DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer

Oncogene

Volumn 31, Issue 13, 2012, Pages 1609-1622

  Lopez Serra, P ^a   Esteller, M ^a,b,c  

^a HOSPITAL DURAN I REYNALS   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

DNA methylation; microRNAs; tumor suppressor genes

Indexed keywords

CLAUDIN; CYCLIN DEPENDENT KINASE 6; EXPORTIN 5; HERMES ANTIGEN; I KAPPA B KINASE BETA; K RAS PROTEIN; KRUPPEL LIKE FACTOR 4; MICRORNA; MYC PROTEIN; NOTCH1 RECEPTOR; NOTCH4 RECEPTOR; OCTAMER TRANSCRIPTION FACTOR; PROTEIN BCL 2; PROTEIN BCL 6; PROTEIN P53; SIRTUIN 1; TRANSCRIPTION FACTOR E2F6; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR SOX4; UVOMORULIN;

ANGIOGENESIS; BLADDER CANCER; BREAST CANCER; CANCER GROWTH; CANCER INVASION; CELL COMMUNICATION; CELL CYCLE REGULATION; CELL DEDIFFERENTIATION; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CHROMOSOMAL INSTABILITY; COLON CANCER; COLORECTAL CANCER; DNA METHYLATION; DOWN REGULATION; ENDOMETRIUM CANCER; EPITHELIAL MESENCHYMAL TRANSITION; EXOSOME; GENE EXPRESSION; GENE LOCUS; GENE SILENCING; GENE TARGETING; GENOMIC INSTABILITY; GLIOBLASTOMA; HEAD AND NECK CANCER; HEMATOLOGIC MALIGNANCY; HUMAN; KIDNEY CANCER; LIVER CANCER; LIVER CELL CARCINOMA; LUNG CANCER; MELANOMA; MOUTH CANCER; NEOPLASM; OPEN READING FRAME; OVARY CANCER; PANCREAS CANCER; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; REVIEW; RNA PROCESSING; RNA SEQUENCE; RNA TRANSCRIPTION; RNA TRANSLATION; RNA TRANSPORT; SIGNAL TRANSDUCTION; STOMACH CANCER; TESTIS CANCER; TRANSCRIPTION INITIATION; TUMOR SUPPRESSOR GENE; UNTRANSLATED REGION; UTERINE CERVIX CANCER;

CELL LINE, TUMOR; DNA METHYLATION; GENE SILENCING; GENES, TUMOR SUPPRESSOR; HUMANS; MICRORNAS; NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 84860408968     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.354     Document Type: Review

References (151)

1. Agirre X, Vilas-Zornoza A, Jiménez-Velasco A, Martin-Subero JI, Cordeu L, Gárate L et al. (2009). 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: 4443-4453.
2. Akao Y, Nakagawa Y, Naoe T. (2006). Let-7 microRNA functions as a potential growth suppressor in human colon cancer cells. Biol Pharm Bull 29: 903-906.
3. Ando T, Yoshida T, Enomoto S, Asada K, Tatematsu M, Ichinose M et al. (2009). 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 124: 2367-2374.
4. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF et al. (2011). Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 108: 5003-5008.
5. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J. (2007). Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318: 798-801. (Pubitemid 351411771)
6. Bahubeshi A, Bal N, Frio TR, Hamel N, Pouchet C, Yilmaz A et al. (2010). Germline DICER1 mutations and familial cystic nephroma. J Med Genet 47: 863-866.
7. Balaguer F, Link A, Lozano JJ, Cuatrecasas M, Nagasaka T, Boland CR et al. (2010). Epigenetic silencing of miR-137 is an early event in colorectal carcinogenesis. Cancer Res 70: 6609-6618.
8. Bandres E, Agirre X, Bitarte N, Ramirez N, Zarate R, Roman-Gomez J et al. (2009). Epigenetic regulation of microRNA expression in colorectal cancer. Int J Cancer 125: 2737-2743.
