Downregulation of miR-452 promotes stem-like traits and tumorigenicity of gliomas

Clinical Cancer Research

Volumn 19, Issue 13, 2013, Pages 3429-3438

  Liu, Liping ^a   Chen, Kun ^b   Wu, Jueheng ^c   Shi, Ling ^a   Hu, Bo ^d   Cheng, Shiyuan ^d   Li, Mengfeng ^c   Song, Libing ^a  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; BREAST CANCER RESISTANCE PROTEIN; KRUPPEL LIKE FACTOR 4; LYMPHOID ENHANCER FACTOR 1; MICRORNA; MICRORNA 452; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN TCF4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; MIRN452 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GRADING; CARCINOGENESIS; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENETIC TRAIT; GLIOMA; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SHORT TANDEM REPEAT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; TUMOR XENOGRAFT; CANCER STEM CELL; CELL TRANSFORMATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORTALITY; PROGNOSIS; QUANTITATIVE TRAIT; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DNA METHYLATION; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; MICRORNAS; NEOPLASTIC STEM CELLS; PROGNOSIS; PROMOTER REGIONS, GENETIC; QUANTITATIVE TRAIT, HERITABLE;

EID: 84879869302     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-3794     Document Type: Article

References (42)

1. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007;21:2683-710. (Pubitemid 350070717)
2. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007;114:97-109. (Pubitemid 47103521)
3. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96. (Pubitemid 40349501)
4. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008;40:499-507. (Pubitemid 351601215)
5. O'Brien CA, Kreso A, Jamieson CH. Cancer stem cells and self-renewal. Clin Cancer Res 2010;16:3113-20.
6. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008;8:755-68.
7. Yu CC, Lo WL, Chen YW, Huang PI, Hsu HS, Tseng LM, et al. Bmi-1 regulates Snail expression and promotes metastasis ability in head and neck squamous cancer-derived ALDH1 positive cells. J Oncol 2011;2011.
8. Chiba T, Seki A, Aoki R, Ichikawa H, Negishi M, Miyagi S, et al. Bmi1 promotes hepatic stem cell expansion and tumorigenicity in both Ink4a/Arf-dependent and -independent manners in mice. Hepatology 2010;52:1111-23.
9. Abdouh M, Facchino S, Chatoo W, Balasingam V, Ferreira J, Bernier G. BMI1 sustains human glioblastoma multiforme stem cell renewal. J Neurosci 2009;29:8884-96.
10. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003;423:255-60. (Pubitemid 40852690)
11. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005;434:843-50. (Pubitemid 40558990)
12. Zhang N, Wei P, Gong A, Chiu WT, Lee HT, Colman H, et al. FoxM1 promotes beta-catenin nuclear localization and controls Wnt targetgene expression and glioma tumorigenesis. Cancer Cell 2011;20:427-42.
13. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281-97.
14. Park DM, Rich JN. Biology of glioma cancer stem cells. Mol Cells 2009;28:7-12.
15. Zhang Y, Dutta A, Abounader R. The role of microRNAs in glioma initiation and progression. Front Biosci 2012;17:700-12.
16. Xia H, Cheung WK, Ng SS, Jiang X, Jiang S, Sze J, et al. Loss of brain-enriched miR-124 microRNA enhances stem-like traits and invasiveness of glioma cells. J Biol Chem 2012;287:9962-71.
17. Lavon I, Zrihan D, Granit A, Einstein O, Fainstein N, Cohen MA, et al. Gliomas display a microRNA expression profile reminiscent of neural precursor cells. Neuro Oncol 2010;12:422-33.
18. Sheehy NT, Cordes KR, White MP, Ivey KN, Srivastava D. The neural crest-enriched microRNA miR-452 regulates epithelial-mesenchymal signaling in the first pharyngeal arch. Development 2010;137:4307-16.
19. Bruna A, Darken RS, Rojo F, Ocana A, Penuelas S, Arias A, et al. High TGFbeta-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene. Cancer Cell 2007;11:147-60. (Pubitemid 46209848)
20. Li J, Zhang N, Song LB, Liao WT, Jiang LL, Gong LY, et al. Astrocyte elevated gene-1 is a novel prognostic marker for breast cancer progression and overall patient survival. Clin Cancer Res 2008;14:3319-26.
21. Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, Gudas LJ, et al. Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 2009;18:1093-108.
22. Wang Y, Lee CG. Role of miR-224 in hepatocellular carcinoma: a tool for possible therapeutic intervention? Epigenomics 2011;3:235-43.
23. Zhao J, Liang Q, Cheung KF, Kang W, Lung RW, Tong JH, et al. Genome-wide identification of Epstein-Barr virus-driven promoter methylation profiles of human genes in gastric cancer cells. Cancer 2012;119:304-12.
24. Maekawa R, Yagi S, Ohgane J, Yamagata Y, Asada H, Tamura I, et al. Disease-dependent differently methylated regions (D-DMRs) of DNA are enriched on the X chromosome in uterine leiomyoma. J Reprod Dev 2011;57:604-12.
25. Molofsky AV, He S, Bydon M, Morrison SJ, Pardal R. Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev 2005;19:1432-7. (Pubitemid 41003009)
26. Park IK, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL, et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003;423:302-5. (Pubitemid 40852701)
27. Li J, Gong LY, Song LB, Jiang LL, Liu LP, Wu J, et al. Oncoprotein Bmi-1 renders apoptotic resistance to glioma cells through activation of the IKK-nuclear factor-kappaB Pathway. Am J Pathol 2010;176:699-709.
28. Bruggeman SW, Hulsman D, Tanger E, Buckle T, Blom M, Zevenhoven J, et al. Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma. Cancer Cell 2007;12:328-41. (Pubitemid 47539307)
29. Marson A, Foreman R, Chevalier B, Bilodeau S, Kahn M, Young RA, et al. Wnt signaling promotes reprogramming of somatic cells to pluripotency. Cell Stem Cell 2008;3:132-5.
30. Nusse R, Fuerer C, Ching W, Harnish K, Logan C, Zeng A, et al. Wnt signaling and stem cell control. Cold Spring Harb Symp Quant Biol 2008;73:59-66.
31. Nusse R. Wnt signaling and stem cell control. Cell Res 2008;18:523-7. (Pubitemid 351630946)
32. Fang X, Yoon JG, Li L, Yu W, Shao J, Hua D, et al. The SOX2 response program in glioblastoma multiforme: an integrated ChIP-seq, expression microarray, and microRNA analysis. BMC Genomics 2011;12:11.
33. Nagy C, Turecki G. Sensitive periods in epigenetics: bringing us closer to complex behavioral phenotypes. Epigenomics 2012;4:445-57.
34. Teodoridis JM, Strathdee G, Brown R. Epigenetic silencing mediated by CpG island methylation: potential as a therapeutic target and as a biomarker. Drug Resist Updat 2004;7:267-78. (Pubitemid 39469099)
35. Suzuki H, Maruyama R, Yamamoto E, Kai M. DNA methylation and microRNA dysregulation in cancer. Mol Oncol 2012;6:567-78.
36. Lee YM, Chen HW, Maurya PK, Su CM, Tzeng CR. MicroRNA regulation via DNA methylation during the morula to blastocyst transition in mice. Mol Hum Reprod 2012;18:184-93.
37. van Schooneveld E, Wouters MC, Van der Auwera I, Peeters DJ, Wildiers H, Van Dam PA, et al. Expression profiling of cancerous and normal breast tissues identi fies microRNAs that are differentially expressed in serum from patients with (metastatic) breast cancer and healthy volunteers. Breast Cancer Res 2012;14:R34.
38. Wang Y, Toh HC, Chow P, Chung AYF, Meyers DJ, Cole PA, et al. MicroRNA-224 is up-regulated in hepatocellular carcinoma through epigenetic mechanisms. FASEB J 2012;26:3032-41.
39. Veerla S, Lindgren D, Kvist A, Frigyesi A, Staaf J, Persson H, et al. MiRNA expression in urothelial carcinomas: important roles of miR-10a, miR-222, miR-125b, miR-7 and miR-452 for tumor stage and metastasis, and frequent homozygous losses of miR-31. Int J Cancer 2009;124:2236-42.
40. Betel D, Koppal A, Agius P, Sander C, Leslie C. Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol 2010;11:R90.
41. Arnold CP, Tan R, Zhou B, Yue SB, Schaffert S, Biggs JR, et al. MicroRNA programs in normal and aberrant stem and progenitor cells. Genome Res 2011;21:798-810.
42. Kim TM, Huang W, Park R, Park PJ, Johnson MD. A developmental taxonomy of glioblastoma de fined and maintained by MicroRNAs. Cancer Res 2011;71:3387-99.