Tumor-suppressive miR148a is silenced by CpG island hypermethylation in IDH1-mutant gliomas

Clinical Cancer Research

Volumn 20, Issue 22, 2014, Pages 5808-5822

  Li, Sichen ^a   Chowdhury, Reshmi ^a   Liu, Fei ^a   Chou, Arthur P ^a   Li, Tie ^a   Mody, Reema R ^a   Lou, Jerry J ^a   Chen, Weidong ^a   Reiss, Jean ^b   Soto, Horacio ^a   Prins, Robert ^a   Liau, Linda M ^a   Mischel, Paul S ^c   Nghiemphu, Phioanh L ^a   Yong, William H ^b   Cloughesy, Timothy F ^a   Lai, Albert ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 1; ISOCITRATE DEHYDROGENASE 1; ISOCITRATE DEHYDROGENASE 2; MICRORNA; MICRORNA 148A; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; IDH1 PROTEIN, HUMAN; ISOCITRATE DEHYDROGENASE; MIRN148 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER PROGNOSIS; CANCER SURVIVAL; CELL CYCLE S PHASE; CELL MIGRATION; CELL PROLIFERATION; CHROMOSOME 7; CIDEB GENE; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; DLC1 GENE; DNA METHYLATION; DNMT1 GENE; DOWN REGULATION; G1 PHASE CELL CYCLE CHECKPOINT; GENE; GENE EXPRESSION REGULATION; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GLIOMA; HUMAN; HUMAN TISSUE; IDH1 GENE; IDH2 GENE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OVERALL SURVIVAL; PROTEIN EXPRESSION; RBP1 GENE; UPREGULATION; ANIMAL; BRAIN TUMOR; CLUSTER ANALYSIS; COHORT ANALYSIS; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE SILENCING; GENETICS; MORTALITY; MUTATION; PATHOLOGY; PROGNOSIS; TUMOR CELL LINE; TUMOR VOLUME; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CLUSTER ANALYSIS; COHORT STUDIES; CPG ISLANDS; DISEASE MODELS, ANIMAL; DNA METHYLATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GLIOMA; HETEROGRAFTS; HUMANS; ISOCITRATE DEHYDROGENASE; MICRORNAS; MUTATION; PROGNOSIS; TUMOR BURDEN;

EID: 84916928230     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-0234     Document Type: Article

References (50)