9. Bass BL. (2002). RNA editing by adenosine deaminases that act on RNA. Annu Rev Biochem 71: 817-846.
10. Berdasco M, Esteller M. (2010). Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Dev Cell 19: 698-711.
11. Bin Hafeez B, Adhami VM, Asim M, Siddiqui IA, Bhat KM, Zhong W et al. (2009). Targeted knockdown of Notch1 inhibits invasion of human prostate cancer cells concomitant with inhibition of matrix metalloproteinase-9 and urokinase plasminogen activator. Clin Cancer Res 15: 452-459.
12. Birney E, Stamatoyannopoulos JA, Dutta A, Guigó R, Gingeras TR, Margulies EH et al. (2007). Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816. (Pubitemid 46920138)
13. Boon K, Caron HN, van Asperen R, Valentijn L, Hermus MC, van Sluis P et al. (2001). N-myc enhances the expression of a large set of genes functioning in ribosome and protein synthesis. EMBO J 20: 1383-1393. (Pubitemid 32233978)
14. Borchert GM, Gilmore BL, Spengler RM, Xing Y, Lanier W, Bhattacharya D et al. (2009). Adenosine deamination in human transcripts generates novel microRNA binding sites. Hum Mol Genet 18: 4801-4807.
15. Borchert GM, Lanier W, Davidson BL. (2006). RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 13: 1097-1101. (Pubitemid 44885920)
16. Bueno MJ, Pérez de Castro I, Gómez de Cedrón M, Santos J, Calin GA, Cigudosa JC et al. (2008). Genetic and epigenetic silencing of microRNA-203 enhances ABL1 and BCR-ABL1 oncogene expression. Cancer Cell 13: 496-506.
17. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S et al. (2008). A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 9: 582-589. (Pubitemid 351772923)
18. Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H, Sanders-Bush E et al. (1997). Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387: 303-308. (Pubitemid 27220768)
19. Calin GA, Cimmino A, Fabbri M, Ferracin M, Wojcik SE, Shimizu M et al. (2008). miR-15a and miR-16-1 cluster functions in human leukemia. Proc Natl Acad Sci USA 105: 5166-5171. (Pubitemid 351738528)
20. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E et al. (2002). Frequent deletions and downregulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 99: 15524-15529. (Pubitemid 35403967)
21. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE et al. (2005). A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 353: 1793-1801. (Pubitemid 41549891)
22. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S et al. (2004). Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 101: 2999-3004. (Pubitemid 38327724)
23. Ceppi P, Mudduluru G, Kumarswamy R, Rapa I, Scagliotti GV, Papotti M et al. (2010). Loss of miR-200c expression induces an aggressive, invasive, and chemoresistant phenotype in non-small cell lung cancer. Mol Cancer Res 8: 1207-1216.
24. Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, West KM et al. (2008). Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet 40: 43-50.
25. Chen R, Alvero AB, Silasi DA, Kelly MG, Fest S, Visintin I et al. (2008). Regulation of IKKb by miR-199a affects NF-kB activity in ovarian cancer cells. Oncogene 27: 4712-4723.
26. Chen R, Alvero AB, Silasi DA, Mor G. (2007). Inflammation, cancer and chemoresistance: taking advantage of the Toll-like receptor signaling pathway. Am J Reprod Immunol 57: 93-107. (Pubitemid 46099804)
27. Chen J, Wang L, Matyunina LV, Hill CG, McDonald JF. (2011). Overexpression of miR-429 induces mesenchymal-to-epithelial transition (MET) in metastatic ovarian cancer cells. Gynecol Oncol 121: 200-205.
28. Cheung HH, Davis AJ, Lee TL, Pang AL, Nagrani S, Rennert OM et al. (2011). Methylation of an intronic region regulates miR-199a in testicular tumor malignancy. Oncogene 30: 3404-3415.
