Pro-neural miR-128 is a glioma tumor suppressor that targets mitogenic kinases

Oncogene

Volumn 31, Issue 15, 2012, Pages 1884-1895

  Papagiannakopoulos, T ^a   Friedmann Morvinski, D ^b   Neveu, P ^a,c   Dugas, J C ^d   Gill, R M ^a   Huillard, E ^e   Liu, C ^f   Zong, H ^f   Rowitch, D H ^e,g   Barres, B A ^d   Verma, I M ^b   Kosik, K S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF OREGON   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

EGFR; glioma stem cells; microRNA; miR 128; PDGFR

Indexed keywords

ACTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GROWTH FACTOR RECEPTOR; MICRORNA; MIRNA 128; NESTIN; PHOSPHOTRANSFERASE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEIN KINASE B; PROTEIN TUJ1; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA; HUMAN; HUMAN CELL; IN VIVO STUDY; MITOGENESIS; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR DIFFERENTIATION; TUMOR MODEL; TUMOR SUPPRESSOR GENE;

ANIMALS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; GLIOMA; HUMANS; MICE; MICE, NUDE; MICE, SCID; MICRORNAS; NEURAL STEM CELLS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA;

EID: 84859757525     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.380     Document Type: Article

References (38)

1. Bachoo RM, Maher EA, Ligon KL, Sharpless NE, Chan SS, You MJ et al. (2002). Epidermal growth factor receptor and Ink4a/Arf:convergent mechanisms governing terminal differentiationand transformation along the neural stem cell to astrocyte axis.Cancer Cell 1: 269-277. (Pubitemid 41039151)
2. Boockvar JA, Kapitonov D, Kapoor G, Schouten J, Counelis GJ, Bogler O et al. (2003). Constitutive EGFR signaling confersa motile phenotype to neural stem cells. Mol Cell Neurosci 24:1116-1130. (Pubitemid 38091521)
3. Cheng LC, Pastrana E, Tavazoie M, Doetsch F. (2009). miR-124regulates adult neurogenesis in the subventricular zone stem cellniche. Nat Neurosci 12: 399-408.
4. Ciafrè SA, Galardi S, Mangiola A, Ferracin M, Liu CG, Sabatino G et al. (2005). Extensive modulation of a set of microRNAsin primary glioblastoma. Biochem Biophys Res Commun 334:1351-1358. (Pubitemid 41074723)
5. Conaco C, Otto S, Han J-J, Mandel G. (2006). Reciprocal actions ofREST and a microRNA promote neuronal identity. Proc Natl AcadSci USA 103: 2422-2427. (Pubitemid 43271685)
6. Conti A, Aguennouz MH, La Torre D, Tomasello C, Cardali S, Angileri F et al. (2009). miR-21 and 221 upregulation and miR-181bdownregulation in human grade II-IV astrocytic tumors. J Neurooncol 93: 325-332.
7. Dai C, Celestino JC, Okada Y, Louis DN, Fuller GN, Holland EC.(2001). PDGF autocrine stimulation dedifferentiates culturedastrocytes and induces oligodendrogliomas and oligoastrocytomasfrom neural progenitors and astrocytes in vivo. Genes Dev 15:1913-1925. (Pubitemid 32738621)
8. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo J-M, Alvarez-BuyllaA. (2002). EGF converts transit-amplifying neurogenic precursorsin the adult brain into multipotent stem cells. Neuron 36: 1021-1034. (Pubitemid 36044505)
9. Filipowicz W, Bhattacharyya SN, Sonenberg N. (2008). Mechanismsof post-transcriptional regulation by microRNAs: are the answers insight? Nat Rev Genet 9: 102-114.
10. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A et al. (2007). Malignant astrocytic glioma: genetics, biology, andpaths to treatment. Genes Dev 21: 2683-2710. (Pubitemid 350070717)
11. Gangaraju VK, Lin H. (2009). MicroRNAs: key regulators of stemcells. Nat Rev Mol Cell Biol 10: 116-125.
12. Godlewski J, Nowicki MO, Bronisz A, Williams S, Otsuki A, Nuovo G et al. (2008). Targeting of the Bmi-1 oncogene/stem cellrenewal factor by microRNA-128 inhibits glioma proliferation andself-renewal. Cancer Res 68: 9125-9130.
13. Hatley ME, Patrick DM, Garcia MR, Richardson JA, Bassel-Duby R, van Rooij E et al. (2010). Modulation of K-Ras-dependent lungtumorigenesis by microRNA-21. Cancer Cell 18: 282-293.
14. Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, Rouhanifard SH et al. (2009). The PTEN-regulating microRNAmiR-26a is amplified in high-grade glioma and facilitates gliomagenesisin vivo. Genes Dev 23: 1327-1337.
15. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M, Quinones-Hinojosa A, VandenBerg S et al. (2006). PDGFR±-positive B cellsare neural stem cells in the adult SVZ that form glioma-likegrowths in response to increased PDGF signaling. Neuron 51:187-199. (Pubitemid 44063617)
16. Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS.(2003). A microRNA array reveals extensive regulation ofmicroRNAs during brain development. RNA 9: 1274-1281. (Pubitemid 37151681)
17. Krichevsky AM, Sonntag K-C, Isacson O, Kosik KS. (2006).Specific microRNAs modulate embryonic stem cell-derivedneurogenesis. Stem Cells 24: 857-864. (Pubitemid 44464719)
18. Lewis BP, Shih Ih, Jones-Rhoades MW, Bartel DP, Burge CB. (2003).Prediction of mammalian microRNA targets. Cell 115: 787-798. (Pubitemid 38058492)
19. Liu C, Sage JC, Miller MR, Verhaak RG, Hippenmeyer S, Vogel H et al. (2011). Mosaic analysis with double markers reveals tumor cellof origin in glioma. Cell 146: 209-221.
20. Liu T, Papagiannakopoulos T, Puskar K, Qi S, Santiago F, Clay W et al. (2007). Detection of a microRNA signal in an in vivoexpression set of mRNAs. PLoS One 2: e804.
21. 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)
22. Marumoto T, Tashiro A, Friedmann-Morvinski D, Scadeng M, Soda Y, Gage FH et al. (2009). Development of a novel mouseglioma model using lentiviral vectors. Nat Med 15: 110-116.
23. Mukasa A, Wykosky J, Ligon KL, Chin L, Cavenee WK, Furnari F.(2010). Mutant EGFR is required for maintenance of gliomagrowth in vivo, and its ablation leads to escape from receptordependence. Proc Natl Acad Sci 107: 2616-2621.
24. : Network TCGA (2008). Comprehensive genomic characterizationdefines human glioblastoma genes and core pathways. Nature 455:1061-1068.
25. Neveu P, Kye MJ, Qi S, Buchholz DE, Clegg DO, Sahin M et al.(2010). MicroRNA profiling reveals two distinct p53-related humanpluripotent stem cell states. Cell Stem Cell 7: 671-681.
26. Papagiannakopoulos T, Shapiro A, Kosik KS. (2008). MicroRNA-21targets a network of key tumor-suppressive pathways in glioblastomacells. Cancer Res 68: 8164-8172.
27. Piccirillo SGM, Reynolds BA, Zanetti N, Lamorte G, Binda E, BroggiG et al. (2006). Bone morphogenetic proteins inhibit the tumorigenicpotential of human brain tumour-initiating cells. Nature 444:761-765. (Pubitemid 44949605)
28. Shih AH, Dai C, Hu X, Rosenblum MK, Koutcher JA, Holland EC.(2004). Dose-dependent effects of platelet-derived growth factor-Bon glial tumorigenesis. Cancer Res 64: 4783-4789. (Pubitemid 38924521)
29. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T et al.(2004). Identification of human brain tumour initiating cells. Nature432: 396-401. (Pubitemid 39551674)
30. Stiles CD, Rowitch DH. (2008). Glioma stem cells: a midterm exam.Neuron 58: 832-846. (Pubitemid 351842757)
31. Sugahara KN, Teesalu T, Karmali PP, Kotamraju VR, Agemy L, Greenwald DR et al. (2010). Coadministration of a tumorpenetratingpeptide enhances the efficacy of cancer drugs. Science328: 1031-1035.
32. Verhaak RGW, Hoadley KA, Purdom E, Wang V, Qi Y, WilkersonMD et al. (2010). Integrated genomic analysis identifies clinically relevantsubtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17: 98-110.
33. Visvanathan J, Lee S, Lee B, Lee JW, Lee S-K. (2007). The microRNAmiR-124 antagonizes the anti-neural REST/SCP1 pathway duringembryonic CNS development. Genes Dev 21: 744-749. (Pubitemid 46572354)
34. Wuchty S, Arjona D, Li AG, Kotliarov Y, Walling J, Ahn S et al.(2011). Prediction of associations between microRNAs and geneexpression in glioma biology. PLoS One 6: e14681.
35. Xu N, Papagiannakopoulos T, Pan GJ, Thomson JA, Kosik KS. (2009).MicroRNA-145 regulates OCT4, SOX2, and KLF4 and repressespluripotency in human embryonic stem cells. Cell 137: 647-658.
36. Zhang Y, Chao T, Li R, Liu W, Chen Y, Yan X et al. (2009).MicroRNA-128 inhibits glioma cells proliferation by targetingtranscription factor E2F3a. J Mol Med 87: 43-51.
37. Zhang Y, Zhang Y-f, Bryant J, Charles A, Boado RJ, Pardridge WM.(2004). Intravenous RNA interference gene therapy targeting thehuman epidermal growth factor receptor prolongs survival inintracranial brain cancer. Clin Cancer Res 10: 3667-3677. (Pubitemid 38697600)
38. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen A-J et al. (2008). p53 and Pten control neural and gliomastem/progenitor cell renewal and differentiation. Nature 455:1129-1133.