1. Behin A, Hoang-Xuan K, Carpentier AF, Delattre JY. Primary brain tumours in adults. Lancet 2003;361:323-31.
2. Ohgaki H, Kleihues P. The definition of primary and secondary glioblastoma. Clin Cancer Res 2013;19:764-72.
3. Lai A, Kharbanda S, Pope WB, Tran A, Solis OE, Peale F, et al. Evidence for sequenced molecular evolution of IDH1 mutant glioblastoma from a distinct cell of origin. J Clin Oncol 2011;29:4482-90.
4. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008;321:1807-12.
5. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010;17: 510-22.
6. Chou AP, Chowdhury R, Li S, Chen W, Kim AJ, Piccioni DE, et al. Identification of retinol binding protein 1 promoter hypermethylation in isocitrate dehydrogenase 1 and 2 mutant gliomas. J Natl Cancer Inst 2012;104:1458-69.
7. Turcan S, Rohle D, Goenka A, Walsh LA, Fang F, Yilmaz E, et al. IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 2012;483:479-83.
8. Duncan CG, Barwick BG, Jin G, Rago C, Kapoor-Vazirani P, Powell DR, et al. A heterozygous IDH1R132H/WT mutation induces genome-wide alterations in DNA methylation. Genome Res 2012; 22:2339-55.
9. Pirozzi CJ, Reitman ZJ, Yan H. Releasing the block: setting differentiation free with mutant IDH inhibitors. Cancer Cell 2013;23: 570-2.
10. Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A. Preparation of reduced representation bisulfite sequencing libraries for genomescale DNA methylation profiling. Nat Protoc 2011;6:468-81.
11. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281-97.
12. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005;433:769-73.
13. Iorio MV, Croce CM. MicroRNAs in cancer: small molecules with a huge impact. J Clin Oncol 2009;27:5848-56.
14. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006;6:857-66.
15. Lujambio A, Lowe SW. The microcosmos of cancer. Nature 2012; 482:347-55.
16. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, et al. MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 2008;28: 5369-80.
17. Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, Rouhanifard SH, et al. The PTEN-regulating microRNA miR-26a is ampli fied in highgrade glioma and facilitates gliomagenesis in vivo. Genes Dev 2009;23:1327-37.
18. Moller HG, Rasmussen AP, Andersen HH, Johnsen KB, Henriksen M, Duroux M. A systematic review of microRNA in glioblastoma multiforme: micro-modulators in the mesenchymal mode of migration and invasion. Mol Neurobiol 2013;47:131-44.
19. Shiota K, Takahashi M, Masaki T, Sudo K. Calcium metabolism, serum thyroid-stimulating hormone, prolactin, and growth hormone in spontaneously hypercholesterolemic rats. Proc Soc Exp Biol Med 1989; 190:229-33.
20. Formosa A, Lena AM, Markert EK, Cortelli S, Miano R, Mauriello A, et al. DNA methylation silences miR-132 in prostate cancer. Oncogene 2013;32:127-34.
21. Mazar J, DeBlasio D, Govindarajan SS, Zhang S, Perera RJ. Epigenetic regulation of microRNA-375 and its role in melanoma development in humans. FEBS Lett 2011;585:2467-76.
22. Wilting SM, van Boerdonk RA, Henken FE, Meijer CJ, Diosdado B, Meijer GA, et al. Methylation-mediated silencing and tumour suppressive function of hsa-miR-124 in cervical cancer. Mol Cancer 2010;9: 167.
23. Li S, Chou AP, Chen W, Chen R, Deng Y, Phillips HS, et al. Overexpression of isocitrate dehydrogenase mutant proteins renders glioma cells more sensitive to radiation. Neuro Oncol 2013;15:57-68.
24. Lalezari S, Chou AP, Tran A, Solis OE, Khanlou N, Chen W, et al. Combined analysis of O6-methylguanine-DNA methyltransferase protein expression and promoter methylation provides optimized prognostication of glioblastoma outcome. Neuro Oncol 2013;15: 370-81.
25. Storey JD. A direct approach to false discovery rates. J R Stat Soc B 2002;64:479-98.
26. Kozomara A, Grif fiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011;39:D152-7.
27. Gardinergarden M, Frommer M. Cpg islands in vertebrate genomes. J Mol Biol 1987;196:261-82.
28. Knudsen S. Promoter2.0: for the recognition of PolII promoter sequences. Bioinformatics 1999;15:356-61.
29. Borodovsky A, Salmasi V, Turcan S, Fabius AW, Baia GS, Eberhart CG, et al. 5-Azacytidine reduces methylation, promotes differentiation and induces tumor regression in a patient-derived IDH1 mutant glioma xenograft. Oncotarget 2013;4:1737-47.
30. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 2007;27:91-105.
31. Xu Q, Jiang Y, Yin Y, Li Q, He J, Jing Y, et al. A regulatory circuit of miR-148a/152 and DNMT1 in modulating cell transformation and tumor angiogenesis through IGF-IR and IRS1. J Mol Cell Biol 2013; 5:3-13.
32. Zhu A, Xia J, Zuo J, Jin S, Zhou H, Yao L, et al. MicroRNA-148a is silenced by hypermethylation and interacts with DNA methyltransferase 1 in gastric cancer. Med Oncol 2012;29:2701-9.
33. Pan W, Zhu S, Yuan M, Cui H, Wang L, Luo X, et al. MicroRNA-21 and microRNA-148a contribute to DNA hypomethylation in lupus CD4+T cells by directly and indirectly targeting DNA methyltransferase 1. J Immunol 2010;184:6773-81.
34. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are micro- RNA targets. Cell 2005;120:15-20.
35. Kutay H, Klepper C, Wang B, Hsu SH, Datta J, Yu L, et al. Reduced susceptibility of DNA methyltransferase 1 hypomorphic (Dnmt1N/+) mice to hepatic steatosis upon feeding liquid alcohol diet. PLoS ONE 2012;7:e41949.
36. Silber J, Lim DA, Petritsch C, Persson AI, Maunakea AK, Yu M, et al. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med 2008;6:14.
37. Wong KY, Yim RL, So CC, Jin DY, Liang R, Chim CS. Epigenetic inactivation of the MIR34B/C in multiple myeloma. Blood 2011; 118:5901-4.
38. Hanoun N, Delpu Y, Suriawinata AA, Bournet B, Bureau C, Selves J, et al. The silencing of microRNA 148a production by DNA hypermethylation is an early event in pancreatic carcinogenesis. Clin Chem 2010;56:1107-18.
39. Takahashi M, Cuatrecasas M, Balaguer F, Hur K, Toiyama Y, Castells A, et al. The clinical significance of MiR-148a as a predictive biomarker in patients with advanced colorectal cancer. PLoS ONE 2012;7: e46684.
40. Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, Blanco D, et al. A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci U S A 2008;105: 13556-61.
41. Gort EH, Suijkerbuijk KP, Roothaan SM, Raman V, Vooijs M, van der Wall E, et al. Methylation of the TWIST1 promoter, TWIST1 mRNA levels, and immunohistochemical expression of TWIST1 in breast cancer. Cancer Epidemiol Biomarkers Prev 2008;17: 3325-30.
42. Caldeira JR, Prando EC, Quevedo FC, Neto FA, Rainho CA, Rogatto SR. CDH1 promoter hypermethylation and E-cadherin protein expression in infi ltrating breast cancer. BMC Cancer 2006;6:48.
43. Zheng B, Liang L, Wang C, Huang S, Cao X, Zha R, et al. MicroRNA-suppresses tumor cell invasion and metastasis by downregulating ROCK1 in gastric cancer. Clin Cancer Res 2011;17: 7574-83.
44. Jurkowska RZ, Jurkowski TP, Jeltsch A. Structure and function of mammalian DNA methyltransferases. Chembiochem 2011;12: 206-22.
45. Xu F, Mao C, Ding Y, Rui C,Wu L, Shi A, et al. Molecular and enzymatic profi les of mammalian DNA methyltransferases: structures and targets for drugs. Curr Med Chem 2010;17:4052-71.
46. Dudley KJ, Revill K, Whitby P, Clayton RN, Farrell WE. Genome-wide analysis in a murine Dnmt1 knockdown model identifies epigenetically silenced genes in primary human pituitary tumors. Mol Cancer Res 2008;6:1567-74.
47. Rohle D, Popovici-Muller J, Palaskas N, Turcan S, Grommes C, Campos C, et al. An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells. Science 2013;340: 626-30.
48. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A, et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 2010;18:553-67.
49. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim SH, et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate- dependent dioxygenases. Cancer Cell 2011;19: 17-30.
50. Turcan S, Fabius AW, Borodovsky A, Pedraza A, Brennan C, Huse J, et al. Efficient induction of differentiation and growth inhibition in IDH1 mutant glioma cells by the DNMT inhibitor decitabine. Oncotarget 2013;4:1729-36.