29. Chim CS, Wong KY, Qi Y, Loong F, Lam WL, Wong LG et al. (2010). Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 31: 745-750.
30. Corney DC, Hwang CI, Matoso A, Vogt M, Flesken-Nikitin A, Godwin AK et al. (2010). Frequent downregulation of miR-34 family in human ovarian cancers. Clin Cancer Res 16: 1119-1128.
31. Dangi-Garimella S, Strouch MJ, Grippo PJ, Bentrem DJ, Munshi HG. (2011). Collagen regulation of let-7 in pancreatic cancer involves TGF-b1-mediated membrane type 1-matrix metalloproteinase expression. Oncogene 30: 1002-1008.
32. Das H, Koizumi T, Sugimoto T, Chakraborty S, Ichimura T, Hasegawa K et al. (2000). Quantitation of Fas and Fas ligand gene expression in human ovarian, cervical and endometrial carcinomas using real-time quantitative RT-PCR. Br J Cancer 82: 1682-1688. (Pubitemid 30229579)
33. Datta J, Kutay H, Nasser MW, Nuovo GJ, Wang B, Majumder S et al. (2008). Methylation mediated silencing of microRNA-1 gene and its role in hepatocellular carcinogenesis. Cancer Res 68: 5049-5058.
34. Davalos V, Moutinho C, Villanueva A, Boque R, Silva P, Carneiro F et al. (2011). Dynamic epigenetic regulation of the microRNA-200 family mediates epithelial and mesenchymal transitions in human tumorigenesis. Oncogene (e-pub ahead of print 2 August 2011; doi:10.1038/onc.2011.383).
35. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E et al. (2006). Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 38: 1060-1065. (Pubitemid 44325933)
36. Eiring AM, Harb JG, Neviani P, Garton C, Oaks JJ, Spizzo R et al. (2010). miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell 140: 652-665.
37. Elbashir SM, Lendeckel W, Tuschl T. (2001). RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15: 188-200. (Pubitemid 32107664)
38. Esteller M. (2008). Epigenetics in cancer. N Engl J Med 358: 1148-1159.
39. Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E et al. (2007). MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci USA 104: 15805-15810. (Pubitemid 350035380)
40. Feinberg AP, Vogelstein B. (1983). Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 301: 89-92. (Pubitemid 13154475)
41. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. (1998). Potent and specific interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811. (Pubitemid 28099681)
42. Friedman RC, Farh KK, Burge CB, Bartel DP. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
43. Furuta M, Kozaki KI, Tanaka S, Arii S, Imoto I, Inazawa J. (2010). miR-124 and miR-203 are epigenetically silenced tumor-suppressive microRNAs in hepatocellular carcinoma. Carcinogenesis 31: 766-776.
44. Gallardo E, Navarro A, Viñolas N, Marrades RM, Diaz T, Gel B et al. (2009). miR-34a as a prognostic marker of relapse in surgically resected non-small-cell lung cancer. Carcinogenesis 30: 1903-1909.
45. Gao XN, Lin J, Li YH, Gao L, Wang XR, Wang W et al. (2011). MicroRNA-193a represses c-kit expression and functions as a methylation-silenced tumor suppressor in acute myeloid leukemia. Oncogene 30: 3416-3428.
46. Grady WM, Parkin RK, Mitchell PS, Lee JH, Kim YH, Tsuchiya KD et al. (2008). Epigenetic silencing of the intronic microRNA has-miR.342 and its host gene EVL in colorectal cancer. Oncogene 27: 3880-3888. (Pubitemid 351862055)
47. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N et al. (2004). The Microprocessor complex mediates the genesis of microRNAs. Nature 432: 235-240. (Pubitemid 39545855)
48. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. (2007). MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105. (Pubitemid 46991392)
49. Grossel MJ, Hinds PW. (2006). Beyond the cell cycle: a new role for Cdk6 in differentiation. J Cell Biochem 97: 485-493. (Pubitemid 43265308)
50. Han J, Lee Y, Yeom KH, Nam JW, Heo I, Rhee JK et al. (2006). Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125: 887-901. (Pubitemid 43810154)
51. Hashimoto Y, Akiyama Y, Otsubo T, Shimada S, Yuasa Y. (2010). Involvement of epigenetically silenced microRNA-181c in gastric carcinogenesis. Carcinogenesis 31: 777-784.
