified epigenetically silenced microRNA associated with invasiveness in non-small-cell lung cancer. Int. J. Cancer 2012, 130:2580-2590.
112. Wiggins J.F., Ruffino L., Kelnar K., Omotola M., Patrawala L., Brown D., Bader A.G. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res. 2010, 70:5923-5930.
113. Wiklund E.D., Bramsen J.B., Hulf T., Dyrskjot L., Ramanathan R., Hansen T.B., Villadsen S.B., Gao S., Ostenfeld M.S., Borre M., Peter M.E., Orntoft T.F., Kjems J., Clark S.J. Coordinated epigenetic repression of the miR-200 family and miR-205 in invasive bladder cancer. Int. J. Cancer 2011, 128:1327-1334.
114. Wilting S.M., van Boerdonk R.A., Henken F.E., Meijer C.J., Diosdado B., Meijer G.A., le Sage C., Agami R., Snijders P.J., Steenbergen R.D. Methylation-mediated silencing and tumour suppressive function of hsa-miR-124 in cervical cancer. Mol. Cancer 2010, 9:167.
115. Wong K.Y., Liang R., So C.C., Jin D.Y., Costello J.F., Chim C.S. Epigenetic silencing of MIR203 in multiple myeloma. Br. J. Haematol. 2011, 154:569-578.
116. Wong K.Y., So C.C., Loong F., Chung L.P., Lam W.W., Liang R., Li G.K., Jin D.Y., Chim C.S. Epigenetic inactivation of the miR-124-1 in haematological malignancies. PLoS One 2011, 6:e19027.
117. Yan H., Choi A.J., Lee B.H., Ting A.H. Identification and functional analysis of epigenetically silenced microRNAs in colorectal cancer cells. PLoS One 2011, 6:e20628.
118. Yu F., Jiao Y., Zhu Y., Wang Y., Zhu J., Cui X., Liu Y., He Y., Park E.Y., Zhang H., Lv X., Ma K., Su F., Park J.H., Song E. MicroRNA 34c gene down-regulation via DNA methylation promotes self-renewal and epithelial-mesenchymal transition in breast tumor-initiating cells. J. Biol. Chem. 2012, 287:465-473.
119. Zaman M.S., Chen Y., Deng G., Shahryari V., Suh S.O., Saini S., Majid S., Liu J., Khatri G., Tanaka Y., Dahiya R. The functional significance of microRNA-145 in prostate cancer. Br. J. Cancer 2010, 103:256-264.
120. Zhang Y., Yan L.X., Wu Q.N., Du Z.M., Chen J., Liao D.Z., Huang M.Y., Hou J.H., Wu Q.L., Zeng M.S., Huang W.L., Zeng Y.X., Shao J.Y. miR-125b is methylated and functions as a tumor suppressor by regulating the ETS1 proto-oncogene in human invasive breast cancer. Cancer Res. 2011, 71:3552-3562.
121. Zhang Z., Tang H., Wang Z., Zhang B., Liu W., Lu H., Xiao L., Liu X., Wang R., Li X., Wu M., Li G. MiR-185 targets the DNA methyltransferases 1 and regulates global DNA methylation in human glioma. Mol. Cancer 2011, 10:124.