Epigenetically regulated MIR941 and MIR1247 target gastric cancer cell growth and migration

Epigenetics

Volumn 9, Issue 7, 2014, Pages 1018-1030

  Kim, Joong Gook ^a   Kim, Tae Oh ^b   Bae, Jin Han ^a   Shim, Jae Woong ^a   Kang, Myoung Joo ^b   Yang, Kwangmo ^a   Ting, Angela H ^c   Yi, Joo Mi ^a  

^a Dongnam Institute of Radiological and Medical Science   (South Korea)

^b Inje University College of Medicine   (South Korea)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

5 aza 2' deoxycytidine; DNA methylation; Epigenetics; Gastric cancer; MicroRNA; MIR1247; MIR941

Indexed keywords

MICRORNA; MICRORNA 1247; MICRORNA 941; UNCLASSIFIED DRUG; MESSENGER RNA;

ADULT; AGED; ARTICLE; BIOINFORMATICS; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DOWNREGULATION; EPIGENETICS; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MTT ASSAY; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; STOMACH CANCER; WESTERN BLOTTING; WOUND HEALING; ADENOCARCINOMA; ADENOMA; CELL MOTION; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; STOMACH TUMOR; TUMOR CELL LINE; VERY ELDERLY;

ADENOCARCINOMA; ADENOMA; ADULT; AGED; AGED, 80 AND OVER; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE SILENCING; HUMANS; MALE; MICRORNAS; MIDDLE AGED; RNA, MESSENGER; STOMACH NEOPLASMS;

EID: 84903726474     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.29007     Document Type: Article

References (52)

1. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120:15-20; PMID:15652477; http://dx.doi.org/10.1016/j.cell.2004.12.035
2. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23:4051-4060; PMID:15372072; http://dx.doi.org/10.1038/sj.emboj.7600385
3. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010; 11:597-610; PMID:20661255
4. Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y, Cheloufi S, Ma E, Mane S, Hannon GJ, Lawson ND, et al. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 2010; 328:1694-1698; PMID:20448148; http://dx.doi.org/10.1126/science.1190809
5. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116:281-297; PMID:14744438; http://dx.doi.org/10.1016/S0092-8674(04)00045-5
6. He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5:522-531; PMID: 15211354; http://dx.doi.org/10.1038/nrg1379
7. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002; 99:15524-15529; PMID:12434020; http://dx.doi.org/10.1073/pnas.242606799
8. Michael MZ, O'Connor SM, van Holst Pellekaan NG, Young GP, James RJ. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 2003; 1:882-891; PMID:14573789
9. Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, Harano T, Yatabe Y, Nagino M, Nimura Y, et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 2004; 64:3753-3756; PMID:15172979; http://dx.doi.org/10.1158/0008-5472.CAN-04-0637
10. Iorio M V, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005; 65:7065-7070; PMID:16103053; http://dx.doi.org/10.1158/0008-5472.CAN-05-1783
11. Guo J, Miao Y, Xiao B, Huan R, Jiang Z, Meng D, Wang Y. Differential expression of microRNA species in human gastric cancer versus non-tumorous tissues. J Gastroenterol Hepatol 2009; 24:652-657; PMID:19175831; http://dx.doi.org/10.1111/j.1440-1746.2008.05666.x
12. Yoon SO, Chun SM, Han EH, Choi J, Jang SJ, Koh SA, Hwang S, Yu E. Deregulated expression of microRNA-221 with the potential for prognostic biomarkers in surgically resected hepatocellular carcinoma. Hum Pathol 2011; 42:1391-1400; PMID: 21458843; http://dx.doi.org/10.1016/j.humpath.2010.12.010
13. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio M V, Visone R, Sever NI, Fabbri M, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 2005; 353:1793-1801; PMID: 16251535; http://dx.doi.org/10.1056/NEJMoa050995
14. Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA, Jones PA. 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; PMID:16766263; http://dx.doi.org/10.1016/j. ccr.2006.04.020
15. Nakamura T, Canaani E, Croce CM. Oncogenic All1 fusion proteins target Drosha-mediated microRNA processing. Proc Natl Acad Sci USA 2007; 104:10980-10985; PMID:17581865; http://dx.doi.org/10.1073/pnas.0704559104
16. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55:74-108; PMID: 15761078; http://dx.doi.org/10.3322/canjclin.55.2.74
17. Crew KD, Neugut AI. Epidemiology of gastric cancer. World J Gastroenterol 2006; 12:354-362; PMID:16489633
18. Ushijima T, Nakajima T, Maekita T. DNA methylation as a marker for the past and future. J Gastroenterol 2006; 41:401-407; PMID:16799880; http://dx.doi.org/10.1007/s00535-006-1846-6
19. Shin SH, Park SY, Kang GH. Down-regulation of dual-specificity phosphatase 5 in gastric cancer by promoter CpG island hypermethylation and its potential role in carcinogenesis. Am J Pathol 2013; 182:1275-1285; PMID:23402999; http://dx.doi.org/10.1016/j.ajpath.2013.01.004
20. Wang X, Kang GH, Campan M, Weisenberger DJ, Long TI, Cozen W, Bernstein L, Wu AH, Siegmund KD, Shibata D, et al. Epigenetic subgroups of esophageal and gastric adenocarcinoma with differential GATA5 DNA methylation associated with clinical and lifestyle factors. PLoS One 2011; 6:e25985; PMID:22028801; http://dx.doi.org/10.1371/jour-nal.pone.0025985
21. Suzuki H, Tokino T, Shinomura Y, Imai K, Toyota M. DNA methylation and cancer pathways in gastrointestinal tumors. Pharmacogenomics 2008; 9:1917-1928; PMID:19072648; http://dx.doi.org/10.2217/14622416.9.12.1917
22. Lujambio A, Ropero S, Ballestar E, Fraga MF, Cerrato C, Setién F, Casado S, Suarez-Gauthier A, Sanchez-Cespedes M, Git A, et al. Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res 2007; 67:1424-1429; PMID:17308079; http://dx.doi.org/10.1158/0008-5472.CAN-06-4218
23. 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; PMID:18519671; http://dx.doi.org/10.1158/0008-5472.CAN-08-0325
24. Yan H, Choi AJ, Lee BH, Ting AH. Identification and functional analysis of epigenetically silenced microRNAs in colorectal cancer cells. PLoS One 2011; 6:e20628; PMID:21698188; http://dx.doi.org/10.1371/journal.pone.0020628
25. Rhee I, Bachman KE, Park BH, Jair KW, Yen RW, Schuebel KE, Cui H, Feinberg A P, Lengauer C, Kinzler KW, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 2002; 416:552-556; PM ID:11932749; http://dx.doi.org/10.1038/416552a
26. Serre D, Lee BH, Ting AH. MBD-isolated Genome Sequencing provides a high-throughput and comprehensive survey of DNA methylation in the human genome. Nucleic Acids Res 2010; 38:391-399; PMID:19906696; http://dx.doi.org/10.1093/nar/gkp992
27. Shivdasani RA. MicroRNAs: regulators of gene expression and cell differentiation. Blood 2006; 108:3646-3653; PMID:16882713; http://dx.doi.org/10.1182/blood-2006-01-030015
28. Carthew RW. Gene regulation by microRNAs. Curr Opin Genet Dev 2006; 16:203-208; PMID:16503132; http://dx.doi.org/10.1016/j.gde.2006.02.012
29. Lewis BP, Shih IH, Jones-Rhoades M W, Bartel D P, Burge CB. Prediction of mammalian microRNA targets. Cell 2003; 115:787-798; PMID:14697198; http://dx.doi.org/10.1016/S0092-8674(03)01018-3
30. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, et al. MIR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 2005; 102:13944-13949; PMID:16166262; http://dx.doi.org/10.1073/pnas.0506654102
31. Lujambio A, Calin GA, Villanueva A, Ropero S, Sánchez-Céspedes M, Blanco D, Montuenga LM, Rossi S, Nicoloso MS, Faller WJ, et al. A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci USA 2008; 105:13556-13561; PMID:18768788; http://dx.doi.org/10.1073/pnas.0803055105
32. Bueno MJ, Pérez de Castro I, Gómez de Cedrón M, Santos J, Calin GA, Cigudosa JC, Croce CM, Fernández-Piqueras J, Malumbres M. Genetic and epigenetic silencing of microRNA-203 enhances ABL1 and BCR-ABL1 oncogene expression. Cancer Cell 2008; 13:496-506; PMID:18538733; http://dx.doi.org/10.1016/j.ccr.2008.04.018
33. Suzuki H, Yamamoto E, Nojima M, Kai M, Yamano HO, Yoshikawa K, Kimura T, Kudo T, Harada E, Sugai T, et al. Methylation-associated silencing of microRNA-34b/c in gastric cancer and its involvement in an epigenetic field defect. Carcinogenesis 2010; 31:2066-2073; PMID:20924086; http://dx.doi.org/10.1093/carcin/bgq203
34. Nadal E, Chen G, Gallegos M, Lin L, Ferrer-Torres D, Truini A, Wang Z, Lin J, Reddy RM, Llatjos R, et al. Epigenetic inactivation of microRNA-34b/c predicts poor disease-free survival in early-stage lung adenocarcinoma. Clin Cancer Res 2013; 19:6842-6852; PMID:24130071; http://dx.doi.org/10.1158/1078-0432.CCR-13-0736
35. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE, Zhai Y, Giordano TJ, Qin ZS, Moore BB, et al. P53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 2007; 17:1298-1307; PMID:17656095; http://dx.doi.org/10.1016/j.cub.2007.06.068
36. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435:834-838; PMID: 15944708; http://dx.doi.org/10.1038/nature03702
37. Heinzelmann J, Henning B, Sanjmyatav J, Posorski N, Steiner T, Wunderlich H, Gajda MR, Junker K. Specific miRNA signatures are associated with metastasis and poor prognosis in clear cell renal cell carcinoma. World J Urol 2011; 29:367-373; PMID:21229250; http://dx.doi.org/10.1007/s00345-010-0633-4
38. Kosaka N, Iguchi H, Ochiya T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 2010; 101:2087-2092; PMID:20624164; http://dx.doi.org/10.1111/j.1349-7006.2010.01650.x
39. Kalimutho M, Di Cecilia S, Del Vecchio Blanco G, Roviello F, Sileri P, Cretella M, Formosa A, Corso G, Marrelli D, Pallone F, et al. Epigenetically silenced miR-34b/c as a novel faecal-based screening marker for colorectal cancer. Br J Cancer 2011; 104:1770-1778; PMID:21610744; http://dx.doi.org/10.1038/bjc.2011.82
40. Kamimae S, Yamamoto E, Yamano HO, Nojima M, Suzuki H, Ashida M, Hatahira T, Sato A, Kimura T, Yoshikawa K, et al. Epigenetic alteration of DNA in mucosal wash fluid predicts invasiveness of colorectal tumors. Cancer Prev Res (Phila) 2011; 4:674-683; PMID:21543345; http://dx.doi.org/10.1158/1940-6207.CAPR-10-0214
41. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet 2011; 12:861-874; PMID:22094949; http://dx.doi.org/10.1038/nrg3074
42. Lan F, Bayliss PE, Rinn JL, Whetstine JR, Wang JK, Chen S, Iwase S, Alpatov R, Issaeva I, Canaani E, et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 2007; 449:689-694; PMID: 17851529; http://dx.doi.org/10.1038/nature06192
43. Xiang Y, Zhu Z, Han G, Lin H, Xu L, Chen CD. JMJD3 is a histone H3K27 demethylase. Cell Res 2007; 17:850-857; PMID:17923864; http://dx.doi.org/10.1038/cr.2007.83
44. Sen GL, Webster DE, Barragan DI, Chang HY, Khavari PA. Control of differentiation in a self-renewing mammalian tissue by the histone demethylase JMJD3. Genes Dev 2008; 22:1865-1870; PMID:18628393; http://dx.doi.org/10.1101/gad.1673508
45. Ramadoss S, Chen X, Wang CY. Histone demeth-ylase KDM6B promotes epithelial-mesenchymal transition. J Biol Chem 2012; 287:44508-44517; PMID:23152497; http://dx.doi.org/10.1074/jbc. M112.424903
46. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 1996; 10:940-954; PMID: 8801176
47. Kakizuka A, Miller WH Jr., Umesono K, Warrell RP Jr., Frankel SR, Murty V V, Dmitrovsky E, Evans RM. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RAR alpha with a novel putative transcription factor, PML. Cell 1991; 66:663-674; PMID:1652368; http://dx.doi.org/10.1016/0092-8674(91)90112-C
48. He LZ, Guidez F, Tribioli C, Peruzzi D, Ruthardt M, Zelent A, Pandolfi PP. Distinct interactions of PML-RARalpha and PLZF-RARalpha with co-repressors determine differential responses to RA in APL. Nat Genet 1998; 18:126-135; PMID:9462740; http://dx.doi.org/10.1038/ng0298-126
49. Pandolfi PP. Oncogenes and tumor suppressors in the molecular pathogenesis of acute promyelocytic leukemia. Hum Mol Genet 2001; 10:769-775; PMID:11257111; http://dx.doi.org/10.1093/hmg/10.7.769
50. Brown NJ, Ramalho M, Pedersen EW, Moravcsik E, Solomon E, Grimwade D. PML nuclear bodies in the pathogenesis of acute promyelocytic leukemia: active players or innocent bystanders? Front Biosci (Landmark Ed) 2009; 14:1684-1707; PMID:19273155; http://dx.doi.org/10.2741/3333
51. Zhu J, Gianni M, Kopf E, Honoré N, Chelbi-Alix M, Koken M, Quignon F, Rochette-Egly C, de Thé H. Retinoic acid induces proteasome-dependent degradation of retinoic acid receptor alpha (RARalpha) and oncogenic RARalpha fusion proteins. Proc Natl Acad Sci USA 1999; 96:14807-14812; PMID:10611294; http://dx.doi.org/10.1073/pnas.96.26.14807
52. Herman JG, Graff JR, Myöhänen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996; 93:9821-9826; PMID:8790415; http://dx.doi.org/10.1073/pnas.93.18.9821