52. Heinzelmann J, Henning B, Sanjmyatav J, Posorski N, Steiner T, Wunderlich H et al. (2011). Specific miRNA signatures are associated with metastasis and poor prognosis in clear cell renal cell carcinoma. World J Urol 29: 367-373.
53. Hildebrandt MA, Gu J, Lin J, Ye Y, Tan W, Tamboli P et al. (2010). Hsa-miR-9 methylation status is associated with cancer development and metastatic recurrence in patients with clear cell renal cell carcinoma. Oncogene 29: 5724-5728.
54. Hong L, Lai M, Chen M, Xie C, Liao R, Kang YJ et al. (2010). The miR-17-92 cluster of microRNAs confers tumorigenicity by inhibiting oncogene-induced senescence. Cancer Res 70: 8547-8557.
55. Hu Z, Chen J, Tian T, Zhou X, Gu H, Xu L et al. (2008). Genetic variants of miRNA sequences and non-small cell lung cancer survival. J Clin Invest 118: 2600-2608. (Pubitemid 351949787)
56. Huang J, Wang Y, Guo Y, Sun S. (2010). Downregulated microRNA-152 induces aberrant DNA methylation in hepatitis B virus-related hepatocellular carcinoma by targeting DNA methyltransferase 1. Hepatology 52: 60-70.
57. Huang YW, Liu JC, Deatherage DE, Luo J, Mutch DG, Goodfellow PJ et al. (2009). Epigenetic repression of microRNA-129-2 leads to overexpression of SOX4 oncogene in endometrial cancer. Cancer Res 69: 9038-9046.
58. Hurteau GJ, Spivack SD, Brock GJ. (2006). Potential mRNA degradation targets of hsa-miR-200c, identified using informatics and qRT-PCR. Cell Cycle 5: 1951-1956. (Pubitemid 44435301)
59. Hutvágner G, McLachlan J, Pasquinelli AE, Bálint E, Tuschl T, Zamore PD. (2001). A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293: 834-838. (Pubitemid 32743968)
60. Hutvágner G, Zamore PD. (2002). RNAi: nature abhors a double-strand. Curr Opin Genet Dev 12: 225-232. (Pubitemid 34219496)
61. Iizasa H, Wulff BE, Alla NR, Maragkakis M, Megraw M, Hatzigeorgiou A et al. (2010). Editing of Epstein-Barr-virus-encoded BART6 microRNAs controls their dicer targeting and consequently affects viral latency. J Biol Chem 285: 33358-33370.
62. Jing Q, Huang S, Guth S, Zarubin T, Motoyama A, Chen J et al. (2005). Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 120: 623-634. (Pubitemid 40343075)
63. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A et al. (2005). RAS is regulated by the let-7 microRNA family. Cell 120: 635-647. (Pubitemid 40343076)
64. Jones PA, Baylin SB. (2007). The epigenomics of cancer. Cell 128: 683-692. (Pubitemid 46273572)
65. Kalimutho M, Di Cecilia S, Del Vecchio Blanco G, Roviello F, Sileri P, Cretella M et al. (2011). Epigenetically silenced miR-34b/c as a novel faecal-based screening marker for colorectal cancer. Br J Cancer 104: 1770-1778.
66. Kamimae S, Yamamoto E, Yamano HO, Nojima M, Suzuki H, Ashida M et al. (2011). Epigenetic alteration of DNA in mucosal wash fluid predicts invasiveness of colorectal tumors. Cancer Prev Res 4: 674-683.
67. Kindler T, Breitenbuecher F, Marx A, Beck J, Hess G, Weinkauf B et al. (2004). Efficacy and safety of imatinib in adult patients with c-kit-positive acute myeloid leukemia. Blood 103: 3644-3654. (Pubitemid 38596277)
68. Kosaka N, Iguchi H, Ochiya T. (2010). Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 101: 2087-2092.
69. Kozaki K, Imoto I, Mogi S, Omura K, Inazawa J. (2008). Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res 68: 2094-2105. (Pubitemid 351521781)
70. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ et al. (2005). Combinatorial microRNA target predictions. Nat Genet 37: 495-500. (Pubitemid 40617277)
71. Krueger A, Fas SC, Baumann S, Krammer PH. (2003). The role of CD95 in the regulation of peripheral T-cell apoptosis. Immunol Rev 193: 58-69. (Pubitemid 36688040)
72. Lai EC. (2002). MicroRNAs are complementary to 3′TR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 30: 363-364.
73. Laios A, O'Toole S, Flavin R, Martin C, Kelly L, Ring M et al. (2008). Potential role of miR-9 and miR-223 in recurrent ovarian cancer. Mol Cancer 7: 35-49.
74. Langevin SM, Stone RA, Bunker CH, Grandis JR, Sobol RW, Taioli E. (2010). 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 31: 864-870.
75. Lee JW, Choi CH, Choi JJ, Park YA, Kim SJ, Hwang SY, et al., Bae DS (2008). Altered microRNA expression in cervical carcinomas. Clin Cancer Res 14: 2535-2542.
76. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J et al. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature 425: 415-419. (Pubitemid 37187272)
77. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH et al. (2004). MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23: 4051-4060. (Pubitemid 39472426)
78. Lehmann U, Hasemeier B, Christgen M, Müller M, Römermann D, Länger F et al. (2008). Epigenetic inactivation of microRNA gene has-mir-9-1 in human breast cancer. J Pathol 214: 17-24.
79. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. (2003). Prediction of mammalian microRNA targets. Cell 115: 787-798. (Pubitemid 38058492)
80. Lim PK, Bliss SA, Patel SA, Taborga M, Dave MA, Gregory LA et al. (2011). Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res 71: 1550-1560.
81. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ et al. (2004). Argonaute2 is the catalytic engine of mammalian RNAi. Science 305: 1437-1441. (Pubitemid 39167657)
82. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Körner H et al. (2008). Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 7: 2591-2600.
83. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D et al. (2005). MicroRNA expression profiles classify human cancers. Nature 435: 834-838. (Pubitemid 40839735)
84. Lu L, Katsaros D, de la Longrais IA, Sochirca O, Yu H. (2007). Hypermethylation of let-7a-3 in epithelial ovarian cancer is associated with low insulin-like growth factor-II expression and favorable prognosis. Cancer Res 67: 10117-10122. (Pubitemid 350070782)
85. Lujambio A, Portela A, Liz J, Melo SA, Rossi S, Spizzo R et al. (2010). CpG island hypermethylation-associated silencing of non-coding RNAs transcribed from ultraconserved regions in human cancer. Oncogene 29: 6390-6401.
86. Lujambio A, Esteller M. (2009). How epigenetics can explain human metastasis: a new role for microRNAs. Cell Cycle 8: 377-382.
87. Lujambio A, Calin GA, Villanueva A, Ropero S, Sánchez- Céspedes M, Blanco D et al. (2008). A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci USA 105: 13556-13561.
88. Lujambio A, Ropero S, Ballestar E, Fraga MF, Cerrato C, Setién F et al. (2007). Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res 67: 1424-1429. (Pubitemid 46383366)
89. Martello G, Rosato A, Ferrari F, Manfrin A, Cordenonsi M, Dupont S et al. (2010). A microRNA targeting Dicer for metastasis control. Cell 141: 1195-1207.
90. Mears R, Craven RA, Hanrahan S, Totty N, Upton C, Young SL et al. (2004). Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics 4: 4019-4031. (Pubitemid 39657475)
91. Medina PP, Nolde M, Slack FJ. (2010). OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature 467: 86-89.
92. Melo SA, Moutinho C, Ropero S, Calin GA, Rossi S, Spizzo R et al. (2010). A genetic defect in exportin-5 traps precursor microRNA in the nucleus of cancer cells. Cancer Cell 18: 303-315.
93. Melo SA, Ropero S, Moutinho C, Aaltonen LA, Yamamoto H, Calin GA et al. (2009). A TARBP2 mutation in human cancer impairs microRNA processing and DICER1 function. Nat Genet 41: 365-370.
94. Melo S, Villanueva A, Moutinho C, Davalos V, Spizzo R, Ivan C et al. (2011). Small molecule enoxacin is a cancer-specific growth inhibitor that acts by enhancing TAR RNA-binding protein 22-mediated microRNA processing. Proc Natl Acad Sci USA 108: 4394-4399.
95. Merritt WM, Lin YG, Han LY, Kamat AA, Spannuth WA, Schmandt R et al. (2008). Dicer, Drosha and outcomes in patients with ovarian cancer. N Engl J Med 359: 2641-2650.
96. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL et al. (2008). Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105: 10513-10518.
97. Neves R, Scheel C, Weinhold S, Honisch E, Iwaniuk KM, Trompeter HI et al. (2010). Role of DNA methylation in miR-200c/141 cluster silencing in invasive breast cancer cells. BMC Res Notes 3: 219.
98. Obad S, Dos Santos CO, Petri A, Heidenblad M, Broom O, Ruse C et al. (2011). Silencing of microRNA families by seed-targeting tiny LNAs. Nat Genet 43: 371-378.
99. Olive V, Bennett MJ, Walker JC, Ma C, Jiang I, Cordon-Cardo C et al. (2009). miR-19 is a key oncogenic component of mir-17-92. Genes Dev 23: 2839-2849.
100. Omura N, Li CP, Li A, Hong SM, Walter K, Jimeno A et al. (2008). Genome-wide profiling of methylated promoters in pancreatic adenocarcinoma. Cancer Biol Ther 7: 1146-1156.
101. Ottaviano AJ, Sun L, Ananthanarayanan V, Munshi HG. (2006). Extracellular matrix-mediated membrane-type 1 matrix metalloproteinase expression in pancreatic ductal cells is regulated by transforming growth facor-beta1. Cancer Res 66: 7032-7040. (Pubitemid 44197679)
102. Ørom UA, Nielsen FC, Lund AH. (2008). MicroRNA-10a binds the 5′TR of ribosomal protein mRNAs and enhances their translation. Mol Cell 30: 460-471. (Pubitemid 351672378)
103. Pagano JS. (2002). Viruses and lymphomas. N Engl J Med 347: 79-79.
104. Pang RT, Leung CO, Ye TM, Liu W, Chiu PC, Lam KK et al. (2010). MicroRNA-34a suppresses invasion through downregulation of Notch1 and Jagged in cervical carcinoma and choriocarcinoma cells. Carcinogenesis 31: 1037-1044.
105. Park SM, Gaur AB, Lengyel E, Peter ME. (2008). The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22: 894-907. (Pubitemid 351482843)
106. Paroo Z, Ye X, Chen S, Liu Q. (2009). Phosphorylation of the human microRNA-generating complex mediates MAPK/Erk signaling. Cell 139: 112-122.
107. Peinado H, Olmeda D, Cano A. (2007). Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7: 415-428. (Pubitemid 46809165)
108. Pfeffer S, Zavolan M, Grässer FA, Chien M, Russo JJ, Ju J et al. (2004). Identification of virus-encoded microRNAs. Science 304: 734-736. (Pubitemid 38560879)
109. Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E et al. (2005). Inhibition of translational initiation by Let-7 microRNA in human cells. Science 309: 1573-1576. (Pubitemid 41266485)
110. Plasterk RH. (2002). RNA silencing: the genome's immune system. Science 296: 1263-1265.
111. Png KJ, Yoshida M, Zhang XH, Shu W, Lee H, Rimner A et al. (2011). MicroRNA-335 inhibits tumor reinitiation and is silenced through genetic and epigenetic mechanisms in human breast cancer. Genes Dev 25: 226-231.
112. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP. (2010). A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465: 1033-1038.
113. Ponjavic J, Ponting CP, Lunter G. (2007). Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res 17: 556-565. (Pubitemid 46715505)
114. Rio Frio T, Bahubeshi A, Kanellopoulou C, Hamel N, Niedziela M, Sabbaghian N et al. (2011). DICER1 mutations in familial multinodular goiter with and without ovarian Sertoli-Leydig cell tumors. JAMA 305: 68-77.
115. Rodríguez-Paredes M, Esteller M. (2011). Cancer epigenetics reaches mainstream oncology. Nat Med 17: 330-339.
116. Roman-Gomez J, Agirre X, Jiménez-Velasco A, Arqueros V, Vilas-Zornoza A, Rodriguez-Otero P et al. (2009). Epigenetic regulation of microRNAs in acute lymphoblastic leukemia. J Clin Oncol 27: 1316-1322.
117. Rosenfeld N, Aharonov R, Meiri E, Rosenwald S, Spector Y, Zepeniuk M et al. (2008). MicroRNAs accurately identify cancer tissue origin. Nat Biotechnol 26: 462-469. (Pubitemid 351501813)
118. Ruggero D, Pandolfi PP. (2003). Does the ribosome translate cancer? Nat Rev Cancer 3: 179-192. (Pubitemid 37328870)
119. Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA et al. (2006). Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 9: 435-443. (Pubitemid 43832188)
120. Sandoval J, Heyn HA, Moran S, Serra-Musach J, Pujana MA, Bibikova M et al. (2011). Validation of a DNA methylation microarray for 450 000 CpG sites in the human genome. Epigenetics 6: 692-702.
121. Shaw G, Kamen R. (1986). A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46: 659-667.
122. Shen R, Pan S, Qi S, Lin X, Cheng S. (2010). Epigenetic repression of microRNA-129-2 leads to overexpression of SOX4 in gastric cancer. Biochem Biophys Res Commun 394: 1047-1052.
123. Silber J, Lim DA, Petritsch C, Persson AI, Maunakea AK, Vandenberg SR et al. (2008). miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BCM Med 6: 14-31.
124. Suh SO, Chen Y, Zaman MS, Hirata H, Yamamura S, Shahryari V et al. (2011). MicroRNA-145 is regulated by DNA methylation and p53 gene mutation in prostate cancer. Carcinogenesis 32: 772-778.
125. Takahashi K, Yamanaka S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676. (Pubitemid 44233629)
126. Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H et al. (2004). Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer res 64: 3753-3756. (Pubitemid 38697282)
127. Tan HX, Wang Q, Chen LZ, Huang XH, Chen JS, Fu XH et al. (2010). MicroRNA-9 reduces cell invasion and E-cadherin secretion in SK-Hep-1 cell. Med Oncol 27: 645-660.
128. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A et al. (2007). 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: 1586-1593. (Pubitemid 47327945)
129. Tavazoie SF, Alarcón C, Oskarsson T, Padua D, Wang Q, Bos PD et al. (2008). Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451: 147-152.
130. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y et al. (2008). Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res 68: 4123-4132.
131. Tsai KW, Wu CW, Hu LY, Li SC, Liao YL, Lai CH et al. (2011). Epigenetic regulation of miR-34b and miR-129 expression in gastric cancer. Int J Cancer (in press).
132. Ueda T, Volinia S, Okumura H, Shimizu M, Taccioli C, Rossi S et al. (2010). Relation between microRNA expression and progression and prognosis of gastric cancer: a microRNA expression analysis. Lancet Oncol 11: 136-146.
133. Urdinguio RG, Fernandez AF, Lopez-Nieva P, Rossi S, Huertas D, Kulis M et al. (2010). Disrupted microRNA expression caused by Mecp2 loss in a mouse model of Rett syndrome. Epigenetics 5: 656-663.
134. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659. (Pubitemid 47214727)
135. Vasudevan S, Tong Y, Steitz JA. (2007). Switching from repression to activation: microRNAs can upregulate translation. Science 318: 1931-1934.
136. Vázquez I, Maicas M, Marcotegui N, Conchillo A, Guruceaga E, Roman-Gomez J et al. (2010). Silencing of hsa-miR-124 by EVI1 in cell lines and patients with acute myeloid leukemia. Proc Natl Acad Sci USA 107: 167-168.
137. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI et al. (2004). RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672-676. (Pubitemid 38141633)
138. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F et al. (2006). A microRNA expression profile signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 103: 2257-2261. (Pubitemid 43271657)
139. Vrba L, Jensen TJ, Garbe JC, Heimark RL, Cress AE, Dickinson S et al. (2010). Role for DNA methylation in the regulation of miR-200c and miR-141 expression in normal and cancer cells. PLoS One 5: e8697.
140. Wang S, Tang Y, Cui H, Zhao X, Luo X, Pan W et al. (2011). Let-7/miR-98 regulate Fas and Fas-mediated apoptosis. Genes Immun 12: 149-154.
141. Wendler A, Keller D, Albrecht C, Peluso JJ, Wehling M. (2011). Involvement of let-7/miR-98 microRNAs in the regulation of progesterone receptor membrane component 1 expression in ovarian cancer cells. Oncol Rep 25: 273-279.
142. Wiklund ED, Bramsen JB, Hulf T, Dyrskjot L, Ramanathan R, Hansen TB et al. (2010). Coordinated epigenetic repression of the miR-200 family and miR-205 in invasive bladder cancer. Int J Cancer 128: 1327-1334.
143. Willis L, Alarcón T, Elia G, Jones JL, Wright NA, Tomlinson IPM et al. (2010). Breast cancer dormancy can be maintained by small numbers of micrometastases. Cancer Res 70: 4310-4317.
144. Wilting SM, van Boerdonk RA, Henken FE, Meijer CJ, Diosdado B, Meijer GA et al. (2010). Methylation-mediated silencing and tumour suppressive function of hsa-miR-124 in cervical cancer. Mol Cancer 9: 167-181.
145. Xu N, Donohoe ME, Silva SS, Lee JT. (2007). Evidence that homologous X-chromosome pairing requires transcription and Ctcf protein. Nat Genet 39: 1390-1396. (Pubitemid 350035004)
146. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS. (2009). MicroRNA-145 regulates OCT4, SOX2 and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137: 647-658.
147. Yamakuchi M, Ferlito M, Lowenstein C. (2008). miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci USA 105: 13421-13426.
148. Yi R, Qin Y, Macara IG, Cullen BR. (2003). Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 17: 3011-3016. (Pubitemid 38040764)
149. Yin G, Chen R, Alvero AB, Fu HH, Holmberg J, Glackin C et al. (2010). TWIST Ting stemness, inflammation and proliferation of epithelial ovarian cell through MIR199A2/214. Oncogene 29: 3545-3553.
150. Yu CC, Chen YW, Chiou GY, Tsai LL, Huang PI, Chang CY et al. (2011). MicroRNA let-7a represses chemoresistance and tumourigenicity in head and neck cancer via stem-like properties ablation. Oral Oncol 47: 202-210.
151. Zhang L, Huang J, Yang N, Greshock J, Megraw MS, Glannakakis A et al. (2006). MicroRNAs exhibit high frequency genomic alterations in human cancer. Proc Natl Acad Sci USA 103: 9136-9141. (Pubitemid 43902545)